Advertisement

Current Systematics of Rhizobia

  • En Tao Wang
Chapter

Abstract

In the investigation of rhizobia, research on diversity forms a basis for studies of other kinds, since diversity studies offer characterised strains that serve as resource for further studies of taxonomy, genetics, biochemistry, evolution, ecology, application and so on. In general, biodiversity includes diversity at three levels: genetic, species and ecosystem. Among these three levels, diversity of species is closely related to the methods or criteria for species definition. In the past century, criteria for definition of bacterial species have changed depending on the development of biological and computer sciences, which also affected the taxonomy of rhizobia. The definition of rhizobial species was at one time based on the host specificity of rhizobial strains (1932–1982) (Fred et al. 1932); on numerical taxonomy and DNA-DNA or DNA-RNA relatedness (1980s–1990s) (Chen et al. 1988; Dreyfus et al. 1988; Jordan 1982); on phylogeny of the 16S rRNA gene combined with numerical taxonomy and DNA-DNA relatedness (Chen et al. 1995; Young et al. 1991); on polyphasic characterisation and multilocus sequence analysis (de Lajudie et al. 1994; Martens et al. 2007); and most recently on genome analysis (Román-Ponce et al. 2016; Wang et al. 2016a). With the addition and shifting of methods, the system of rhizobial taxonomy has been greatly improved, while the species definition is more related to their evolutionary relationships.

References

  1. Agius F, Sanguinetti C, Monza J. Strain-specific fingerprints of Rhizobium loti generated by PCR with arbitrary and repetitive sequences. FEMS Microbiol Ecol. 1997;24(1):87–92.CrossRefGoogle Scholar
  2. Aguilar A, Peralta H, Mora Y, Díaz R, Vargas-Lagunas C, Girard L, Mora J. Genomic comparison of Agrobacterium pusense strains isolated from bean nodules. Front Microbiol. 2017;7:1720.Google Scholar
  3. Ahnia H, Bourebaba Y, Durán D, Boulila F, Palacios JM, Rey L, Ruiz-Argüeso T, Boulila A, Imperial J. Bradyrhizobium algeriense sp. nov., a novel species isolated from effective nodules of Retama sphaerocarpafrom Northeastern Algeria. Syst Appl Microbiol. 2018;41(4):333–9.PubMedCrossRefGoogle Scholar
  4. Allen EK, Allen ON. Biochemical and symbiotic properties of the rhizobia. Bacteriol Rev. 1950;14:273–330.PubMedPubMedCentralGoogle Scholar
  5. Amarger N, Macheret V, Laguerre G. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int J Syst Bacteriol. 1997;47(4):996–1006.CrossRefGoogle Scholar
  6. An DS, Im WT, Yang HC, Lee ST. Shinella granuli gen. nov., sp. nov., and proposal of the reclassification of Zoogloea ramigera ATCC 19623 as Shinella zoogloeoides sp. nov. Int J Syst Evol Microbiol. 2006;56(2):443–8.PubMedCrossRefGoogle Scholar
  7. Andrews M, De Meyer S, James EK, Stępkowski T, Hodge S, Simon MF, Young JPW. Horizontal transfer of symbiosis genes within and between rhizobial genera: occurrence and importance. Genes (Basel). 2018;9(7):E321.CrossRefGoogle Scholar
  8. Araújo WL, Santos DS, Dini-Andreote F, Salgueiro-Londoño JK, Camargo-Neves AA, Andreote FD, Dourado MN. Genes related to antioxidant metabolism are involved in Methylobacterium mesophilicum-soybean interaction. Antonie Van Leeuwenhoek. 2015;108(4):951–63.PubMedCrossRefGoogle Scholar
  9. Araújo J, Flores-Félix JD, Igual JM, Peix A, González-Andrés F, Díaz-Alcántara CA, Velázquez E. Bradyrhizobium cajani sp. nov. isolated from nodules of Cajanus cajan. Int J Syst Evol Microbiol. 2017;67(7):2236–41.PubMedCrossRefGoogle Scholar
  10. Ardley JK, O'Hara GW, Reeve WG, Yates RJ, Dilworth MJ, Tiwari RP, Howieson JG. Root nodule bacteria isolated from South African Lotononis bainesii, L. listii and L. solitudinis are species of Methylobacterium that are unable to utilize methanol. Arch Microbiol. 2009;191(4):311–8.PubMedCrossRefGoogle Scholar
  11. Ardley JK, Parker MA, De Meyer SE, Trengove RD, O'Hara GW, Reeve WG, Yates RJ, Dilworth MJ, Willems A, Howieson JG. Microvirga lupini sp. nov., Microvirga lotononidis sp. nov. and Microvirga zambiensis sp. nov. are alphaproteobacterial root-nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int J Syst Evol Microbiol. 2012;62(11):2579–88.PubMedCrossRefGoogle Scholar
  12. Arora N. Sinorhizobium indiaense sp. nov. and Sinorhizobium abri sp. nov. isolated from tropical legumes, Sesbania rostrata and Abrus precatorius, respectively. Symbiosis. 2003;34:53–98.Google Scholar
  13. Aserse AA, Woyke T, Kyrpides NC, Whitman WB, Lindström K. Draft genome sequence of type strain HBR26T and description of Rhizobium aethiopicum sp. nov. Stand Genomic Sci. 2017a;12:14.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Aserse AA, Woyke T, Kyrpides NC, Whitman WB, Lindström K. Draft genome sequences of Bradyrhizobium shewense sp. nov. ERR11T and Bradyrhizobium yuanmingense CCBAU 10071T. Stand Genomic Sci. 2017b;12:74.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bala A, Giller KE. Relationships between rhizobial diversity and host legume nodulation and nitrogen fixation in tropical ecosystems. Nutr Cycl Agroecosyst. 2006;76:319–30.CrossRefGoogle Scholar
  16. Baraúna AC, Rouws LF, Simoes-Araujo JL, Dos Reis Junior FB, Iannetta PP, Maluk M, Goi SR, Reis VM, James EK, Zilli JE. Rhizobium altiplani sp. nov., isolated from effective nodules on Mimosa pudica growing in untypically alkaline soil in central Brazil. Int J Syst Evol Microbiol. 2016;66(10):4118–24.PubMedCrossRefGoogle Scholar
  17. Behrendt U, Kämpfer P, Glaeser SP, Augustin J, Ulrich A. Characterization of the N2O-producing soil bacterium Rhizobium azooxidifex sp. nov. Int J Syst Evol Microbiol. 2016;66(6):2354–61.PubMedCrossRefGoogle Scholar
  18. Berge O, Lodhi A, Brandelet G, Santaella C, Roncato MA, Christen R, Heulin T, Achouak W. Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. Int J Syst Evol Microbiol. 2009;59(2):367–72.PubMedCrossRefGoogle Scholar
  19. Beringer JE. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol. 1974;84:188–98.PubMedGoogle Scholar
  20. Beyhaut E, Tlusty B, van Berkum P, Graham PH. Rhizobium giardinii is the microsymbiont of Illinois bundleflower (Desmanthus illinoensis (Michx.) Macmillan) in midwestern prairies. Can J Microbiol. 2006;52(9):903–7.PubMedCrossRefGoogle Scholar
  21. Bibi F, Chung EJ, Khan A, Jeon CO, Chung YR. Rhizobium halophytocola sp. nov., isolated from the root of a coastal dune plant. Int J Syst Evol Microbiol. 2012;62(8):1997–2003.PubMedCrossRefGoogle Scholar
  22. Binde DR, Menna P, Bangel EV, Barcellos FG, Hungria M. rep-PCR fingerprinting and taxonomy based on the sequencing of the 16S rRNA gene of 54 elite commercial rhizobial strains. Appl Microbiol Biotechnol. 2009;83(5):897–908.PubMedCrossRefGoogle Scholar
  23. Boivin C, Ndoye I, Lortet G, Ndiaye A, de Lajudie P, Dreyfus B. The Sesbania root symbionts Sinorhizobium saheli and S. teranga bv. sesbaniae can form stem nodules on Sesbania rostrata, although less adapted to stem nodulation than Azorhizobium. Appl Environ Microbiol. 1997;63:1040–7.PubMedPubMedCentralGoogle Scholar
  24. Bonaldi K, Gargani D, Prin Y, Fardoux J, Gully D, Nouwen N, Goormachtig S, Giraud E. Nodulation of Aeschynomene afraspera and A. indica by photosynthetic Bradyrhizobium sp. strain ORS285: the Nod-dependent versus the Nod-independent symbiotic interaction. Mol Plant Microbe Interact. 2011;24:1359–71.PubMedCrossRefGoogle Scholar
  25. Boonsnongcheep P, Prathanturarug S, Takahashi Y, Matsumoto A. Rhizobium puerariae sp. nov., an endophytic bacterium from the root nodules of the medicinal plant Pueraria candollei var. candollei. Int J Syst Evol Microbiol. 2016;66(3):1236–41.PubMedCrossRefGoogle Scholar
  26. Bournaud C, Moulin L, Cnockaert M, de Faria S, Prin Y, Severac D, Vandamme P. Paraburkholderia piptadeniae sp. nov. and Paraburkholderia ribeironis sp. nov., two root-nodulating symbiotic species of Piptadenia gonoacantha in Brazil. Int J Syst Evol Microbiol. 2017;67:432–40.PubMedCrossRefGoogle Scholar
  27. Bouzar H, Jones JB. Agrobacterium larrymoorei sp. nov., a pathogen isolated from aerial tumours of Ficus benjamina. Int J Syst Evol Microbiol. 2001;51:1023–6.PubMedCrossRefGoogle Scholar
  28. Cao Y, Wang E-T, Zhao L, Chen W-M, Wei G-H. Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biol Biochem. 2014;78:128–37.CrossRefGoogle Scholar
  29. Casida LE. Ensifer adhaerens gen. nov., sp. nov.: a bacterial predator of bacteria in soil. Int J Syst Bacteriol. 1982;32(3):339–45.CrossRefGoogle Scholar
  30. Celador-Lera L, Menéndez E, Peix A, Igual JM, Velázquez E, Rivas R. Rhizobium zeae sp. nov., isolated from maize (Zea mays L.) roots. Int J Syst Evol Microbiol. 2017;67(7):2306–11.PubMedCrossRefGoogle Scholar
  31. Chahboune R, Carro L, Peix A, Barrijal S, Velázquez E, Bedmar EJ. Bradyrhizobium cytisi sp. nov., isolated from effective nodules of Cytisus villosus. Int J Syst Evol Microbiol. 2011;61(12):2922–7.PubMedCrossRefGoogle Scholar
  32. Chahboune R, Carro L, Peix A, Ramírez-Bahena MH, Barrijal S, Velázquez E, Bedmar EJ. Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst Appl Microbiol. 2012;35(5):302–5.PubMedCrossRefGoogle Scholar
  33. Chaintreuil C, Perrier X, Martin G, Fardoux J, Lewis GP, Brottier L, Rivallan R, Gomez-Pacheco M, Bourges M, Lamy L, Thibaud B, Ramanankierana H, Randriambanona H, Vandrot H, Mournet P, Giraud E, Arrighi JF. Naturally occurring variations in the nod-independent model legume Aeschynomene evenia and relatives: a resource for nodulation genetics. BMC Plant Biol. 2018;18(1):54.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Chang YL, Wang JY, Wang ET, Liu HC, Sui XH, Chen WX. Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea. Int J Syst Evol Microbiol. 2011;61(10):2496–502.CrossRefGoogle Scholar
  35. Chen WX, Yan GH, Li JL. Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol. 1988;38(4):392–7.CrossRefGoogle Scholar
  36. Chen WX, Li GS, Qi YL, Wang ET, Yuan HL, Li JL. Rhizobium huakuii sp. nov. isolated from the root nodules of Astragalus sinicus. Int J Syst Bacteriol. 1991;41:275–80.CrossRefGoogle Scholar
  37. Chen WX, Wang ET, Wang SY, Li YB, Li Y. Characteristics of Rhizobium tianshanense sp. nov., a moderately and slowly growing root nodule bacterium isolated from an arid saline environment in Xinjiang, People’s Republic of China. Int J Syst Bacteriol. 1995;45:153–9.CrossRefGoogle Scholar
  38. Chen WX, Tan ZY, Gao JL, Li Y, Wang ET. Rhizobium hainanense sp. nov., isolated from tropical legumes. Int J Syst Bacteriol. 1997;47(3):870–3.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Chen LS, Figueredo A, Pedrosa FO, Hungria M. Genetic characterization of soybean rhizobia in Paraguay. Appl Environ Microbiol. 2000;66(11):5099–103.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P. Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol. 2001;51(5):1729–35.PubMedCrossRefGoogle Scholar
  41. Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C. Legume symbiotic nitrogen fixation by β -Proteobacteria is widespread in nature. J Bacteriol. 2003;185(24):7266–72.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Chen WM, de Faria SM, Straliotto R, Pitard RM, Simões-Araùjo JL, Chou JH, Chou YJ, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young JP, James EK. Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol. 2005;71(11):7461–71.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Chen WM, James EK, Coenye T, Chou JH, Barrios E, de Faria SM, Elliott GN, Sheu SY, Sprent JI, Vandamme P. Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int J Syst Evol Microbiol. 2006;56(8):1847–51.PubMedCrossRefGoogle Scholar
  44. Chen WM, de Faria SM, James EK, Elliott GN, Lin KY, Chou JH, Sheu SY, Cnockaert M, Sprent JI, Vandamme P. Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella. Int J Syst Evol Microbiol. 2007;57(5):1055–9.PubMedCrossRefGoogle Scholar
  45. Chen WM, Zhu WF, Bontemps C, Young JP, Wei GH. Mesorhizobium alhagi sp. nov., isolated from wild Alhagi sparsifolia in north-western China. Int J Syst Evol Microbiol. 2010;60(4):958–62.PubMedCrossRefGoogle Scholar
  46. Chen WM, Zhu WF, Bontemps C, Young JP, Wei GH. Mesorhizobium camelthorni sp. nov., isolated from Alhagi sparsifolia. Int J Syst Evol Microbiol. 2011;61(3):574–9.PubMedCrossRefGoogle Scholar
  47. Chen W, Sheng XF, He LY, Huang Z. Rhizobium yantingense sp. nov., a mineral-weathering bacterium. Int J Syst Evol Microbiol. 2015;65(2):412–7.PubMedCrossRefGoogle Scholar
  48. Chen L, He L-Y, Wang Q, Sheng X-F. Synergistic effects of plant growth-promoting Neorhizobium huautlense T1-17 and immobilizers on the growth and heavy metal accumulation of edible tissues of hot pepper. J Hadard Mater. 2016a;312:123–31.CrossRefGoogle Scholar
  49. Chen J, Hu M, Ma H, Wang Y, Wang ET, Zhou Z, Gu J. Genetic diversity and distribution of bradyrhizobia nodulating peanut in acid-neutral soils in Guangdong Province. Syst Appl Microbiol. 2016b;39(6):384–90.CrossRefGoogle Scholar
  50. Chen WH, Yang SH, Li ZH, Zhang XX, Sui XH, Wang ET, Chen WX, Chen WF. Ensifer shofinae sp. nov., a novel rhizobial species isolated from root nodules of soybean (Glycine max). Syst Appl Microbiol. 2017;40(3):144–9.CrossRefGoogle Scholar
  51. Choma A, Komaniecka I. The polar lipid composition of Mesorhizobium ciceri. Biochim Biophys Acta. 2003;1631:188–96.PubMedCrossRefGoogle Scholar
  52. Cordeiro AB, Ribeiro RA, Helene LCF, Hungria M. Rhizobium esperanzae sp. nov., a N2-fixing root symbiont of Phaseolus vulgaris from Mexican soils. Int J Syst Evol Microbiol. 2017;67(10):3937–45.PubMedCrossRefGoogle Scholar
  53. Crook MB, Mitra S, Ané J-M, Sadowsky MJ, Gyaneshwar P. Complete genome sequence of the Sesbania symbiont and rice growth-promoting endophyte Rhizobium sp. strain IRBG74. Genome Announc. 2013;1:e00934-13.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Crovadore J, Cochard B, Calmin G, Chablais R, Schulz T, Lefort F. Whole-genome sequence of Mesorhizobium hungaricum sp. nov. strain UASWS1009, a potential resource for agricultural and environmental uses. Genome Announc. 2016;4(5):e01158–16.PubMedPubMedCentralGoogle Scholar
  55. Cummings SP, Gyaneshwar P, Vinuesa P, Farruggia FT, Andrews M, Humphry D, Elliott GN, Nelson A, Orr C, Pettitt D, Shah GR, Santos SR, Krishnan HB, Odee D, Moreira FM, Sprent JI, Young JP, James EK. Nodulation of Sesbania species by Rhizobium (Agrobacterium) strain IRBG74 and other rhizobia. Environ Microbiol. 2009;11:2510–25.PubMedCrossRefGoogle Scholar
  56. da Silva K, De Meyer SE, Rouws LF, Farias EN, dos Santos MA, O'Hara G, Ardley JK, Willems A, Pitard RM, Zilli JE. Bradyrhizobium ingae sp. nov., isolated from effective nodules of Inga laurina grown in Cerrado soil. Int J Syst Evol Microbiol. 2014;64(10):3395–401.PubMedCrossRefGoogle Scholar
  57. Dall'Agnol RF, Ribeiro RA, Ormeño-Orrillo E, Rogel MA, Delamuta JR, Andrade DS, Martínez-Romero E, Hungria M. Rhizobium freirei sp. nov., a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. Int J Syst Evol Microbiol. 2013;63(11):4167–73.PubMedCrossRefGoogle Scholar
  58. Dall'Agnol RF, Ribeiro RA, Delamuta JR, Ormeño-Orrillo E, Rogel MA, Andrade DS, Martínez-Romero E, Hungria M. Rhizobium paranaense sp. nov., an effective N2-fixing symbiont of common bean (Phaseolus vulgaris L.) with broad geographical distribution in Brazil. Int J Syst Evol Microbiol. 2014;64(9):3222–9.PubMedCrossRefGoogle Scholar
  59. Dall’Agnol RF, Bournaud C, de Faria SM, Béna G, Moulin L, Hungria M. Genetic diversity of symbiotic Paraburkholderia species isolated from nodules of Mimosa pudica (L.) and Phaseolus vulgaris (L.) grown in soils of the Brazilian Atlantic Forest (Mata Atlântica). FEMS Microbiol Ecol. 2017;93(4)  https://doi.org/10.1093/femsec/fix027.
  60. Date RA, Hurse LS. Intrinsic antibiotic resistance and serological characterization of populations of indigenous Bradyrhizobium isolated from nodules of Desmodium intortum and Macroptilium atropurpureum in three soils of S.E. Queensland. Soil Biol Biochem. 1991;23:551–61.CrossRefGoogle Scholar
  61. de Lajudie PM, Young JPW. International committee on systematics of prokaryotes subcommittee for the taxonomy of Rhizobium and Agrobacterium: minutes of the meeting, Budapest, 25 August 2016. Int J Syst Evol Microbiol. 2017;67(7):2485–94.PubMedCrossRefGoogle Scholar
  62. de Lajudie PM, Young JPW. International committee on systematics of prokaryotes subcommittee on the taxonomy of rhizobia and agrobacteria: Minutes of the closed meeting, Granada, 4 September 2017. Int J Syst Evol Microbiol. 2018;68:3363–8.PubMedCrossRefGoogle Scholar
  63. de Lajudie PM, Young JPW. International committee on systematics of prokaryotes subcommittee for the taxonomy of rhizobia and agrobacteria: Minutes of the meeting by video conference, 11 July 2018. Int J Syst Evol Microbiol. 2019;69:1835–40.Google Scholar
  64. de Lajudie P, Willems A, Pot B, Dewettinck D, Maestrojuan G, Neyra M, Collins MD, Dreyfus B, Kersters K, Gillis M. Polyphasic taxonomy of rhizobia: Emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov. and Sinorhizobium teranga sp. nov. Int J Syst Bacteriol. 1994;44:715–33.CrossRefGoogle Scholar
  65. de Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M. Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol. 1998a;48(4):1277–90.PubMedPubMedCentralCrossRefGoogle Scholar
  66. de Lajudie P, Willems A, Nick G, Moreira F, Molouba F, Hoste B, Torck U, Neyra M, Collins MD, Lindström K, Dreyfus B, Gillis M. Characterization of tropical tree rhizobia and description of Mesorhizobium plurifarium sp. nov. Int J Syst Bacteriol. 1998b;48(2):369–82.PubMedCrossRefGoogle Scholar
  67. de Lajudie PM, Andrews M, Ardley J, Eardly B, Jumas-Bilak E, Kuzmanović N, Lassalle F, Lindström K, Mhamdi R, Martínez-Romero E, Moulin L, Mousavi SA, Nesme X, Peix A, Puławska J, Steenkamp E, Stępkowski T, Tian CF, Vinuesa P, Wei G, Willems A, Zilli J, Young P. Minimal standards for the description of new genera and species of rhizobia and agrobacteria. Int J Syst Evol Microbiol. 2019;69(7):1852–63.PubMedCrossRefGoogle Scholar
  68. De Ley J. Re-examination of the association between melting point, buoyant density, and chemical base composition of deoxyribonucleic acid. J Bacteriol. 1970;101:738–54.PubMedPubMedCentralGoogle Scholar
  69. De Ley J, Cattoir H, Reynaerts A. The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem. 1975;12:133–42.CrossRefGoogle Scholar
  70. de Matos GF, Zilli JE, de Araújo JLS, Parma MM, Melo IS, Radl V, Baldani JI, Rouws LFM. Bradyrhizobium sacchari sp. nov., a legume nodulating bacterium isolated from sugarcane roots. Arch Microbiol. 2017;199(9):1251–8.PubMedCrossRefGoogle Scholar
  71. De Meyer SE, Cnockaert M, Ardley JK, Maker G, Yates R, Howieson JG, Vandamme P. Burkholderia sprentiae sp. nov., isolated from Lebeckia ambigua root nodules. Int J Syst Evol Microbiol. 2013a;63(11):3950–7.PubMedCrossRefGoogle Scholar
  72. De Meyer SE, Cnockaert M, Ardley JK, Trengove RD, Garau G, Howieson JG, Vandamme P. Burkholderia rhynchosiae sp. nov., isolated from Rhynchosia ferulifolia root nodules. Int J Syst Evol Microbiol. 2013b;63(11):3944–9.PubMedCrossRefGoogle Scholar
  73. De Meyer SE, Cnockaert M, Ardley JK, Van Wyk BE, Vandamme PA, Howieson JG. Burkholderia dilworthii sp. nov., isolated from Lebeckia ambigua root nodules. Int J Syst Evol Microbiol. 2014;64(4):1090–5.PubMedCrossRefGoogle Scholar
  74. De Meyer SE, Tan HW, Heenan PB, Andrews M, Willems A. Mesorhizobium waimense sp. nov. isolated from Sophora longicarinata root nodules and Mesorhizobium cantuariense sp. nov. isolated from Sophora microphylla root nodules. Int J Syst Evol Microbiol. 2015;65(10):3419–26.PubMedPubMedCentralCrossRefGoogle Scholar
  75. De Meyer SE, Tan HW, Andrews M, Heenan PB, Willems A. Mesorhizobium calcicola sp. nov., Mesorhizobium waitakense sp. nov., Mesorhizobium sophorae sp. nov., Mesorhizobium newzealandense sp. nov. and Mesorhizobium kowhai sp. nov. isolated from Sophora root nodules. Int J Syst Evol Microbiol. 2016;66(2):786–95.PubMedPubMedCentralCrossRefGoogle Scholar
  76. De Meyer SE, Cnockaert M, Moulin L, Howieson JG, Vandamme P. Symbiotic and non-symbiotic Paraburkholderia isolated from South African Lebeckia ambigua root nodules and the description of Paraburkholderia fynbosensis sp. nov. Int J Syst Evol Microbiol. 2018;68(8):2607–14.PubMedCrossRefGoogle Scholar
  77. de Oliveira Cunha C, Goda Zuleta LF, Paula de Almeida LG, Prioli Ciapina L, Lustrino Borges W, Pitard RM, Baldani JI, Straliotto R, de Faria SM, Hungria M, Sousa Cavada B, Mercante FM, Ribeiro de Vasconcelos AT. Complete genome sequence of Burkholderia phenoliruptrix BR3459a (CLA1), a heat-tolerant, nitrogen-fixing symbiont of Mimosa flocculosa. J Bacteriol. 2012;194(23):6675–6.PubMedPubMedCentralCrossRefGoogle Scholar
  78. De Souza Moreira FM, Cruz L, Miana De Faria S, Marsh T, Martínez-Romero E, De Oliveira Pedrosa F, Pitat RM, Young JPW. Azorhizobium doebereinerae sp. nov. microsymbiont of Sesbania virgata (Caz.) Pers. Syst Appl Microbiol. 2006;29(3):197–206.CrossRefGoogle Scholar
  79. Degefu T, Wolde-Meskel E, Liu B, Cleenwerck I, Willems A, Frostegård Å. Mesorhizobium shonense sp. nov., Mesorhizobium hawassense sp. nov. and Mesorhizobium abyssinicae sp. nov., isolated from root nodules of different agroforestry legume trees. Int J Syst Evol Microbiol. 2013;63(5):1746–53.PubMedCrossRefGoogle Scholar
  80. Delamuta JR, Ribeiro RA, Ormeño-Orrillo E, Melo IS, Martínez-Romero E, Hungria M. Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol. 2013;63(9):3342–51.CrossRefGoogle Scholar
  81. Delamuta JR, Ribeiro RA, Ormeño-Orrillo E, Parma MM, Melo IS, Martínez-Romero E, Hungria M. Bradyrhizobium tropiciagri sp. nov. and Bradyrhizobium embrapense sp. nov., nitrogen-fixing symbionts of tropical forage legumes. Int J Syst Evol Microbiol. 2015;65(12):4424–33.PubMedCrossRefGoogle Scholar
  82. Delamuta JR, Ribeiro RA, Araújo JL, Rouws LF, Zilli JÉ, Parma MM, Melo IS, Hungria M. Bradyrhizobium stylosanthis sp. nov., comprising nitrogen-fixing symbionts isolated from nodules of the tropical forage legume Stylosanthes spp. Int J Syst Evol Microbiol. 2016;66(8):3078–87.PubMedCrossRefGoogle Scholar
  83. Diange EA, Lee SS. Rhizobium halotolerans sp. nov., Isolated from chloroethylenes contaminated soil. Curr Microbiol. 2013;66(6):599–605.PubMedCrossRefGoogle Scholar
  84. Diouf A, de Lajudie P, Neyra M, Kersters K, Gillis M, Martinez-Romero E, Gueye M. Polyphasic characterization of rhizobia that nodulate Phaseolus vulgaris in West Africa (Senegal and Gambia). Int J Syst Evol Microbiol. 2000;50:159–70.PubMedCrossRefGoogle Scholar
  85. Dobritsa AP, Samadpour M. Transfer of eleven species of the genus Burkholderia to the genus Paraburkholderia and proposal of Caballeronia gen. nov. to accommodate twelve species of the genera Burkholderia and Paraburkholderia. Int J Syst Evol Microbiol. 2016;66(8):2836–46.PubMedCrossRefGoogle Scholar
  86. Dreyfus B, Garcia L, Gillis M. Characterization of Azorhizobium caulinodans gen. nov. sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrate. Int J Syst Bacteriol. 1988;38(1):89–98.CrossRefGoogle Scholar
  87. Duodu S, Nsiah EK, Bhuvaneswari TV, Svenning MM. Genetic diversity of a natural population of Rhizobium leguminosarum biovar trifolii analysed from field nodules and by a plant infection technique. Soil Biol Biochem. 2006;38(5):1162–5.CrossRefGoogle Scholar
  88. Durán D, Rey L, Navarro A, Busquets A, Imperial J, Ruiz-Argüeso T. Bradyrhizobium valentinum sp. nov., isolated from effective nodules of Lupinus mariae-josephae, a lupine endemic of basic-lime soils in Eastern Spain. Syst Appl Microbiol. 2014a;37(5):336–41.PubMedCrossRefGoogle Scholar
  89. Durán D, Rey L, Mayo J, Zúñiga-Dávila D, Imperial J, Ruiz-Argüeso T, Martínez-Romero E, Ormeño-Orrillo E. Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of Lima bean (Phaseolus lunatus L.) in Peru. Int J Syst Evol Microbiol. 2014b;64(6):2072–8.PubMedCrossRefGoogle Scholar
  90. Eardly BD, Nour SM, van Berkum P, Selander RK. Rhizobial 16S rRNA and dnaK genes: mosaicism and the uncertain phylogenetic placement of Rhizobium galegae. Appl Environ Microb. 2005;71:1328–35.CrossRefGoogle Scholar
  91. Estrada-de los Santos P, Palmer M, Chávez-Ramírez B, Beukes C, Steenkamp ET, Briscoe L, Khan N, Maluk M, Lafos M, Humm E, Arrabit M, Crook M, Gross E, Simon MF, Dos Reis Junior FB, Whitman WB, Shapiro N, Poole PS, Hirsch AM, Venter SN, James EK. Whole genome analyses suggests that Burkholderia sensu lato contains two additional novel genera (Mycetohabitans gen. nov., and Trinickia gen. nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae. Genes. 2018;9(8):389.PubMedCentralCrossRefPubMedGoogle Scholar
  92. Fan MC, Guo YQ, Zhang LP, Zhu YM, Chen WM, Lin YB, Wei GH. Herbaspirillum robiniae sp. nov., isolated from root nodules of Robinia pseudoacacia in a lead-zinc mine. Int J Syst Evol Microbiol. 2018;68(4):1300–6.PubMedCrossRefGoogle Scholar
  93. Farrand SK, Van Berkum PB, Oger P. Agrobacterium is a definable genus of the family Rhizobiaceae. Int J Syst Evol Microbiol. 2003;53(5):1681–7.PubMedCrossRefGoogle Scholar
  94. Flores-Félix JD, Carro L, Velázquez E, Valverde Á, Cerda-Castillo E, García-Fraile P, Rivas R. Phyllobacterium endophyticum sp. nov., isolated from nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol. 2013;63(3):821–6.PubMedCrossRefGoogle Scholar
  95. Flores-Félix JD, Ramírez-Bahena MH, Salazar S, Peix A, Velázquez E. Reclassification of Arthrobacter viscosus as Rhizobium viscosum comb. nov. Int J Syst Evol Microbiol. 2017;67(6):1789–92.PubMedCrossRefGoogle Scholar
  96. Fred EB, Baldwin IL, Mc Coy E. Root nodule bacteria and Leguminous plants. In: Studies in Science, vol. 5. Madison: University of Wisconsin, Press; 1932. p. 343.Google Scholar
  97. Fu GY, Yu XY, Zhang CY, Zhao Z, Wu D, Su Y, Wang RJ, Han SB, Wu M, Sun C. Mesorhizobium oceanicum sp. nov., isolated from deep seawater. Int J Syst Evol Microbiol. 2017;67(8):2739–45.PubMedCrossRefGoogle Scholar
  98. Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, and other 50 authors. The composite genome of the legume symbiont Sinorhizobium meliloti. Science. 2001;293:668–72.PubMedCrossRefGoogle Scholar
  99. Gao JL, Sun JG, Li Y, Wang ET, Chen WX. Numerical taxonomy and DNA relatedness of tropical rhizobia isolated from Hainan Province, China. Int J Syst Bacteriol. 1994;44:151–8.CrossRefGoogle Scholar
  100. Gao J, Terefework Z, Chen W, Kristina LK. Genetic diversity of rhizobia isolated from Astragalus adsurgens growing in different geographical regions of China. J Biotechnol. 2001;91:155–68.CrossRefGoogle Scholar
  101. Gao JL, Turner SL, Kan FL, Wang ET, Tan ZY, Qiu YH, Gu J, Terefework Z, Young JP, Lindström K, Chen WX. Mesorhizobium septentrionale sp. nov. and Mesorhizobium temperatum sp. nov., isolated from Astragalus adsurgens growing in the northern regions of China. Int J Syst Evol Microbiol. 2004;54(6):2003–12.CrossRefGoogle Scholar
  102. Gao JL, Sun P, Wang XM, Lv FY, Mao XJ, Sun JG. Rhizobium wenxiniae sp. nov., an endophytic bacterium isolated from maize root. Int J Syst Evol Microbiol. 2017a;67(8):2798–803.PubMedCrossRefPubMedCentralGoogle Scholar
  103. Gao JL, Sun P, Wang XM, Lv FY, Mao XJ, Sun JG. Rhizobium wenxiniae sp. nov., an endophytic bacterium isolated from maize root. Int J Syst Evol Microbiol. 2017b;67(8):2798–803.PubMedCrossRefPubMedCentralGoogle Scholar
  104. García-Fraile P, Rivas R, Willems A, Peix A, Martens M, Martínez-Molina E, Mateos PF, Velázquez E. Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int J Syst Evol Microbiol. 2007;57(4):844–8.PubMedCrossRefPubMedCentralGoogle Scholar
  105. Garrity GM, Bell JA, Lilburn T. Family IX. Methylobacteriaceae fam. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM, editors. Bergey’s manual of systematic bacteriology, (The Proteobacteria), part C (The Alpha-, Beta-, Delta-, and Epsilonproteobacteria), vol. 2. 2nd ed. New York: Springer; 2005. p. 567.Google Scholar
  106. Ghosh W, Roy P. Mesorhizobium thiogangeticum sp. nov., a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant. Int J Syst Evol Microbiol. 2006;56(1):91–7.PubMedCrossRefPubMedCentralGoogle Scholar
  107. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, and 28 other authors. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science. 2007;316:1307–131.CrossRefGoogle Scholar
  108. Goodacre R, Hartmann A, Beringer JE, Berkeley RCW. The use of pyrolysis mass spectrometry in the characterization of Rhizobium meliloti. Lett Appl Microbiol. 1991;13:157–60.CrossRefGoogle Scholar
  109. Goris J, De Vos P, Caballero-Mellado J, Park J, Falsen E, Quensen JF 3rd, Tiedje JM, Vandamme P. Classification of the biphenyl- and polychlorinated biphenyl-degrading strain LB400T and relatives as Burkholderia xenovorans sp. nov. Int J Syst Evol Microbiol. 2004;54(5):1677–81.PubMedCrossRefPubMedCentralGoogle Scholar
  110. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol. 2007;57:81–91.CrossRefGoogle Scholar
  111. Graham PH. The application of computer tech- niques to the taxonomy of the root-nodule bacteria of legumes. J Gen Microbiol. 1964;35:511–7.CrossRefGoogle Scholar
  112. Graham PH, Sadowsky MJ, Keyser HH, Barnet YM, Bradley RS, Cooper JE, De Ley DJ, Jarvis BDW, Roslycky EB, Strijdom BW, Young JPW. Proposed minimal standards for the description of new genera and species of root- and stem-nodulating bacteria. Int J Syst Bacteriol. 1991;41(4):582–7.CrossRefGoogle Scholar
  113. Grison CM, Jackson S, Merlot S, Dobson A, Grison C. Rhizobium metallidurans sp. nov., a symbiotic heavy metal resistant bacterium isolated from the Anthyllis vulneraria Zn-hyperaccumulator. Int J Syst Evol Microbiol. 2015;65(5):1525–30.PubMedCrossRefGoogle Scholar
  114. Grönemeyer JL, Chimwamurombe P, Reinhold-Hurek B. Bradyrhizobium subterraneum sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of groundnuts. Int J Syst Evol Microbiol. 2015;65(10):3241–7.PubMedCrossRefPubMedCentralGoogle Scholar
  115. Grönemeyer JL, Hurek T, Bünger W, Reinhold-Hurek B. Bradyrhizobium vignae sp. nov., a nitrogen-fixing symbiont isolated from effective nodules of Vigna and Arachis. Int J Syst Evol Microbiol. 2016;66(1):62–9.PubMedCrossRefPubMedCentralGoogle Scholar
  116. Grönemeyer JL, Bünger W, Reinhold-Hurek B. Bradyrhizobium namibiense sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of Lablab purpureus, hyacinth bean, in Namibia. Int J Syst Evol Microbiol. 2017;67(12):4884–91.PubMedCrossRefPubMedCentralGoogle Scholar
  117. Gu CT, Wang ET, Sui XH, Chen WF, Chen WX. Diversity and geographical distribution of rhizobia associated with Lespedeza spp. in temperate and subtropical regions of China. Arch Microbiol. 2007;188(4):355–65.CrossRefGoogle Scholar
  118. Gu CT, Wang ET, Tian CF, Han TX, Chen WF, Sui XH, Chen WX. Rhizobium miluonense sp. nov., a symbiotic bacterium isolated from Lespedeza root nodules. Int J Syst Evol Microbiol. 2008;58(6):1364–8.PubMedCrossRefPubMedCentralGoogle Scholar
  119. Gu T, Sun LN, Zhang J, Sui XH, Li SP. Rhizobium flavum sp. nov., a triazophos-degrading bacterium isolated from soil under the long-term application of triazophos. Int J Syst Evol Microbiol. 2014;64(6):2017–22.PubMedCrossRefPubMedCentralGoogle Scholar
  120. Guan SH, Chen WF, Wang ET, Lu YL, Yan XR, Zhang XX, Chen WX. Mesorhizobium caraganae sp. nov., a novel rhizobial species nodulated with Caragana spp. in China. Int J Syst Evol Microbiol. 2008;58(11):2646–53.CrossRefGoogle Scholar
  121. Guerrouj K, Ruíz-Díez B, Chahboune R, Ramírez-Bahena MH, Abdelmoumen H, Quiñones MA, El Idrissi MM, Velázquez E, Fernández-Pascual M, Bedmar EJ, Peix A. Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst Appl Microbiol. 2013;36(4):218–23.PubMedCrossRefPubMedCentralGoogle Scholar
  122. Gully D, Teulet A, Busset N, Nouwen N, Fardoux J, Rouy Z, Vallenet D, Cruveiller S, Giraud E. Complete genome sequence of Bradyrhizobium sp. ORS285, a photosynthetic strain able to establish Nod factor-dependent or Nod factor-independent symbiosis with Aeschynomene legumes. Genome Announc. 2017;5(30):e00421–17.PubMedPubMedCentralCrossRefGoogle Scholar
  123. Guo HJ, Wang ET, Zhang XX, Li QQ, Zhang YM, Tian CF, Chen WX. Replicon-dependent differentiation of symbiosis-related genes in Sinorhizobium strains nodulating Glycine max. Appl Environ Microbiol. 2014;80(4):1245–55.PubMedPubMedCentralCrossRefGoogle Scholar
  124. Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de Los Santos P, Gross E, Dos Reis FB, Sprent JI, Young JP, James EK. Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe Interact. 2011;24:1276–88.PubMedCrossRefPubMedCentralGoogle Scholar
  125. Han TX, Wang ET, Wu LJ, Chen WF, Gu JG, Gu CT, Tian CF, Chen WX. Rhizobium multihospitium sp. nov., isolated from multiple legume species native of Xinjiang, China. Int J Syst Evol Microbiol. 2008a;58(7):1693–9.CrossRefGoogle Scholar
  126. Han TX, Wang ET, Han LL, Chen WF, Sui XH, Chen WX. Molecular diversity and phylogeny of rhizobia associated with wild legumes native to Xinjiang, China. Syst Appl Microbiol. 2008b;31(4):287–301.CrossRefGoogle Scholar
  127. Han TX, Han LL, Wu LJ, Chen WF, Sui XH, Gu JG, Wang ET, Chen WX. Mesorhizobium gobiense sp. nov. and Mesorhizobium tarimense sp. nov., isolated from wild legumes growing in desert soils of Xinjiang, China. Int J Syst Evol Microbiol. 2008c;58(11):2610–8.PubMedCrossRefPubMedCentralGoogle Scholar
  128. Han LL, Wang ET, Han TX, Liu J, Sui XH, Chen WF, Chen WX. Unique community structure and biogeography of soybean rhizobia in the saline-alkaline soils of Xinjiang, China. Plant and Soil. 2009;324(1-2):291–305.CrossRefGoogle Scholar
  129. Han TX, Tian CF, Wang ET, Chen WX. Associations among rhizobial chromosomal background, nod genes, and host plants based on the analysis of symbiosis of indigenous rhizobia and wild legumes native to Xinjiang. Microb Ecol. 2010;59(2):311–23.PubMedCrossRefPubMedCentralGoogle Scholar
  130. Handley BA, Hedges AJ, Beringer JE. Importance of host plants for detecting the population diversity of Rhizobium leguminosarum biovar viciae in soil. Soil Biol Biochem. 1998;30:241–9.CrossRefGoogle Scholar
  131. Harrison S, Young JPW, Jones DG. Rhizobium population genetics: effect of clover variety and inoculum dilution on the genetic diversity sampled from natural populations. Plant Soil. 1987;103:147–50.CrossRefGoogle Scholar
  132. He YR, Wang JY, Wang ET, Feng G, Chang YL, Sui XH, Chen WX. Trigonella arcuata-associated rhizobia, an Ensifer (Sinorhizobium) meliloti population adapted to the desert environment. Plant and Soil. 2011;345(1-2):89–102.CrossRefGoogle Scholar
  133. Helene LC, Delamuta JR, Ribeiro RA, Ormeño-Orrillo E, Rogel MA, Martínez-Romero E, Hungria M. Bradyrhizobium viridifuturi sp. nov., encompassing nitrogen-fixing symbionts of legumes used for green manure and environmental services. Int J Syst Evol Microbiol. 2015;65(12):4441–8.PubMedCrossRefPubMedCentralGoogle Scholar
  134. Helene LCF, Delamuta JRM, Ribeiro RA, Hungria M. Bradyrhizobium mercantei sp. nov., a nitrogen-fixing symbiont isolated from nodules of Deguelia costata (syn. Lonchocarpus costatus). Int J Syst Evol Microbiol. 2017;67(6):1827–34.PubMedCrossRefPubMedCentralGoogle Scholar
  135. Hirsch P. Blastobacter aggregatus sp. nov., Blastobacter capsulatus sp. nov., and Blastobacter denitrificans sp. nov., new budding bacteria from freshwater habitats. Syst Appl Microbiol. 1985;6(3):281–6.CrossRefGoogle Scholar
  136. Holmes B, Roberts P. The classification, identification and nomenclature of agrobacteria. J Appl Bacteriol. 1981;50(3):443–67.CrossRefGoogle Scholar
  137. Hou BC, Wang ET, Li Y Jr, Jia RZ, Chen WF, Gao Y, Dong RJ, Chen WX. Rhizobium tibeticum sp. nov., a symbiotic bacterium isolated from Trigonella archiducis-nicolai (Sirj.) Vassilcz. Int J Syst Evol Microbiol. 2009;59(12):3051–7.PubMedPubMedCentralCrossRefGoogle Scholar
  138. Hu G, Li W, Zhou J. Incompatibility behavior of a symbiotic plasmid pMH7653Rb in Mesorhizobium huakuii 7653R. Sci China Life Sci. 2010;53(6):738–42.PubMedCrossRefPubMedCentralGoogle Scholar
  139. Hunter WJ, Kuykendall LD, Manter DK. Rhizobium selenireducens sp. nov.: a selenite-reducing alpha-Proteobacteria isolated from a bioreactor. Curr Microbiol. 2007;55(5):455–60.PubMedCrossRefPubMedCentralGoogle Scholar
  140. Ibañez F, Taurian T, Angelini J, Tonelli ML, Fabra A. Rhizobia phylogenetically related to common bean symbionts Rhizobium giardinii and Rhizobium tropici isolated from peanut nodules in Central Argentina. Soil Biol Biochem. 2008;40:537–9.CrossRefGoogle Scholar
  141. Imran A, Hafeez FY, Frühling A, Schumann P, Malik KA, Stackebrandt E. Ochrobactrum ciceri sp. nov., isolated from nodules of Cicer arietinum. Int J Syst Evol Microbiol. 2010;60(7):1548–53.PubMedCrossRefPubMedCentralGoogle Scholar
  142. Islam MS, Kawasaki H, Muramatsu Y, Nakagawa Y, Seki T. Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Biosci Biotechnol Biochem. 2008;72(6):1416–29.PubMedCrossRefPubMedCentralGoogle Scholar
  143. Jaftha JB, Strijdom BW, Steyn PL. Characterization of pigmented methylotrophic bacteria which nodulate Lotononis bainesii. Syst Appl Microbiol. 2002;25(3):440–9.PubMedCrossRefPubMedCentralGoogle Scholar
  144. Jang JH, Lee D, Cha S, Seo T. Ensifer collicola sp. nov., a bacterium isolated from soil in South Korea. J Microbiol. 2017;55(7):520–4.PubMedCrossRefPubMedCentralGoogle Scholar
  145. Jarvis BDW, Dick AG, Greenwood RM. Deoxyribonucleic acid homology among strains of Rhizobium trifolii and related species. Int J Syst Bacteriol. 1980;30:42–52.CrossRefGoogle Scholar
  146. Jarvis BDW, Pankhurst CE, Patel JJ. Rhizobium loti, a new species of legume root nodule bacteria. Int J Syst Bacteriol. 1982;32:378–80.CrossRefGoogle Scholar
  147. Jarvis BDW, Van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gillis M. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol. 1997;47:895–8.CrossRefGoogle Scholar
  148. Ji Z, Yan H, Cui Q, Wang E, Chen W, Chen W. Genetic divergence and gene flow among Mesorhizobium strains nodulating the shrub legume Caragana. Syst Appl Microbiol. 2015;38(3):176–83.CrossRefGoogle Scholar
  149. Jia RZ, Gu J, Tian CF, Man CX, Wang ET, Chen WX. Screening of high effective alfalfa rhizobial strains with a comprehensive protocol. Ann Microbiol. 2008;58(4):731–40.CrossRefGoogle Scholar
  150. Jia RZ, Wang ET, Liu JH, Li Y, Gu J, Yuan HL, Chen WX. Effectiveness of different combinations among the Sinorhizobium meliloti strains and alfalfa cultivars and their influence on nodulation of native rhizobia. Soil Biol Biochem. 2013;57:960–3.CrossRefGoogle Scholar
  151. Jia RZ, Zhang RJ, Wei Q, Chen WF, Cho IK, Chen WX, Li QX. Identification and classification of rhizobia by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J Proteomics Bioinform. 2015;8:098–107.Google Scholar
  152. Jiao YS, Liu YH, Yan H, Wang ET, Tian CF, Chen WX, Guo BL, Chen WF. Rhizobial diversity and nodulation characteristics of the extremely promiscuous legume Sophora flavescens. Mol Plant Microbe Interact. 2015a;28(12):1338–52.PubMedCrossRefPubMedCentralGoogle Scholar
  153. Jiao YS, Yan H, Ji ZJ, Liu YH, Sui XH, Wang ET, Guo BL, Chen WX, Chen WF. Rhizobium sophorae sp. nov. and Rhizobium sophoriradicis sp. nov., nitrogen-fixing rhizobial symbionts of the medicinal legume Sophora flavescens. Int J Syst Evol Microbiol. 2015b;65(2):497–503.CrossRefGoogle Scholar
  154. Jiao YS, Yan H, Ji ZJ, Liu YH, Sui XH, Zhang XX, Wang ET, Chen WX, Chen WF. Phyllobacterium sophorae sp. nov., a symbiotic bacterium isolated from root nodules of Sophora flavescens. Int J Syst Evol Microbiol. 2015c;65(2):399–406.PubMedPubMedCentralCrossRefGoogle Scholar
  155. Jiao J, Ni M, Zhang B, Zhang Z, Young JPW, Chan TF, Chen WX, Lam HM, Tian CF. Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii. PLoS Genet. 2018;14(5):e1007428.PubMedPubMedCentralCrossRefGoogle Scholar
  156. Jordan DC. Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Evol Microbiol. 1982;32:136–9.Google Scholar
  157. Jordan DC. Family 111.Rhizobiaceae Conn 1938,321AL. In: Krieg NR, Holt JG, editors. Bergey’s manual of systematic bacteriology, vol. 1. Baltimore: Williams & Wilkins; 1984. p. 234–54.Google Scholar
  158. Jourand P, Giraud E, Béna G, Sy A, Willems A, Gillis M, Dreyfus B, de Lajudie P. Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Int J Syst Evol Microbiol. 2004;54(6):2269–73.PubMedCrossRefPubMedCentralGoogle Scholar
  159. Jurado V, Laiz L, Gonzalez JM, Hernandez-Marine M, Valens M, Saiz-Jimenez C. Phyllobacterium catacumbae sp. nov., a member of the order 'Rhizobiales' isolated from Roman catacombs. Int J Syst Evol Microbiol. 2005;55(4):1487–90.PubMedCrossRefPubMedCentralGoogle Scholar
  160. Kaijalainen S, Lindström K. Restriction fragment length polymorphism analysis of Rhizobium galegae strains. J Bacteriol. 1989;171(10):5561–6.PubMedPubMedCentralCrossRefGoogle Scholar
  161. Kaiya S, Rubaba O, Yoshida N, Yamada T, Hiraishi A. Characterization of Rhizobium naphthalenivorans sp. nov. with special emphasis on aromatic compound degradation and multilocus sequence analysis of housekeeping genes. J Gen Appl Microbiol. 2012;58(3):211–24.PubMedCrossRefGoogle Scholar
  162. Kanso S, Patel BK. Microvirga subterranea gen. nov., sp. nov., a moderate thermophile from a deep subsurface Australian thermal aquifer. Int J Syst Evol Microbiol. 2003;53(2):401–6.PubMedCrossRefPubMedCentralGoogle Scholar
  163. Kaur J, Verma M, Lal R. Rhizobium rosettiformans sp. nov., isolated from a hexachlorocyclohexane dump site, and reclassification of Blastobacter aggregatus Hirsch and Muller 1986 as Rhizobium aggregatum comb. nov. Int J Syst Evol Microbiol. 2011;61(5):1218–25.PubMedCrossRefPubMedCentralGoogle Scholar
  164. Kerr A, Panagopoulco GS. Biotypes of Agrobacterium radiobacter var. tumefaciens and their biological control. Phytopath Z. 1977;90:172–9.CrossRefGoogle Scholar
  165. Khalid R, Zhang YJ, Ali S, Sui XH, Zhang XX, Amara U, Chen WX, Hayat R. Rhizobium pakistanensis sp. nov., isolated from groundnut (Arachis hypogaea) nodules grown in rainfed Pothwar, Pakistan. Antonie Van Leeuwenhoek. 2015;107(1):281–90.PubMedCrossRefGoogle Scholar
  166. Kimes NE, López-Pérez M, Flores-Félix JD, Ramírez-Bahena MH, Igual JM, Peix A, Rodriguez-Valera F, Velázquez E. Pseudorhizobium pelagicum gen. nov., sp. nov. isolated from a pelagic Mediterranean zone. Syst Appl Microbiol. 2015;38(5):293–9.PubMedCrossRefPubMedCentralGoogle Scholar
  167. Kittiwongwattana C, Thawai C. Rhizobium lemnae sp. nov., a bacterial endophyte of Lemna aequinoctialis. Int J Syst Evol Microbiol. 2014;64(7):2455–60.PubMedCrossRefPubMedCentralGoogle Scholar
  168. Kuykendall LD, Saxena B, Devine TE, Udell SE. Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp. nov. Can J Microbiol. 1992;38:501–5.CrossRefGoogle Scholar
  169. Kuzmanović N, Smalla K, Gronow S, Puławska J. Rhizobium tumorigenes sp. nov., a novel plant tumorigenic bacterium isolated from cane gall tumors on thornless blackberry. Sci Rep. 2018;8(1):9051.PubMedPubMedCentralCrossRefGoogle Scholar
  170. Lagares A, Sanjuán J, Pistorio M. The plasmid mobilome of the model plant-symbiont Sinorhizobium meliloti: coming up with new questions and answers. Microbiol Spectr. 2014;2(5)  https://doi.org/10.1128/microbiolspec.PLAS-0005-2013.
  171. Laguerre G, Bardin M, Amarger N. Isolation from soil of symbiotic and nonsymbiotic Rhizobium leguminosarum by DNA hybridization. Can J Microbiol. 1993;39:1142–9.CrossRefGoogle Scholar
  172. Laguerre G, Mavingui P, Allard MR, Charnay MP, Louvrier P, Mazurier SI, Rigottier-Gois L, Amarger N. Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. Appl Environ Microbiol. 1996;62(6):2029–36.PubMedPubMedCentralGoogle Scholar
  173. Lang E, Schumann P, Adler S, Spröer C, Sahin N. Azorhizobium oxalatiphilum sp. nov., and emended description of the genus Azorhizobium. Int J Syst Evol Microbiol. 2013;63(4):1505–11.PubMedCrossRefGoogle Scholar
  174. Lapage SP, Sneath PHA, Lessel EF, Skerman VBD, Seeliger HPR, Clark WA. International Code of Nomenclature of Bacteria: Bacteriological Code, 1990 Revision. Washington, DC: ASM Press; 1992.Google Scholar
  175. Lasse Grönemeyer J, Hurek T, Reinhold-Hurek B. Bradyrhizobium kavangense sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of traditional Namibian pulses. Int J Syst Evol Microbiol. 2015;65(12):4886–94.PubMedCrossRefGoogle Scholar
  176. Lehman AP, Long SR. OxyR-dependent transcription response of Sinorhizobium meliloti to oxidative stress. J Bacteriol. 2018;200(7):e00622–17.PubMedPubMedCentralCrossRefGoogle Scholar
  177. Lemaire B, Van Cauwenberghe J, Verstraete B, Chimphango S, Stirton C, Honnay O, Smets E, Sprent J, James EK, Muasya AM. Characterization of the papilionoid-Burkholderia interaction in the Fynbos biome: The diversity and distribution of beta-rhizobia nodulating Podalyria calyptrata (Fabaceae, Podalyrieae). Syst Appl Microbiol. 2016;39(1):41–8.PubMedCrossRefGoogle Scholar
  178. León-Barrios M, Ramírez-Bahena MH, Igual JM, Peix Á, Velázquez E. Phyllobacterium salinisoli sp. nov., isolated from a Lotus lancerottensis root nodule in saline soil from Lanzarote. Int J Syst Evol Microbiol. 2018;68(4):1085–9.PubMedCrossRefGoogle Scholar
  179. Li QQ, Wang ET, Zhang YZ, Zhang YM, Tian CF, Sui XH, Chen WF, Chen WX. Diversity and biogeography of rhizobia isolated from root nodules of Glycine max grown in Hebei Province, China. Microb Ecol. 2011a;61(4):917–31.PubMedCrossRefGoogle Scholar
  180. Li QQ, Wang ET, Chang YL, Zhang YZ, Zhang YM, Sui XH, Chen WF, Chen WX. Ensifer sojae sp. nov., isolated from root nodules of Glycine max grown in saline-alkaline soils. Int J Syst Evol Microbiol. 2011b;61(8):1981–8.CrossRefGoogle Scholar
  181. Li L, Sinkko H, Montonen L, Wei G, Lindström K, Räsänen LA. Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microbiol Ecol. 2012;79:46–68.PubMedCrossRefGoogle Scholar
  182. Li YH, Wang R, Zhang XX, Young JP, Wang ET, Sui XH, Chen WX. Bradyrhizobium guangdongense sp. nov. and Bradyrhizobium guangxiense sp. nov., isolated from effective nodules of peanut. Int J Syst Evol Microbiol. 2015;65(12):4655–61.CrossRefGoogle Scholar
  183. Li Y, Wang ET, Liu Y, Li X, Yu B, Ren C, Liu W, Li Y, Xie Z. Rhizobium anhuiense as the predominant microsymbionts of Lathyrus maritimus along the Shandong Peninsula seashore line. Syst Appl Microbiol. 2016a;39(6):384–90.PubMedCrossRefGoogle Scholar
  184. Li Y, Xu Y, Liu L, Jiang X, Zhang K, Zheng T, Wang H. First evidence of bioflocculant from Shinella albus with flocculation activity on harvesting of Chlorella vulgaris biomass. Bioresour Technol. 2016b;218:807–15.PubMedCrossRefGoogle Scholar
  185. Li Y, Yan J, Yu B, Wang ET, Li X, Yan H, Liu W, Xie Z. Ensifer alkalisoli sp. nov. isolated from root nodules of Sesbania cannabina grown in saline-alkaline soils. Int J Syst Evol Microbiol. 2016c;66(12):5294–300.PubMedCrossRefGoogle Scholar
  186. Li Y, Lei X, Xu Y, Zhu H, Xu M, Fu L, Zheng W, Zhang J, Zheng T. Rhizobium albus sp. nov., isolated from lake water in Xiamen, Fujian Province of China. Curr Microbiol. 2017;74(1):42–8.PubMedCrossRefGoogle Scholar
  187. Lin DX, Wang ET, Tang H, Han TX, He YR, Guan SH, Chen WX. Shinella kummerowiae sp. nov., a symbiotic bacterium isolated from root nodules of the herbal legume Kummerowia stipulacea. Int J Syst Evol Microbiol. 2008;58(6):1409–13.PubMedCrossRefGoogle Scholar
  188. Lin DX, Chen WF, Wang FQ, Hu D, Wang ET, Sui XH, Chen WX. Rhizobium mesosinicum sp. nov., isolated from root nodules of three different legumes. Int J Syst Evol Microbiol. 2009;59(8):1919–23.PubMedCrossRefGoogle Scholar
  189. Lin SY, Hsu YH, Liu YC, Hung MH, Hameed A, Lai WA, Yen WS, Young CC. Rhizobium straminoryzae sp. nov., isolated from the surface of rice straw. Int J Syst Evol Microbiol. 2014;64(9):2962–8.PubMedCrossRefGoogle Scholar
  190. Lin SY, Hung MH, Hameed A, Liu YC, Hsu YH, Wen CZ, Arun AB, Busse HJ, Glaeser SP, Kämpfer P, Young CC. Rhizobium capsici sp. nov., isolated from root tumor of a green bell pepper (Capsicum annuum var. grossum) plant. Antonie Van Leeuwenhoek. 2015;107(3):773–84.PubMedCrossRefGoogle Scholar
  191. Lindström K. Rhizobium galegae, a new species of legume root nodule bacteria. Int J Syst Bacteriol. 1989;39:365–7.CrossRefGoogle Scholar
  192. Lindstrom K, Young JPW. International committee on systematics of prokaryotes subcommittee on the taxonomy of agrobacterium and rhizobium: minutes of the meeting, 31 August 2008 Gent, Belgium. Int J Syste Evol Microbiol. 2009;59:921–2.CrossRefGoogle Scholar
  193. Lindström K, Young JP. International Committee on Systematics of Prokaryotes Subcommittee on the taxonomy of Agrobacterium and Rhizobium: minutes of the meeting, 7 September 2010, Geneva, Switzerland. Int J Syst Evol Microbiol. 2011;61(12):3089–93.PubMedCrossRefGoogle Scholar
  194. Liu TY, Li Y Jr, Liu XX, Sui XH, Zhang XX, Wang ET, Chen WX, Chen WF, Puławska J. Rhizobium cauense sp. nov., isolated from root nodules of the herbaceous legume Kummerowia stipulacea grown in campus lawn soil. Syst Appl Microbiol. 2012;35(7):415–20.PubMedCrossRefGoogle Scholar
  195. Liu Y, Wang RP, Ren C, Lai QL, Zeng RY. Rhizobium marinum sp. nov., a malachite-green-tolerant bacterium isolated from seawater. Int J Syst Evol Microbiol. 2015;65(12):4449–54.PubMedCrossRefGoogle Scholar
  196. Lloret L, Martínez-Romero E. Evolución y filogenia de Rhizobium. Revista Latinoamer Microbiol. 2005;47(1-2):43–60.Google Scholar
  197. Lloret L, Ormeño-Orrillo E, Rincón R, Martínez-Romero J, Rogel-Hernández MA, Martínez-Romero E. Ensifer mexicanus sp. nov. a new species nodulating Acacia angustissima (Mill.) Kuntze in Mexico. Syst Appl Microbiol. 2007;30:280–90.PubMedCrossRefGoogle Scholar
  198. López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E. Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol. 2010;33(6):322–7.PubMedCrossRefGoogle Scholar
  199. López-López A, Rogel-Hernández MA, Barois I, Ortiz Ceballos AI, Martínez J, Ormeño-Orrillo E, Martínez-Romero E. Rhizobium grahamii sp. nov., from nodules of Dalea leporina, Leucaena leucocephala and Clitoria ternatea, and Rhizobium mesoamericanum sp. nov., from nodules of Phaseolus vulgaris, siratro, cowpea and Mimosa pudica. Int J Syst Evol Microbiol. 2012;62(9):2264–71.PubMedCrossRefGoogle Scholar
  200. Lorite MJ, Flores-Félix JD, Peix A, Sanjuán J, Velázquez E. Mesorhizobium olivaresii sp. nov. isolated from Lotus corniculatus nodules. Syst Appl Microbiol. 2016;39(8):557–61.PubMedCrossRefGoogle Scholar
  201. Lu YL, Chen WF, Han LL, Wang ET, Chen WX. Rhizobium alkalisoli sp. nov., isolated from Caragana intermedia growing in saline-alkaline soils in the north of China. Int J Syst Evol Microbiol. 2009a;59:3006–11.CrossRefGoogle Scholar
  202. Lu YL, Chen WF, Wang ET, Han LL, Zhang XX, Chen WX, Han SZ. Mesorhizobium shangrilense sp. nov., isolated from root nodules of Caragana species. Int J Syst Evol Microbiol. 2009b;59(12):3012–8.CrossRefGoogle Scholar
  203. Lu JK, Dou YJ, Zhu YJ, Wang SK, Sui XH, Kang LH. Bradyrhizobium ganzhouense sp. nov., an effective symbiotic bacterium isolated from Acacia melanoxylon R. Br. nodules. Int J Syst Evol Microbiol. 2014;64(6):1900–5.PubMedPubMedCentralCrossRefGoogle Scholar
  204. Madhaiyan M, Poonguzhali S, Senthilkumar M, Sundaram S, Sa T. Nodulation and plant-growth promotion by methylotrophic bacteria isolated from tropical legumes. Microbiol Res. 2009;164(1):114–20.PubMedCrossRefPubMedCentralGoogle Scholar
  205. Man CX, Wang H, Chen WF, Sui XH, Wang ET, Chen WX. Diverse rhizobia associated with soybean grown in the subtropical and tropical regions of China. Plant Soil. 2008;310(1):77–87.CrossRefGoogle Scholar
  206. Mantelin S, Saux MF, Zakhia F, Béna G, Bonneau S, Jeder H, de Lajudie P, Cleyet-Marel JC. Emended description of the genus Phyllobacterium and description of four novel species associated with plant roots: Phyllobacterium bourgognense sp. nov., Phyllobacterium ifriqiyense sp. nov., Phyllobacterium leguminum sp. nov. And Phyllobacterium brassicacearum sp. nov. Int J Syst Evol Microbiol. 2006;56(4):827–39.CrossRefGoogle Scholar
  207. Marcos-García M, Menéndez E, Ramírez-Bahena MH, Mateos PF, Peix Á, Velazquez E, Rivas R. Mesorhizobium helmanticense sp. nov., isolated from Lotus corniculatus nodules. Int J Syst Evol Microbiol. 2017;67(7):2301–5.PubMedCrossRefPubMedCentralGoogle Scholar
  208. Martens M, Delaere M, Coopman R, De Vos P, Gillis M, Willems A. Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol. 2007;57:489–503.PubMedCrossRefPubMedCentralGoogle Scholar
  209. Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A. Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol. 2008;58:200–14.CrossRefGoogle Scholar
  210. Martínez-Aguilar L, Salazar-Salazar C, Méndez RD, Caballero-Mellado J, Hirsch AM, Vásquez-Murrieta MS, Estrada-de los Santos P. Burkholderia caballeronis sp. nov., a nitrogen fixing species isolated from tomato (Lycopersicon esculentum) with the ability to effectively nodulate Phaseolus vulgaris. Antonie Van Leeuwenhoek. 2013;104(6):1063–671.PubMedCrossRefPubMedCentralGoogle Scholar
  211. Martínez-Hidalgo P, Ramírez-Bahena MH, Flores-Félix JD, Rivas R, Igual JM, Mateos PF, Martínez-Molina E, León-Barrios M, Peix Á, Velázquez E. Revision of the taxonomic status of type strains of Mesorhizobium loti and reclassification of strain USDA 3471T as the type strain of Mesorhizobium erdmanii sp. nov. and ATCC 33669T as the type strain of Mesorhizobium jarvisii sp. nov. Int J Syst Evol Microbiol. 2015;65(6):1703–8.PubMedCrossRefPubMedCentralGoogle Scholar
  212. Martínez-Hidalgo P, Ramírez-Bahena MH, Flores-Félix JD, Igual JM, Sanjuán J, León-Barrios M, Peix A, Velázquez E. Reclassification of strains MAFF 303099T and R7A into Mesorhizobium japonicum sp. nov. Int J Syst Evol Microbiol. 2016;66(12):4936–41.PubMedCrossRefPubMedCentralGoogle Scholar
  213. Martínez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol. 1991;41(3):417–26.PubMedCrossRefPubMedCentralGoogle Scholar
  214. Martins da Costa E, Azarias Guimarães A, Pereira Vicentin R, de Almeida Ribeiro PR, Ribas Leão AC, Balsanelli E, Lebbe L, Aerts M, Willems A, de Souza Moreira FM. Bradyrhizobium brasilense sp. nov., a symbiotic nitrogen-fixing bacterium isolated from Brazilian tropical soils. Arch Microbiol. 2017;199(8):1211–21.PubMedCrossRefPubMedCentralGoogle Scholar
  215. Martins da Costa E, Azarias Guimarães A, Soares de Carvalho T, Louzada Rodrigues T, de Almeida Ribeiro PR, Lebbe L, Willems A, de Souza Moreira FM. Bradyrhizobium forestalis sp. nov., an efficient nitrogen-fixing bacterium isolated from nodules of forest legume species in the Amazon. Arch Microbiol. 2018;200(5):743–52.PubMedCrossRefPubMedCentralGoogle Scholar
  216. Máthé I, Tóth E, Mentes A, Szabó A, Márialigeti K, Schumann P, Felföldi T. A new Rhizobium species isolated from the water of a crater lake, description of Rhizobium aquaticum sp. nov. Antonie Van Leeuwenhoek. 2018;  https://doi.org/10.1007/s10482-018-1110-0.. [Epub ahead of print]PubMedCrossRefPubMedCentralGoogle Scholar
  217. Mattarozzi M, Manfredi M, Montanini B, Gosetti F, Sanangelantoni AM, Marengo E, Careri M, Visioli G. A metaproteomic approach dissecting major bacterial functions in the rhizosphere of plants living in serpentine soil. Anal Bioanal Chem. 2017;409(9):2327–39.PubMedCrossRefPubMedCentralGoogle Scholar
  218. Mavengere NR, Ellis AG, Le Roux JJ. Burkholderia aspalathi sp. nov., isolated from root nodules of the South African legume Aspalathus abietina Thunb. Int J Syst Evol Microbiol. 2014;64(6):1906–12.PubMedCrossRefPubMedCentralGoogle Scholar
  219. Mazur A, Stasiak G, Wielbo J, Koper P, Kubik-Komar A, Skorupska A. Phenotype profiling of Rhizobium leguminosarum bv. trifolii clover nodule isolates reveal their both versatile and specialized metabolic capabilities. Arch Microbiol. 2013;195(4):255–67.PubMedPubMedCentralCrossRefGoogle Scholar
  220. McInnes A, Thies JE, Abbott LK, Howieson JG. Structure and diversity among rhizobial strains, populations and communities–a review. Soil Biol Biochem. 2004;36:1295–308.CrossRefGoogle Scholar
  221. McInroy SG, Campbell CD, Haukka KE, Odee DW, Sprent JI, Wen-Jun Wang W-J, Young JPW, Sutherland JM. Characterisation of rhizobia from African acacias and other tropical woody legumes using Biolog I and partial 16S rRNA sequencing. FEMS Microbiol Lett. 1999;170:111–7.PubMedPubMedCentralGoogle Scholar
  222. Merabet C, Martens M, Mahdhi M, Zakhia F, Sy A, Le Roux C, Domergue O, Coopman R, Bekki A, Mars M, Willems A, de Lajudie P. Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp. nov. and Ensifer garamanticus sp. nov. Int J Syst Evol Microbiol. 2010;60(3):664–74.PubMedCrossRefPubMedCentralGoogle Scholar
  223. Mergaert J, Cnockaert MC, Swings J. Phyllobacterium myrsinacearum (subjective synonym Phyllobacterium rubiacearum) emend. Int J Syst Evol Microbiol. 2002;52:1821–3.PubMedPubMedCentralGoogle Scholar
  224. Michel DC, Passos SR, Simões-Araujo JL, Baraúna AC, da Silva K, Parma MM, Melo IS, De Meyer SE, O'Hara G, Zilli JE. Bradyrhizobium centrolobii and Bradyrhizobium macuxiense sp. nov. isolated from Centrolobium paraense grown in soil of Amazonia, Brazil. Arch Microbiol. 2017;199(5):657–64.PubMedCrossRefPubMedCentralGoogle Scholar
  225. Miller KJ, Shon BC, Gore RS, Hunt WP. The phospholipid composition of Bradyrhizobium spp. Curr Microbiol. 1990;21:205–10.CrossRefGoogle Scholar
  226. Minder AC, de Rudder KEE, Narberhaus F, Fischer HM, Hennecke H, Geiger O. Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol Microbiol. 2001;39:1186–98.PubMedCrossRefPubMedCentralGoogle Scholar
  227. Mnasri B, Mrabet M, Laguerre G, Aouani ME, Mhamdi R. Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch Microbiol. 2007;187:79–85.PubMedCrossRefPubMedCentralGoogle Scholar
  228. Mnasri B, Saïdi S, Chihaoui SA, Mhamdi R. Sinorhizobium americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a Northern Tunisian field. Syst Appl Microbiol. 2012;35(4):263–369.PubMedCrossRefPubMedCentralGoogle Scholar
  229. Mnasri B, Liu TY, Saidi S, Chen WF, Chen WX, Zhang XX, Mhamdi R. Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root-nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol. 2014;64(5):1501–6.PubMedCrossRefPubMedCentralGoogle Scholar
  230. Mohamad R, Willems A, Le Quéré A, Maynaud G, Pervent M, Bonabaud M, Dubois E, Cleyet-Marel JC, Brunel B. Mesorhizobium delmotii and Mesorhizobium prunaredense are two new species containing rhizobial strains within the symbiovar anthyllidis. Syst Appl Microbiol. 2017;40(3):135–43.PubMedCrossRefPubMedCentralGoogle Scholar
  231. Mohapatra B, Sarkar A, Joshi S, Chatterjee A, Kazy SK, Maiti MK, Satyanarayana T, Sar P. An arsenate-reducing and alkane-metabolizing novel bacterium, Rhizobium arsenicireducens sp. nov., isolated from arsenic-rich groundwater. Arch Microbiol. 2017;199(2):191–201.PubMedCrossRefPubMedCentralGoogle Scholar
  232. Moulin L, Munive A, Dreyfus B, Boivin-Masson C. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature. 2001;411(6840):948–50.PubMedCrossRefPubMedCentralGoogle Scholar
  233. Mousavi SA, Österman J, Wahlberg N, Nesme X, Lavire C, Vial L, Paulin L, de Lajudie P, Lindström K. Phylogeny of the Rhizobium-Allorhizobium-Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst Appl Microbiol. 2014;37(3):208–15.CrossRefGoogle Scholar
  234. Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindström K. Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol. 2015;38(2):84–90.CrossRefGoogle Scholar
  235. Msaddak A, Rejili M, Durán D, Rey L, Imperial J, Palacios JM, Ruiz-Argüeso T, Mars M. Members of Microvirga and Bradyrhizobium genera are native endosymbiotic bacteria nodulating Lupinus luteus in Northern Tunisian soils. FEMS Microbiol Ecol. 2017a;93(6)  https://doi.org/10.1093/femsec/fix068.
  236. Msaddak A, Durán D, Rejili M, Mars M, Ruiz-Argüeso T, Imperial J, Palacios J, Rey L. Diverse bacteria affiliated with the genera Microvirga, Phyllobacterium, and Bradyrhizobium Nodulate Lupinus micranthus growing in soils of Northern Tunisia. Appl Environ Microbiol. 2017b;83(6):e02820–16.PubMedPubMedCentralCrossRefGoogle Scholar
  237. Msaddak A, Rejili M, Durán D, Rey L, Palacios JM, Imperial J, Ruiz-Argüeso T, Mars M. Definition of two new symbiovars, sv. lupini and sv. mediterranense, within the genera Bradyrhizobium and Phyllobacterium efficiently nodulating Lupinus micranthus in Tunisia. Syst Appl Microbiol. 2018;41(5):487–93.PubMedCrossRefPubMedCentralGoogle Scholar
  238. Nandasena KG, O'Hara GW, Tiwari RP, Willems A, Howieson JG. Mesorhizobium australicum sp. nov. and Mesorhizobium opportunistum sp. nov., isolated from Biserrula pelecinus L. in Australia. Int J Syst Evol Microbiol. 2009;59(9):2140–7.PubMedCrossRefPubMedCentralGoogle Scholar
  239. Nguyen TM, Pham VH, Kim J. Mesorhizobium soli sp. nov., a novel species isolated from the rhizosphere of Robinia pseudoacacia L. in South Korea by using a modified culture method. Antonie Van Leeuwenhoek. 2015;108(2):301–10.PubMedCrossRefPubMedCentralGoogle Scholar
  240. Nick G, de Lajudie P, Eardly BD, Suomalainen S, Paulin L, Zhang X, Gillis M, Lindström K. Sinorhizobium arboris sp. nov. and Sinorhizobium kostiense sp. nov., isolated from leguminous trees in Sudan and Kenya. Int J Syst Bacteriol. 1999;49(4):1359–68.PubMedCrossRefPubMedCentralGoogle Scholar
  241. Nour SM, Fernandez MP, Normand P, Cleyet-Marel J-C. Rhizobium ciceri sp. nov. consisting of strains that nodulate chickpeas (Cicer ariehum L.). Int J Syst Bacteriol. 1994;44:511–22.CrossRefGoogle Scholar
  242. Nour SM, Cleyet-Marel J-C, Normand P, Fernandez MP. Genomic heterogeneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. Int J Syst Bacteriol. 1995;45:640–8.CrossRefGoogle Scholar
  243. Novikova N, Safronova V. Transconjugants of Agrobacterium radiobacter harbouring sym genes of Rhizobium galegae can form an effective symbiosis with Medicago sativa. FEMS Microbiol Lett. 1992;72(3):261–8.PubMedCrossRefPubMedCentralGoogle Scholar
  244. Odair A, Glaciela K, Mariangela H. Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biol Biochem. 2006;38(6):1298–307.CrossRefGoogle Scholar
  245. Okazaki S, Noisangiam R, Okubo T, Kaneko T, Oshima K, Hattori M, Teamtisong K, Songwattana P, Tittabutr P, Boonkerd N, Saeki K, Sato S, Uchiumi T, Minamisawa K, Teaumroong N. Genome analysis of a novel Bradyrhizobium sp. DOA9 carrying a symbiotic plasmid. PLoS One. 2015;10(2):e0117392.PubMedPubMedCentralCrossRefGoogle Scholar
  246. Okubo T, Piromyou P, Tittabutr P, Teaumroong N, Minamisawa K. Origin and evolution of nitrogen fixation genes on symbiosis islands and plasmid in Bradyrhizobium. Microbes Environ. 2016;31(3):260–7.PubMedPubMedCentralCrossRefGoogle Scholar
  247. Ophel K, Kerr A. Agrobacteriurn vitis sp. nov. for strains of Agrobacteriurn biovar 3 from grapevines. Int J Syst Bacteriol. 1990;40(3):236–41.CrossRefGoogle Scholar
  248. Orgambide GG, Huang ZH, Gage DA, Dazzo FB. Phospholipid and fatty acid compositions of Rhizobium leguminosarum biovar trifolii ANU843 in relation to flavone-activated pSym nod gene expression. Lipids. 1993;28:975–9.PubMedCrossRefPubMedCentralGoogle Scholar
  249. Parag B, Sasikala C, Ramana CV. Molecular and culture dependent characterization of endolithic bacteria in two beach sand samples and description of Rhizobium endolithicum sp. nov. Antonie Van Leeuwenhoek. 2013;104(6):1235–44.PubMedCrossRefPubMedCentralGoogle Scholar
  250. Peng GX, Tan ZY, Wang ET, Reinhold-Hurek B, Chen WF, Chen WX. Identification of isolates from soybean nodules in Xinjiang Region as Sinorhizobium xinjiangense and genetic differentiation of S. xinjiangense from S. fredii. Int J Syst Evol Microbiol. 2002;52(5):457–62.PubMedCrossRefPubMedCentralGoogle Scholar
  251. Peng G, Yuan Q, Li H, Zhang W, Tan Z. Rhizobium oryzae sp. nov., isolated from the wild rice Oryza alta. Int J Syst Evol Microbiol. 2008;58(9):2158–63.PubMedCrossRefPubMedCentralGoogle Scholar
  252. Peyret M, Freney J, Meugnier H, Fleurette J. Determination of G + C content of DNA using high-performance liquid chromatography for the identification of staphylococci and micrococci. Res Microbiol. 1989;140(7):467–75.PubMedCrossRefPubMedCentralGoogle Scholar
  253. Platero R, James EK, Rios C, Iriarte A, Sandes L, Zabaleta M, Battistoni F, Fabiano E. Novel Cupriavidus strains isolated from root nodules of native Uruguayan Mimosa species. Appl Environ Microbiol. 2016;82(11):3150–64.PubMedPubMedCentralCrossRefGoogle Scholar
  254. Poupot R, Martinez-Romero E, Gautier N, Promeè JC. Wild-type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-methylated, and carbamoylated nodulation factors. J Biol Chem. 1995;270:6050–5.PubMedCrossRefPubMedCentralGoogle Scholar
  255. Puławska J, Kuzmanović N, Willems A, Pothier JF. Pararhizobium polonicum sp. nov. isolated from tumors on stone fruit rootstocks. Syst Appl Microbiol. 2016;39(3):164–9.PubMedCrossRefPubMedCentralGoogle Scholar
  256. Qin W, Deng ZS, Xu L, Wang NN, Wei GH. Rhizobium helanshanense sp. nov., a bacterium that nodulates Sphaerophysa salsula (Pall.) DC. in China. Arch Microbiol. 2012;194:371–8.PubMedCrossRefPubMedCentralGoogle Scholar
  257. Quan ZX, Bae HS, Baek JH, Chen WF, Im WT, Lee ST. Rhizobium daejeonense sp. nov. isolated from a cyanide treatment bioreactor. Int J Syst Evol Microbiol. 2005;55(6):2543–9.PubMedCrossRefPubMedCentralGoogle Scholar
  258. Radeva G, Jurgens G, Niemi M, Nick G, Suominen L, Lindström K. Description of two biovars in the Rhizobium galegae species: biovar orientalis and biovar officinalis. Syst Appl Microbiol. 2001;24:192–205.PubMedCrossRefPubMedCentralGoogle Scholar
  259. Radl V, Simões-Araújo JL, Leite J, Passos SR, Martins LM, Xavier GR, Rumjanek NG, Baldani JI, Zilli JE. Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int J Syst Evol Microbiol. 2014;64(3):725–30.PubMedCrossRefPubMedCentralGoogle Scholar
  260. Ramana CV, Parag B, Girija KR, Ram BR, Ramana VV, Sasikala C. Rhizobium subbaraonis sp. nov., an endolithic bacterium isolated from beach sand. Int J Syst Evol Microbiol. 2013;63(2):581–5.PubMedCrossRefPubMedCentralGoogle Scholar
  261. Ramírez-Bahena MH, García-Fraile P, Peix A, Valverde A, Rivas R, Igual JM, Mateos PF, Martínez-Molina E, Velázquez E. Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (=NCIMB 11478) as Rhizobium pisi sp. nov. Int J Syst Evol Microbiol. 2008;58(11):2484–90.CrossRefGoogle Scholar
  262. Ramírez-Bahena MH, Peix A, Rivas R, Camacho M, Rodríguez-Navarro DN, Mateos PF, Martínez-Molina E, Willems A, Velázquez E. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int J Syst Evol Microbiol. 2009;59(8):1929–34.PubMedCrossRefPubMedCentralGoogle Scholar
  263. Ramírez-Bahena MH, Hernández M, Peix A, Velázquez E, León-Barrios M. Mesorhizobial strains nodulating Anagyris latifolia and Lotus berthelotii in Tamadaya ravine (Tenerife, Canary Islands) are two symbiovars of the same species. Mesorhizobium tamadayense sp. nov. Syst Appl Microbiol. 2012;35(5):334–41.PubMedCrossRefPubMedCentralGoogle Scholar
  264. Ramírez-Bahena MH, Chahboune R, Peix A, Velázquez E. Reclassification of Agromonas oligotrophica into the genus Bradyrhizobium as Bradyrhizobium oligotrophicum comb. nov. Int J Syst Evol Microbiol. 2013;63(3):1013–6.PubMedCrossRefPubMedCentralGoogle Scholar
  265. Ramírez-Bahena MH, Flores-Félix JD, Chahboune R, Toro M, Velázquez E, Peix A. Bradyrhizobium centrosemae (symbiovar centrosemae) sp. nov., Bradyrhizobium americanum (symbiovar phaseolarum) sp. nov. and a new symbiovar (tropici) of Bradyrhizobium viridifuturi establish symbiosis with Centrosema species native to America. Syst Appl Microbiol. 2016;39(6):378–83.PubMedCrossRefPubMedCentralGoogle Scholar
  266. Rashid MH, Young JP, Everall I, Clercx P, Willems A, Santhosh Braun M, Wink M. Average nucleotide identity of genome sequences supports the description of Rhizobium lentis sp. nov., Rhizobium bangladeshense sp. nov. and Rhizobium binae sp. nov. from lentil (Lens culinaris) nodules. Int J Syst Evol Microbiol. 2015;65(9):3037–45.PubMedCrossRefPubMedCentralGoogle Scholar
  267. Ren DW, Chen WF, Sui XH, Wang ET, Chen WX. Rhizobium vignae sp. nov., a symbiotic bacterium isolated from multiple legume species. Int J Syst Evol Microbiol. 2011a;61:580–6.CrossRefGoogle Scholar
  268. Ren DW, Wang ET, Chen WF, Sui XH, Zhang XX, Liu HC, Chen WX. Rhizobium herbae sp. nov. and Rhizobium giardinii-related bacteria, minor microsymbionts of various wild legumes in China. Int J Syst Evol Microbiol. 2011b;61:1912–20.CrossRefGoogle Scholar
  269. Renier A, De Faria SM, Jourand P, Giraud E, Dreyfus B, Rapior S, Prin Y. Nodulation of Crotalaria podocarpa DC. by Methylobacterium nodulans displays very unusual features. J Exp Bot. 2011;62(10):3693–7.PubMedCrossRefPubMedCentralGoogle Scholar
  270. Ribeiro RA, Rogel MA, López-López A, Ormeño-Orrillo E, Barcellos FG, Martínez J, Thompson FL, Martínez-Romero E, Hungria M. Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int J Syst Evol Microbiol. 2012;62(5):1179–84.CrossRefGoogle Scholar
  271. Ribeiro RA, Martins TB, Ormeño-Orrillo E, Marçon Delamuta JR, Rogel MA, Martínez-Romero E, Hungria M. Rhizobium ecuadorense sp. nov., an indigenous N2-fixing symbiont of the Ecuadorian common bean (Phaseolus vulgaris L.) genetic pool. Int J Syst Evol Microbiol. 2015;65(9):3162–9.PubMedCrossRefPubMedCentralGoogle Scholar
  272. Rincón-Rosales R, Lloret L, Ponce E, Martínez-Romero E. Rhizobia with different symbiotic efficiencies nodulate Acaciella angustissima in Mexico, including Sinorhizobium chiapanecum sp. nov. which has common symbiotic genes with Sinorhizobium mexicanum. FEMS Microbiol Ecol. 2009;67(1):103–17.PubMedCrossRefPubMedCentralGoogle Scholar
  273. Rincón-Rosales R, Villalobos-Escobedo JM, Rogel MA, Martinez J, Ormeño-Orrillo E, Martínez-Romero E. Rhizobium calliandrae sp. nov., Rhizobium mayense sp. nov. and Rhizobium jaguaris sp. nov., rhizobial species nodulating the medicinal legume Calliandra grandiflora. Int J Syst Evol Microbiol. 2013;63(9):3423–9.PubMedCrossRefPubMedCentralGoogle Scholar
  274. Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl Environ Microbiol. 2002;68(11):5217–22.PubMedPubMedCentralCrossRefGoogle Scholar
  275. Rivas R, Willems A, Subba-Rao NS, Mateos PF, Dazzo FB, Kroppenstedt RM, Martínez-Molina E, Gillis M, Velázquez E. Description of Devosia neptuniae sp. nov. that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Microbiol. 2003;26(1):47–53.PubMedCrossRefPubMedCentralGoogle Scholar
  276. Rivas R, Willems A, Palomo JL, García-Benavides P, Mateos PF, Martínez-Molina E, Gillis M, Velázquez E. Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int J Syst Evol Microbiol. 2004;54(4):1271–5.PubMedCrossRefPubMedCentralGoogle Scholar
  277. Roberts GP, Leps WT, Silver LE, Brill WJ. Use of Two-dimensional polyacrylamide gel electrophoresis to identify and classify Rhizobium strains. Appl Environ Microbiol. 1980;39(2):414–22.PubMedPubMedCentralGoogle Scholar
  278. Rogel MA, Bustos P, Santamaría RI, González V, Romero D, Cevallos MÁ, Lozano L, Castro-Mondragón J, Martínez-Romero J, Ormeño-Orrillo E, Martínez-Romero E. Genomic basis of symbiovar mimosae in Rhizobium etli. BMC Genomics. 2014;15:575.PubMedPubMedCentralCrossRefGoogle Scholar
  279. Román-Ponce B, Zhang YJ, Vásquez-Murrieta MS, Sui XH, Chen WF, Alberto Padilla JC, Guo XW, Gao JL, Yan J, Wei GH, Wang ET. Rhizobium acidisoli sp. nov., isolated from root nodules of Phaseolus vulgaris in acid soils. Int J Syst Evol Microbiol. 2016;66(1):398–406.CrossRefGoogle Scholar
  280. Rome S, Fernandez MP, Brunel B, Normand P, Cleyet-Marel JC. Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. Int J Syst Bacteriol. 1996;46(4):972–80.PubMedPubMedCentralCrossRefGoogle Scholar
  281. Rozahon M, Ismayil N, Hamood B, Erkin R, Abdurahman M, Mamtimin H, Abdukerim M, Lal R, Rahman E. Rhizobium populi sp. nov., an endophytic bacterium isolated from Populus euphratica. Int J Syst Evol Microbiol. 2014;64(9):3215–21.PubMedCrossRefPubMedCentralGoogle Scholar
  282. Ruan H, Hu M, Chen J, Li X, Li T, Lai Y, Wang ET, Gu J. Detection of the type III secretion system and its phylogenetic and symbiotic characterization in peanut bradyrhizobia isolated from Guangdong Province, China. Syst Appl Microbiol. 2018;41(5):437–44.PubMedCrossRefPubMedCentralGoogle Scholar
  283. Rüger H-J, Hofle MG. Marine star-shaped-aggregate-forming bacteria: Agrobacterium atlanticum sp. nov.; Agrobacterium meteori sp. nov.; Agrobacterium ferrugineum sp. nov., nom. rev.; Agrobacterium gelatinovorum sp. nov., nom. rev.; and Agrobacterium stellulatum sp. nov., nom. rev. Int J Syst Bacteriol. 1992;42(1):133–43.PubMedCrossRefGoogle Scholar
  284. Safronova VI, Kuznetsova IG, Sazanova AL, Belimov AA, Andronov EE, Chirak ER, Osledkin YS, Onishchuk OP, Kurchak ON, Shaposhnikov AI, Willems A, Tikhonovich IA. Microvirga ossetica sp. nov., a species of rhizobia isolated from root nodules of the legume species Vicia alpestris Steven. Int J Syst Evol Microbiol. 2017;67(1):94–100.PubMedCrossRefPubMedCentralGoogle Scholar
  285. Safronova VI, Sazanova AL, Kuznetsova IG, Belimov AA, Andronov EE, Chirak ER, Popova JP, Verkhozina AV, Willems A, Tikhonovich IA. Phyllobacterium zundukense sp. nov., a novel species of rhizobia isolated from root nodules of the legume species Oxytropis triphylla (Pall.) Pers. Int J Syst Evol Microbiol. 2018;68(5):1644–51.PubMedCrossRefGoogle Scholar
  286. Saïdi S, Ramírez-Bahena MH, Santillana N, Zúñiga D, Álvarez-Martínez E, Peix A, Mhamdi R, Velázquez E. Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int J Syst Evol Microbiol. 2014;64(1):242–7.CrossRefGoogle Scholar
  287. Sánchez M, Ramírez-Bahena MH, Peix A, Lorite MJ, Sanjuán J, Velázquez E, Monza J. Phyllobacterium loti sp. nov. isolated from nodules of Lotus corniculatus. Int J Syst Evol Microbiol. 2014;64(3):781–6.PubMedPubMedCentralCrossRefGoogle Scholar
  288. Sawana A, Adeolu M, Gupta RS. Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet. 2014;5:429.PubMedPubMedCentralCrossRefGoogle Scholar
  289. Schmeisser C, Liesegang H, Krysciak D, Bakkou N, Le Quere A, Wollherr A, and 12 other authors. Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl Env Microbiol. 2009;75:4035–45.CrossRefGoogle Scholar
  290. Segovia L, Young JP, Martínez-Romero E. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Bacteriol. 1993;43(2):374–7.CrossRefGoogle Scholar
  291. Shamseldin A, Carro L, Peix A, Velázquez E, Moawad H, Sadowsky MJ. The symbiovar trifolii of Rhizobium bangladeshense and Rhizobium aegyptiacum sp. nov. nodulate Trifolium alexandrinum in Egypt. Syst Appl Microbiol. 2016;39(4):275–9.PubMedCrossRefPubMedCentralGoogle Scholar
  292. Shen L, Zheng LP, Liu H, Liu R, Zhang KY, Lai R. Rhizobium kunmingense sp. nov., isolated from rhizosphere soil of Camptotheca acuminata Decne. J Gen Appl Microbiol. 2010;56(2):143–9.PubMedCrossRefGoogle Scholar
  293. Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, James EK, Sprent JI, Young JP, Chen WM. Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol. 2012;62(9):2272–8.PubMedCrossRefPubMedCentralGoogle Scholar
  294. Sheu SY, Chou JH, Bontemps C, Elliott GN, Gross E, dos Reis Junior FB, Melkonian R, Moulin L, James EK, Sprent JI, Young JP, Chen WM. Burkholderia diazotrophica sp. nov., isolated from root nodules of Mimosa spp. Int J Syst Evol Microbiol. 2013;63(2):435–41.PubMedCrossRefGoogle Scholar
  295. Sheu SY, Huang HW, Young CC, Chen WM. Rhizobium alvei sp. nov., isolated from a freshwater river. Int J Syst Evol Microbiol. 2015a;65(2):472–8.PubMedCrossRefGoogle Scholar
  296. Sheu SY, Chen MH, Liu WY, Andrews M, James EK, Ardley JK, De Meyer SE, James TK, Howieson JG, Coutinho BG, Chen WM. Burkholderia dipogonis sp. nov., isolated from root nodules of Dipogon lignosus in New Zealand and Western Australia. Int J Syst Evol Microbiol. 2015b;65(12):4716–23.PubMedCrossRefPubMedCentralGoogle Scholar
  297. Sheu SY, Chen ZH, Young CC, Chen WM. Rhizobium ipomoeae sp. nov., isolated from a water convolvulus field. Int J Syst Evol Microbiol. 2016;66(4):1633–40.PubMedCrossRefPubMedCentralGoogle Scholar
  298. Shi X, Li C, Zhao L, Si M, Zhu L, Xin K, Chen C, Wang Y, Shen X, Zhang L. Rhizobium gei sp. nov., a bacterial endophyte of Geum aleppicum. Int J Syst Evol Microbiol. 2016;66(10):4282–8.PubMedCrossRefGoogle Scholar
  299. Shiraishi A, Matsushita N, Hougetsu T. Nodulation in black locust by the Gammaproteobacteria Pseudomonas sp. and the Betaproteobacteria Burkholderia sp. Syst Appl Microbiol. 2010;33(5):269–74.PubMedCrossRefGoogle Scholar
  300. Silva FV, De Meyer SE, Simões-Araújo JL, Barbé Tda C, Xavier GR, O'Hara G, Ardley JK, Rumjanek NG, Willems A, Zilli JE. Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils. Int J Syst Evol Microbiol. 2014;64(7):2358–63.PubMedCrossRefGoogle Scholar
  301. Smith EF, Townsend CO. A plant-tumor of bacterial origin. Science 1907;25:671–673.PubMedCrossRefGoogle Scholar
  302. Soenens A, Gomila M, Imperial J. Neorhizobium tomejilense sp. nov., first non-symbiotic Neorhizobium species isolated from a dryland agricultural soil in southern Spain. Syst Appl Microbiol. 2018;  https://doi.org/10.1016/j.syapm.2018.09.001.. [Epub ahead of print]PubMedCrossRefGoogle Scholar
  303. Squartini A, Struffi P, Döring H, Selenska-Pobell S, Tola E, Giacomini A, Vendramin E, Velázquez E, Mateos PF, Martínez-Molina E, Dazzo FB, Casella S, Nuti MP. Rhizobium sullae sp. nov. (formerly 'Rhizobium hedysari'), the root-nodule microsymbiont of Hedysarum coronarium L. Int J Syst Evol Microbiol. 2002;52(4):1267–76.PubMedPubMedCentralGoogle Scholar
  304. Steenkamp ET, van Zyl E, Beukes CW, Avontuur JR, Chan WY, Palmer M, Mthombeni LS, Phalane FL, Sereme TK, Venter SN. Burkholderia kirstenboschensis sp. nov. nodulates papilionoid legumes indigenous to South Africa. Syst Appl Microbiol. 2015;38(8):545–54.PubMedCrossRefPubMedCentralGoogle Scholar
  305. Sullivan JT, Ronson CW. Evolution of rhizobia by acquisition of a 500-Kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA. 1998;95:5145–9.PubMedCrossRefPubMedCentralGoogle Scholar
  306. Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol. 2001;183(1):214–20.PubMedPubMedCentralCrossRefGoogle Scholar
  307. Tak A, Gehlot P, Pathak R, Singh SK. Species diversity of rhizobia. In: Hansen A, Choudhary D, Agrawal P, Varma A, editors. Rhizobium biology and biotechnology, Soil biology, vol. 50. Cham: Springer; 2017.CrossRefGoogle Scholar
  308. Tan ZY, Xu XD, Wang ET, Gao JL, Martínez-Romero E, Chen WX. Phylogenetic and genetic relationships of Mesorhizobium tianshanense and related rhizobia. Int J Syst Bacteriol. 1997;47(3):874–9.PubMedCrossRefPubMedCentralGoogle Scholar
  309. Tan Z, Hurek T, Vinuesa P, Müller P, Ladha JK, Reinhold-Hurek B. Specific detection of Bradyrhizobium and Rhizobium strains colonizing rice (Oryza sativa) roots by 16S-23S ribosomal DNA intergenic spacer-targeted PCR. Appl Environ Microbiol. 2001;67(8):3655–64.PubMedPubMedCentralCrossRefGoogle Scholar
  310. Tang H, Wang E, Sui X, Man C, Jia R, Lin D, Qu Z, Chen W. The novel alkali tolerance function of tfxG in Sinorhizobium meliloti. Res Microbiol. 2007;158(6):501–5.PubMedCrossRefPubMedCentralGoogle Scholar
  311. Taulé C, Zabaleta M, Mareque C, Platero R, Sanjurjo L, Sicardi M, Frioni L, Battistoni F, Fabiano E. New betaproteobacterial Rhizobium strains able to efficiently nodulate Parapiptadenia rigida (Benth.) Brenan. Appl Environ Microbiol. 2012;78(6):1692–700.PubMedPubMedCentralCrossRefGoogle Scholar
  312. Teng Y, Feng S, Ren W, Zhu L, Ma W, Christie P, Luo Y. Phytoremediation of diphenylarsinic-acid-contaminated soil by Pteris vittata associated with Phyllobacterium myrsinacearum RC6b. Int J Phytoremed. 2017;19(5):463–9.CrossRefGoogle Scholar
  313. Terefework Z, Kaijalainen S, Lindström K. AFLP fingerprinting as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and Galega officinalis. J Biotechnol. 2001;91(2-3):169–80.PubMedPubMedCentralCrossRefGoogle Scholar
  314. Tian CF, Wang ET, Han TX, Sui XH, Chen WX. Genetic diversity of rhizobia associated with Vicia faba in three ecological regions of China. Arch Microbiol. 2007;188(3):273–82.PubMedCrossRefPubMedCentralGoogle Scholar
  315. Tian CF, Wang ET, Wu LJ, Han TX, Chen WF, Gu CT, Gu JG, Chen WX. Rhizobium fabae sp. nov., a bacterium that nodulates Vicia faba. Int J Syst Evol Microbiol. 2008;58(12):2871–5.CrossRefGoogle Scholar
  316. Tighe SW, de Lajudie P, Dipietro K, Lindstrom K, Nick G, Jarvis BDW. Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. Int J Syst Evol Microbiol. 2000;50:787–801.PubMedCrossRefPubMedCentralGoogle Scholar
  317. Toledo I, Lloret L, Martínez-Romero E. Sinorhizobium americanus sp. nov., a new Sinorhizobium species nodulating native Acacia spp. in Mexico. Syst Appl Microbiol. 2003;26(1):54–64.PubMedCrossRefPubMedCentralGoogle Scholar
  318. Toma MA, de Carvalho TS, Guimarães AA, da Costa EM, da Silva JS, de Souza Moreira FM. Tripartite symbiosis of Sophora tomentosa, rhizobia and arbuscular mycorhizal fungi. Braz J Microbiol. 2017;48(4):680–8.PubMedPubMedCentralCrossRefGoogle Scholar
  319. Torres Tejerizo G, Rogel MA, Ormeño-Orrillo E, Althabegoiti MJ, Nilsson JF, Niehaus K, Schlüter A, Pühler A, Del Papa MF, Lagares A, Martínez-Romero E, Pistorio M. Rhizobium favelukesii sp. nov., isolated from the root nodules of alfalfa (Medicago sativa L). Int J Syst Evol Microbiol. 2016;66(11):4451–7.PubMedPubMedCentralCrossRefGoogle Scholar
  320. Trujillo ME, Willems A, Abril A, Planchuelo AM, Rivas R, Ludeña D, Mateos PF, Martínez-Molina E, Velázquez E. Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl Environ Microbiol. 2005;71(3):1318–27.PubMedPubMedCentralCrossRefGoogle Scholar
  321. Turdahon M, Osman G, Hamdun M, Yusuf K, Abdurehim Z, Abaydulla G, Abdukerim M, Fang C, Rahman E. Rhizobium tarimense sp. nov., isolated from soil in the ancient Khiyik River. Int J Syst Evol Microbiol. 2013;63(7):2424–9.PubMedCrossRefPubMedCentralGoogle Scholar
  322. Uchino Y, Hirata A, Yokota A, Sugiyama J. Reclassification of marine Agrobacterium species: Proposals of Stappia stellulata gen. nov., comb. nov., Stappia aggregata sp. nov., nom. rev., Ruegeria atlantica gen. nov., comb. nov., Ruegeria gelatinovora comb. nov., Ruegeria algicola comb. nov., and Ahrensia kieliense gen. nov., sp. nov., nom. rev. J Gen Appl Microbiol. 1998;44:201–10.PubMedCrossRefPubMedCentralGoogle Scholar
  323. Valverde A, Velázquez E, Gutiérrez C, Cervantes E, Ventosa A, Igual JM. Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol. 2003;53(6):1979–83.PubMedCrossRefPubMedCentralGoogle Scholar
  324. Valverde A, Velázquez E, Fernández-Santos F, Vizcaíno N, Rivas R, Mateos PF, Martínez-Molina E, Igual JM, Willems A. Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. Int J Syst Evol Microbiol. 2005;55(5):1985–9.PubMedCrossRefPubMedCentralGoogle Scholar
  325. Valverde A, Igual JM, Peix A, Cervantes E, Velázquez E. Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Microbiol. 2006;56(11):2631–7.CrossRefGoogle Scholar
  326. van Berkum P, Beyene D, Bao G, Campbell TA, Eardly BD. Rhizobium mongolense sp. nov. is one of three rhizobial genotypes identified which nodulate and form nitrogen-fixing symbioses with Medicago ruthenica [(L.) Ledebour]. Int J Syst Bacteriol. 1998;48(1):13–22.CrossRefGoogle Scholar
  327. van Berkum P, Leibold JM, Eardly BD. Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst Appl Microbiol. 2006;29(3):207–15.PubMedCrossRefPubMedCentralGoogle Scholar
  328. Van Cauwenberghe J, Lemaire B, Stefan A, Efrose R, Michiels J, Honnay O. Symbiont abundance is more important than pre-infection partner choice in a Rhizobium-legume mutualism. Syst Appl Microbiol. 2016;39(5):345–9.PubMedCrossRefPubMedCentralGoogle Scholar
  329. van Loo B, Schober M, Valkov E, Heberlein M, Bornberg-Bauer E, Faber K, Hyvönen M, Hollfelder F. Structural and mechanistic analysis of the choline sulfatase from Sinorhizobium melliloti: a class I sulfatase specific for an alkyl sulfate ester. J Mol Biol. 2018;430(7):1004–23.PubMedPubMedCentralCrossRefGoogle Scholar
  330. Vandamme P, Coenye T. Taxonomy of the genus Cupriavidus: a tale of lost and found. Int J Syst Evol Microbiol. 2004;54(6):2285–9.PubMedCrossRefPubMedCentralGoogle Scholar
  331. Vandamme P, Goris J, Chen WM, de Vos P, Willems A. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol. 2002;25(4):507–12.PubMedCrossRefPubMedCentralGoogle Scholar
  332. Velázquez E, Igual JM, Willems A, Fernández MP, Muñoz E, Mateos PF, Abril A, Toro N, Normand P, Cervantes E, Gillis M, Martínez-Molina E. Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina). Int J Syst Evol Microbiol. 2001;51(3):1011–21.PubMedCrossRefPubMedCentralGoogle Scholar
  333. Velázquez E, Peix A, Zurdo-Piñeiro JL, Palomo JL, Mateos PF, Rivas R, Muñoz-Adelantado E, Toro N, García-Benavides P, Martínez-Molina E. The coexistence of symbiosis and pathogenicity-determining genes in Rhizobium rhizogenes strains enables them to induce nodules and tumors or hairy roots in plants. Mol Plant Microbe Interact. 2005;18(12):1325–32.PubMedCrossRefPubMedCentralGoogle Scholar
  334. Verástegui-Valdés MM, Zhang YJ, Rivera-Orduña FN, Cheng H-P, Sui XH, Wang ET. Microsymbionts of Phaseolus vulgaris in acid and alkaline soils of Mexico. Syst Appl Microbiol. 2014;37(8):605–12.PubMedPubMedCentralCrossRefGoogle Scholar
  335. Vidal C, Chantreuil C, Berge O, Mauré L, Escarré J, Béna G, Brunel B, Cleyet-Marel JC. Mesorhizobium metallidurans sp. nov., a metal-resistant symbiont of Anthyllis vulneraria growing on metallicolous soil in Languedoc, France. Int J Syst Evol Microbiol. 2009;59(4):850–5.PubMedCrossRefPubMedCentralGoogle Scholar
  336. Vinardell J-M, Acosta-Jurado S, Zehner S, Göttfert M, Becker A, Baena I, and 17 other authors. The Sinorhizobium fredii HH103 genome: a comparative analysis with S. fredii strains differing in their symbiotic behavior with soybean. Mol Plant-Microbe Interact. 2015;28:811–24.PubMedCrossRefPubMedCentralGoogle Scholar
  337. Vincent JM. A manual for the practical study of root nodule bacteria. Oxford: Blackwell Scientific; 1970.Google Scholar
  338. Vinuesa P, Rademaker JLW, de Bruijn FJ, Werner D. Genotypic characterization of Bradyrhizobium strains nodulating endemic woody legumes of the Canary Islands by PCR-restriction fragment length polymorphism analysis of genes encoding 16S rRNA (16S rDNA) and 16S-23S rDNA intergenic spacers, repetitive extragenic palindromic PCR genomic fingerprinting, and partial 16S rDNA sequencing. Appl Environ Microbiol. 1998;64(6):2096–104.PubMedPubMedCentralGoogle Scholar
  339. Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral M, Bedmar EJ, Martínez-Romero E. Molecular systematics of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA and nifH sequences, and their use in the classification of Sesbania microsymbionts from Venezuelan wetlands. Syst Appl Microbiol. 2005a;28:702–16.PubMedCrossRefPubMedCentralGoogle Scholar
  340. Vinuesa P, León-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A, Pérez-Galdona R, Werner D, Martínez-Romero E. Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol. 2005b;55(2):569–75.PubMedCrossRefPubMedCentralGoogle Scholar
  341. Wang ET, Martínez-Romero E. Sesbania herbacea-Rhizobium huautlense nodulation in flooded soils and comparative characterization of S. herbacea-nodulating rhizobia in different environments. Microbiol Ecol. 2000;40(1):25–32.CrossRefGoogle Scholar
  342. Wang ET, van Berkum P, Beyene D, Sui XH, Dorado O, Chen WX, Martínez-Romero E. Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int J Syst Bacteriol. 1998;48(3):687–99.PubMedPubMedCentralCrossRefGoogle Scholar
  343. Wang ET, van Berkum P, Sui XH, Beyene D, Chen WX, Martinez-Romero E. Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int J Syst Bacteriol. 1999a;49:51–65.CrossRefGoogle Scholar
  344. Wang ET, Rogel MA, Gracía-de los Santos A, Martínez-Romero J, Cevallos MA, Martínez-Romero E. Rhizobium etli bv. mimosae isolated from Mimosa affinis. Int J Syst Bacteriol. 1999b;49(4):1479–91.PubMedCrossRefPubMedCentralGoogle Scholar
  345. Wang ET, Martínez-Romero J, Martínez-Romero E. Genetic diversity of rhizobia from Leucaena leucocephala nodules in Mexican soils. Mol Ecol. 1999c;8:711–24.CrossRefGoogle Scholar
  346. Wang ET, Tan ZY, Willems A, Fernández-López M, Reinhold-Hurek B, Martínez-Romero E. Sinorhizobium morelense sp. nov., a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. Int J Syst Evol Microbiol. 2002;52(5):1687–93.PubMedPubMedCentralGoogle Scholar
  347. Wang FQ, Wang ET, Liu J, Chen Q, Sui XH, Chen WF, Chen WX. Mesorhizobium albiziae sp. nov., a novel bacterium that nodulates Albizia kalkora in a subtropical region of China. Int J Syst Evol Microbiol. 2007;57(6):1192–9.PubMedCrossRefPubMedCentralGoogle Scholar
  348. Wang F, Wang ET, Wu LJ, Sui XH, Li Y Jr, Chen WX. Rhizobium vallis sp. nov., isolated from nodules of three leguminous species. Int J Syst Evol Microbiol. 2011;61(11):2582–8.CrossRefGoogle Scholar
  349. Wang R, Chang YL, Zheng WT, Zhang D, Zhang XX, Sui XH, Wang ET, Hu JQ, Zhang LY, Chen WX. Bradyrhizobium arachidis sp. nov., isolated from effective nodules of Arachis hypogaea grown in China. Syst Appl Microbiol. 2013a;36(2):101–5.CrossRefGoogle Scholar
  350. Wang JY, Wang R, Zhang YM, Liu HC, Chen WF, Wang ET, Sui XH, Chen WX. Bradyrhizobium daqingense sp. nov., isolated from soybean nodules. Int J Syst Evol Microbiol. 2013b;63(2):616–24.PubMedPubMedCentralCrossRefGoogle Scholar
  351. Wang YC, Wang F, Hou BC, Wang ET, Chen WF, Sui XH, Chen WX, Li Y, Zhang YB. Proposal of Ensifer psoraleae sp. nov., Ensifer sesbaniae sp. nov., Ensifer morelense comb. nov. and Ensifer americanum comb. nov. Syst Appl Microbiol. 2013c;36(7):467–73.PubMedCrossRefPubMedCentralGoogle Scholar
  352. Wang Q, Zhu W, Wang E, Zhang L, Li X, Wang G. Genomic identification of rhizobia-related strains and threshold of ANI and core-genome for family, genus and species. Int J Environ Agri Res. 2016a;2(6):76–86.Google Scholar
  353. Wang L, Cao Y, Wang ET, Qiao YJ, Jiao S, Liu ZS, Zhao L, Wei GH. Biodiversity and biogeography of rhizobia associated with common bean (Phaseolus vulgaris L.) in Shaanxi Province. Syst Appl Microbiol. 2016b;39(3):211–9.CrossRefGoogle Scholar
  354. Wang X, Liu D, Luo Y, Zhao L, Liu Z, Chou M, Wang E, Wei G. Comparative analysis of rhizobial chromosomes and plasmids to estimate their evolutionary relationships. Plasmid. 2018;96-97:13–24.PubMedCrossRefPubMedCentralGoogle Scholar
  355. Wedlock DN, Jarvis BDW. DNA homologies between Rhizobium fredii, rhizobia that nodulate Galega sp., and other Rhizobium and Bradyrhizobium species. Int J Syst Bacteriol. 1986;36:550–8.CrossRefGoogle Scholar
  356. Wei GH, Wang ET, Tan ZY, Zhu ME, Chen WX. Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol. 2002;52(6):2231–9.PubMedPubMedCentralGoogle Scholar
  357. Wei GH, Tan ZY, Zhu ME, Wang ET, Han SZ, Chen WX. Characterization of rhizobia isolated from legume species within the genera Astragalus and Lespedeza grown in the Loess Plateau of China and description of Rhizobium loessense sp. nov. Int J Syst Evol Microbiol. 2003;53(5):1575–83.CrossRefGoogle Scholar
  358. Wei X, Yan S, Li D, Pang H, Li Y, Zhang J. Rhizobium helianthi sp. nov., isolated from the rhizosphere of sunflower. Int J Syst Evol Microbiol. 2015;65(12):4455–60.PubMedCrossRefPubMedCentralGoogle Scholar
  359. Wen Y, Zhang J, Yan Q, Li S, Hong Q. Rhizobium phenanthrenilyticum sp. nov., a novel phenanthrene-degrading bacterium isolated from a petroleum residue treatment system. J Gen Appl Microbiol. 2011;57(6):319–29.PubMedCrossRefPubMedCentralGoogle Scholar
  360. Willems A, Fernández-López M, Muñoz-Adelantado E, Goris J, De Vos P, Martínez-Romero E, Toro N, Gillis M. Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an opinion. Int J Syst Evol Microbiol. 2003;53(4):1207–17.CrossRefGoogle Scholar
  361. Wolde-Meskel E, Terefework Z, Frostegård Å, Lindström K. Genetic diversity and phylogeny of rhizobia isolated from agroforestry legume species in southern Ethiopia. Int J Syst Evol Microbiol. 2005;55:1439–52.PubMedCrossRefPubMedCentralGoogle Scholar
  362. Xu LM, Ge C, Cui Z, Li J, Fan H. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol. 1995;45(4):706–11.PubMedPubMedCentralCrossRefGoogle Scholar
  363. Xu L, Shi JF, Zhao P, Chen WM, Qin W, Tang M, Wei GH. Rhizobium sphaerophysae sp. nov., a novel species isolated from root nodules of Sphaerophysa salsula in China. Antonie van Leeuwenhoek. 2011;99:845–54.PubMedCrossRefPubMedCentralGoogle Scholar
  364. Xu L, Shi J, Li C, Zhu S, Li B. Rhizobium hedysari sp. nov., a novel species isolated from a root nodule of Hedysarum multijugum in China. Antonie van Leeuwenhoek. 2017;110:479–88.PubMedCrossRefPubMedCentralGoogle Scholar
  365. Xu L, Zhang Y, Mohamad OA, Jiang C, Friman V-P. Mesorhizobium zhangyense sp. nov., isolated from wild Thermopsis lanceolate in northwestern China. Arch Microbiol. 2018;20:603–10.CrossRefGoogle Scholar
  366. Xue S, Biondi EG. Coordination of symbiosis and cell cycle functions in Sinorhizobium meliloti. Biochim Biophys Acta. 2018;pii:S1874-9399(17)30415-7.. [Epub ahead of print]Google Scholar
  367. Yan AM, Wang ET, Kan FL, Tan ZY, Sui XH, Reinhold-Hurek B, Chen WX. Sinorhizobium meliloti associated with Medicago sativa and Melilotus spp. in arid saline soils in Xinjiang, China. Int J Syst Evol Microbiol. 2000;50(5):1887–91.PubMedCrossRefPubMedCentralGoogle Scholar
  368. Yan J, Han XZ, Ji ZJ, Li Y, Wang ET, Xie ZH, Chen WF. Abundance and diversity of soybean-nodulating rhizobia in black soil are impacted by land use and crop management. Appl Environ Microbiol. 2014;80(17):5394–402.PubMedPubMedCentralCrossRefGoogle Scholar
  369. Yan H, Yan J, Sui XH, Wang ET, Chen WX, Zhang XX, Chen WF. Ensifer glycinis sp. nov., an novel rhizobial species associated with Glycine spp. Int J Syst Evol Microbiol. 2016;66(8):2910–6.CrossRefGoogle Scholar
  370. Yan H, Xie JB, Ji ZJ, Yuan N, Tian CF, Ji SK, Wu ZY, Zhong L, Chen WX, Du ZL, Wang ET, Chen WF. Evolutionarily conserved nodE, nodO, T1SS, and hydrogenase system in rhizobia of Astragalus membranaceus and Caragana intermedia. Front Microbiol. 2017a;8:2282.PubMedPubMedCentralCrossRefGoogle Scholar
  371. Yan J, Chen W, Han X, Wang E, Zou W, Zhang Z. Genetic diversity of indigenous soybean-nodulating rhizobia in response to locally-based long term fertilization in a Mollisol of Northeat China. World J Microbiol Biotechnol. 2017b;33(1):6.PubMedCrossRefPubMedCentralGoogle Scholar
  372. Yan J, Yan H, Liu LX, Chen WF, Zhang XX, Verástegui-Valdés MM, Wang ET, Han XZ. Rhizobium hidalgonense sp. nov., a nodule endophytic bacterium of Phaseolus vulgaris in acid soil. Arch Microbiol. 2017c;199(1):97–104.CrossRefGoogle Scholar
  373. Yan J, Li Y, Han XZ, Chen WF, Zou WX, Xie Z, Li M. Agrobacterium deltaense sp. nov., an endophytic bacteria isolated from nodule of Sesbania cannabina. Arch Microbiol. 2017d;199(7):1003–9.PubMedCrossRefPubMedCentralGoogle Scholar
  374. Yang SH, Chen WH, Wang ET, Chen WF, Yan J, Han XZ, Tian CF, Sui XH, Singh RP, Jiang G, Chen WX. Rhizobial biogeography and inoculation application to soybean in four regions across China. J Appl Microbiol. 2018;125(3):853–66.PubMedCrossRefPubMedCentralGoogle Scholar
  375. Yao ZY, Kan FL, Wang ET, Wei GH, Chen WX. Characterization of rhizobia that nodulate legume species of the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int J Syst Evol Microbiol. 2002;52(6):2219–30.PubMedPubMedCentralGoogle Scholar
  376. Yao Y, Wang R, Lu J, Sui X, Wang E, Chen W. Genetic diversity and evolution of Bradyrhizobium populations nodulated with Erythrophloeum fordii endemic to the southern subtropical region of China. Appl Environ Microbiol. 2014;80(19):6184–94.PubMedPubMedCentralCrossRefGoogle Scholar
  377. Yao Y, Sui XH, Zhang XX, Wang ET, Chen WX. Bradyrhizobium erythrophlei sp. nov. and Bradyrhizobium ferriligni sp. nov., isolated from effective nodules of Erythrophleum fordii. Int J Syst Evol Microbiol. 2015;65(6):1831–7.PubMedPubMedCentralCrossRefGoogle Scholar
  378. Yoon JH, Kang SJ, Yi HS, Oh TK, Ryu CM. Rhizobium soli sp. nov., isolated from soil. Int J Syst Evol Microbiol. 2010;60(6):1387–93.PubMedCrossRefPubMedCentralGoogle Scholar
  379. Young JM. The genus name Ensifer Casida 1982 takes priority over Sinorhizobium Chen et al., 1988, and Sinorhizobium morelense Wang et al., 2002 is a later synonym of Ensifer adhaerens Casida 1982. Is the combination ‘Sinorhizobium adhaerens’ (Casida 1982) Willems et al., 2003 legitimate? Request for an opinion. Int J Syst Evol Microbiol. 2003;53(6):2107–10.Google Scholar
  380. Young JM. Sinorhizobium versus Ensifer: may a taxonomy subcommittee of the ICSP contradict the Judicial Commission? Int J Syst Evol Microbiol. 2010;60(7):1711–3.PubMedCrossRefPubMedCentralGoogle Scholar
  381. Young JPW, Haukka K. Diversity and phylogeny of rhizobia. New Phytol. 1996;133:87–94.CrossRefGoogle Scholar
  382. Young JPW, Downer HL, Eardly BD. Phylogeny of the phototrophic rhizobium strain BTAil by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J Bacteriol. 1991;173:2271–22.PubMedPubMedCentralCrossRefGoogle Scholar
  383. Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H. A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol. 2001;51:89–103.PubMedCrossRefPubMedCentralGoogle Scholar
  384. Yu X, Cloutier S, Tambong JT, Bromfield ES. Bradyrhizobium ottawaense sp. nov., a symbiotic nitrogen fixing bacterium from root nodules of soybeans in Canada. Int J Syst Evol Microbiol. 2014;64(9):3202–7.PubMedPubMedCentralCrossRefGoogle Scholar
  385. Yuan CG, Jiang Z, Xiao M, Zhou EM, Kim CJ, Hozzein WN, Park DJ, Zhi XY, Li WJ. Mesorhizobium sediminum sp. nov., isolated from deep-sea sediment. J Syst Evol Microbiol. 2016;66(11):4797–802.CrossRefGoogle Scholar
  386. Yuan T, Liu L, Huang S, Hussein Taher A, Tan Z, Wu G, Peng G. Rhizobium wuzhouense sp. nov., isolated from roots of Oryza officinalis. Int J Syst Evol Microbiol. 2018;68(9):2918–23.PubMedCrossRefPubMedCentralGoogle Scholar
  387. Zakhia F, Jeder H, Domergue O, Willems A, Cleyet-Marel J, Gillis M, Dreyfus B, de Lajudie P. Characterisation of wild legume nodulating bacteria (LNB) in the infra-arid zone of Tunisia. Syst Appl Microbiol. 2004;27:380–95.CrossRefGoogle Scholar
  388. Zhang YM, Li Y Jr, Chen WF, Wang ET, Tian CF, Li QQ, Zhang YZ, Sui XH, Chen WX. Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China Plain. Appl Environ Microbiol. 2011a;77(18):6331–42.PubMedPubMedCentralCrossRefGoogle Scholar
  389. Zhang RJ, Hou BC, Wang ET, Li Y Jr, Zhang XX, Chen WX. Rhizobium tubonense sp. nov., isolated from root nodules of Oxytropis glabra. Int J Syst Evol Microbiol. 2011b;61(3):512–7.PubMedCrossRefPubMedCentralGoogle Scholar
  390. Zhang JJ, Lou K, Jin X, Mao PH, Wang ET, Tian CF, Sui XH, Chen WF, Chen WX. Distinctive Mesorhizobium populations associated with Cicer arietinum L. in alkaline soils of Xinjiang, China. Plant Soil. 2012a;353(1-2):123–34.CrossRefGoogle Scholar
  391. Zhang JJ, Liu TY, Chen WF, Wang ET, Sui XH, Zhang XX, Li Y, Li Y, Chen WX. Mesorhizobium muleiense sp. nov., nodulating with Cicer arietinum L. Int J Syst Evol Microbiol. 2012b;62(11):2737–42.CrossRefGoogle Scholar
  392. Zhang X, Li B, Wang H, Sui X, Ma X, Hong Q, Jiang R. Rhizobium petrolearium sp. nov., isolated from oil-contaminated soil. Int J Syst Evol Microbiol. 2012c;62(8):1871–6.PubMedCrossRefPubMedCentralGoogle Scholar
  393. Zhang YM, Li Y Jr, Chen WF, Wang ET, Sui XH, Li QQ, Zhang YZ, Zhou YG, Chen WX. Bradyrhizobium huanghuaihaiense sp. nov., an effective symbiotic bacterium isolated from soybean (Glycine max L.) nodules. Int J Syst Evol Microbiol. 2012d;62(8):1951–7.PubMedPubMedCentralCrossRefGoogle Scholar
  394. Zhang JJ, Yu T, Lou K, Mao PH, Wang ET, Chen WF, Chen WX. Genotypic alteration and competitive nodulation of the Mesorhizobium muleiense against exotic chickpea rhizobia in alkaline soils from Xinjiang, China. Syst Appl Microbiol. 2014a;37(7):520–4.PubMedPubMedCentralCrossRefGoogle Scholar
  395. Zhang XX, Guo HJ, Wang R, Sui XH, Zhang YM, Wang ET, Tian CF, Chen WX. Genetic divergence of Bradyrhizobium strains nodulating soybeans as revealed by multilocus sequence analysis of genes inside and outside the symbiosis island. Appl Environ Microbiol. 2014b;80(10):3181–90.PubMedPubMedCentralCrossRefGoogle Scholar
  396. Zhang XX, Tang X, Sheirdil RA, Sun L, Ma XT. Rhizobium rhizoryzae sp. nov., isolated from rice roots. Int J Syst Evol Microbiol. 2014c;64(4):1373–7.PubMedPubMedCentralCrossRefGoogle Scholar
  397. Zhang L, Shi X, Si M, Li C, Zhu L, Zhao L, Shen X, Wang Y. Rhizobium smilacinae sp. nov., an endophytic bacterium isolated from the leaf of Smilacina japonica. Antonie Van Leeuwenhoek. 2014d;106(4):715–23.PubMedCrossRefPubMedCentralGoogle Scholar
  398. Zhang XX, Gao JS, Cao YH, Sheirdil RA, Wang XC, Zhang L. Rhizobium oryzicola sp. nov., potential plant-growth-promoting endophytic bacteria isolated from rice roots. Int J Syst Evol Microbiol. 2015;65(9):2931–6.PubMedCrossRefPubMedCentralGoogle Scholar
  399. Zhang S, Yang S, Chen W, Chen Y, Zhang M, Zhou X, Fan G, Feng FY. Rhizobium arenae sp. nov., isolated from the sand of Desert Mu Us, China. Int J Syst Evol Microbiol. 2017;67:2098–103.PubMedCrossRefPubMedCentralGoogle Scholar
  400. Zhang J, Guo C, Chen W, Shang Y, de Lajudie P, Yang X, Mao P, Zheng J, Wang ET. Dynamic succession of chickpea rhizobium over years and sampling sites in Xinjiang, China. Plant Soil. 2018a;425(1–2):241–51.Google Scholar
  401. Zhang J, Guo C, Chen W, de Lajudie P, Zhang Z, Shang Y, Wang ET. Mesorhizobium wenxiniae sp. nov., isolated from chickpea (Cicer arietinum L.) in China. Int J Syst Evol Microbiol. 2018b;68(6):1930–6.CrossRefGoogle Scholar
  402. Zhao CT, Wang ET, Zhang YM, Chen WF, Sui XH, Chen WX, Liu HC, Zhang XX. Mesorhizobium silamurunense sp. nov., isolated from root nodules of Astragalus species. Int J Syst Evol Microbiol. 2012;62(9):2180–6.CrossRefGoogle Scholar
  403. Zhao JJ, Zhang J, Sun L, Zhang RJ, Zhang CW, Yin HQ, Zhang XX. Rhizobium oryziradicis sp. nov., isolated from rice roots. Int J Syst Evol Microbiol. 2017a;67(4):963–8.PubMedCrossRefGoogle Scholar
  404. Zhao JJ, Zhang J, Zhang RJ, Zhang CW, Yin HQ, Zhang XX. Rhizobium rhizosphaerae sp. nov., a novel species isolated from rice rhizosphere. Antonie Van Leeuwenhoek. 2017b;110(5):651–6.PubMedCrossRefGoogle Scholar
  405. Zheng WT, Li Y Jr, Wang R, Sui XH, Zhang XX, Zhang JJ, Wang ET, Chen WX. Mesorhizobium qingshengii sp. nov., isolated from effective nodules of Astragalus sinicus. Int J Syst Evol Microbiol. 2013;63(6):2002–7.CrossRefGoogle Scholar
  406. Zhou PF, Chen WM, Wei GH. Mesorhizobium robiniae sp. nov., isolated from root nodules of Robinia pseudoacacia. Int J Syst Evol Microbiol. 2010;60(11):2552–26.PubMedCrossRefGoogle Scholar
  407. Zhou S, Li Q, Jiang H, Lindström K, Zhang X. Mesorhizobium sangaii sp. nov., isolated from the root nodules of Astragalus luteolus and Astragalus ernestii. Int J Syst Evol Microbiol. 2013;63(8):2794–9.CrossRefGoogle Scholar
  408. Zhu YJ, Kun J, Chen YL, Wang SK, Sui XH, Kang LH. Mesorhizobium acaciae sp. nov., isolated from root nodules of Acacia melanoxylon R. Br. Int J Syst Evol Microbiol. 2015;65(10):3558–63.PubMedPubMedCentralCrossRefGoogle Scholar
  409. Zilli JE, Baraúna AC, da Silva K, De Meyer SE, Farias EN, Kaminski PE, da Costa IB, Ardley JK, Willems A, Camacho NN, Dourado Fdos S, O'Hara G. Bradyrhizobium neotropicale sp. nov., isolated from effective nodules of Centrolobium paraense. Int J Syst Evol Microbiol. 2014;64(12):3950–7.PubMedCrossRefGoogle Scholar
  410. Zurdo-Piñeiro JL, Rivas R, Trujillo ME, Vizcaíno N, Carrasco JA, Chamber M, Palomares A, Mateos PF, Martínez-Molina E, Velázquez E. Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int J Syst Evol Microbiol. 2007;57(4):784–8.PubMedCrossRefGoogle Scholar
  411. Zurdo-Piñeiro JL, García-Fraile P, Rivas R, Peix A, León-Barrios M, Willems A, Mateos PF, Martínez-Molina E, Velázquez E, van Berkum P. Rhizobia from Lanzarote, the Canary Islands, that nodulate Phaseolus vulgaris have characteristics in common with Sinorhizobium meliloti isolates from mainland Spain. Appl Environ Microbiol. 2009;75(8):2354–9.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • En Tao Wang
    • 1
  1. 1.Departamento de Microbiología, Escuela Nacional de Ciencias BiológicasInstituto Politécnico NacionalCiudad de MexicoMexico

Personalised recommendations