Antonie van Leeuwenhoek

, Volume 112, Issue 2, pp 319–327 | Cite as

Rhizobium album sp. nov., isolated from a propanil-contaminated soil

  • Ping Hang
  • Long Zhang
  • Xi-Yi Zhou
  • Qiang Hu
  • Jian-Dong JiangEmail author
Original Paper


A novel Gram-stain negative, facultatively anaerobic, non-spore-forming, motile and rod-shaped bacterium (NS-104T) was isolated from a propanil-contaminated soil in Nanjing, China. Growth occurred at pH 5.0–9.0 (optimum 6.0), 16–37 °C (optimum 30 °C) and in the presence of 0–2.0% (w/v) NaCl (optimum, without NaCl). Strain NS-104T showed high 16S rRNA gene sequence identity to Rhizobium azooxidifex DSM 100211T (96.7%). The phylogenetic analysis of the 16S rRNA gene as well as the housekeeping genes recA, atpD and glnA demonstrated that strain NS-104T belongs to the genus Rhizobium. Strain NS-104T did not form nodules on six different legumes, and the nodD, nodC and nifH genes were neither amplified by PCR nor found in the draft genome of strain NS-104T. The sole respiratory quinone was ubiquinone Q-10. The polar lipid profile included the major amounts phosphatidylmonomethylethanolamine, phosphatidylglycerol and moderate amounts of phosphatidylethanolamine, phosphatidylcholine, diphosphatidylglycerol and unidentified aminolipids. The major cellular fatty acids were C18:1ω7c (39.6%), C19:0 cyclo ω8c (29.8%) and C16:0 (11.5%). The G + C content of strain NS-104T was 61.9 mol%. Strain NS-104T therefore represents a new species, for which the name Rhizobium album sp. nov. is proposed, with the type strain NS-104T (= KCTC 62327T = CCTCC AB 2017250T).


Rhizobium album sp. nov. Gram-stain negative 16S rRNA gene The housekeeping genes 



This work was financially supported by Grants from the National Natural Science Foundation of China (31670111) and the National Key Research and Development Program of China (2016YFD0800203).

Conflict of interest

The authors declare that there are no conflicts of interest.

Supplementary material

10482_2018_1160_MOESM1_ESM.docx (861 kb)
Supplementary material 1 (DOCX 861 kb)


  1. Beveridge TJ, Lawrence JR, Murray RGE (2007) Sampling and staining for light microscopy. Methods Gen Mol Microbiol 3:19–33Google Scholar
  2. Breznak JA, Costilow RN (2007) Physicochemical factors in growth. Methods Gen Mol Bacteriol 3:309–329Google Scholar
  3. Chen WF (2016) Progress and perspective of systematics of rhizobia. Microbiology China 43(5):1095–1100Google Scholar
  4. Dall’Agnol RF, Ribeiro RA, Delamuta JR, Ormeño-Orrillo E, Rogel MA, Andrade DS, Matínez-Romero E, Hungria M (2014) 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 64:3222–3229CrossRefGoogle Scholar
  5. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefGoogle Scholar
  6. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  7. Frank B (1889) Über die Pilzsymbiose der Leguminosen. Ber Dtsch Bot Ges 7:332–346 (in German) Google Scholar
  8. Ghosh W, Roy P (2006) Mesorhizobium thiogangeticum sp. nov., a novel sulfur-oxidizing chemolithoautotroph from rhizosphere soil of an Indian tropical leguminous plant. Int J Syst Evol Microbiol 56(1):91–97CrossRefGoogle Scholar
  9. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721CrossRefGoogle Scholar
  10. Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Syst Zool 18:1–32CrossRefGoogle Scholar
  11. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874CrossRefGoogle Scholar
  12. Laguerre G, Nour SM, Macheret V, Sanjuan J, Drouin P, Amarger N (2001) Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 147:981–993CrossRefGoogle Scholar
  13. Lane DL (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  14. Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714CrossRefGoogle Scholar
  15. Li R, Zhu H, Ruan J, Qian W, Fang XD, Shi ZB, Li YR, Li ST, Shan G, Kristiansen K, Li SG, Yang HM, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272CrossRefGoogle Scholar
  16. Liu TY, Li Y Jr, Liu XX, Sui XH, Zhang XX, Wang ET, Chen WX, Chen WF, Puławska J (2012) Rhizobium cauense sp. nov., isolated from root nodules of the herbaceous legume Kummerowia stipulacea grown in campus lawn soil. Syst Appl Microbiol 35(7):415–420CrossRefGoogle Scholar
  17. Liu XM, Chen K, Meng C, Zhang L, Zhu JC, Huang X, Li SP, Jiang JD (2014) Pseudoxanthobacter liyangensis sp. nov., isolated from dichlorodiphenyltrichloroethane-contaminated soil. Int J Syst Evol Microbiol 64:3390–3394CrossRefGoogle Scholar
  18. Martens M, Delaere M, Coopman R, De Vos P, Gillis M, Willems A (2007) Multilocus sequence analysis of Ensifer and related taxa. Int J Syst Evol Microbiol 57:489–503CrossRefGoogle Scholar
  19. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241CrossRefGoogle Scholar
  20. Parag B, Sasikala Ch, Ramana ChV (2013) Molecular and culture dependent characterization of endolithic bacteria in two beach sand samples and description of Rhizobium endolithicum sp. nov. Antonie Van Leeuwenhoek 104:1235–1244CrossRefGoogle Scholar
  21. Ramírez-Bahena MH, García-Fraile P, Peix A, Valverde A, Rivas R, Igual JM, Mateos PF, Martínez-Molina E, Velázquez E (2008) 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 58:2484–2490CrossRefGoogle Scholar
  22. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  23. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. Technical Note 101. Newark, DE: MIDI IncGoogle Scholar
  24. Tamaoka J, Katayama-Fujimura Y, Kuraishi H (1983) Analysis of bacterial menaquinone mixtures by high performance liquid chromatography. J Appl Bacteriol 54:31–36CrossRefGoogle Scholar
  25. Tel-Zur N, Abbo S, Myslabodski D, Mizrahi Y (1999) Modified CTAB procedure for DNA isolation from epiphytic cacti of the genera Hylocereus and Selenicereus (Cactaceae). Plant Mol Biol Rep 17:249–254CrossRefGoogle Scholar
  26. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefGoogle Scholar
  27. Tighe SW, De Lajudie P, Dipietro K, Lindström K, Nick G, Jarvis BD (2000) 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 50:787–801CrossRefGoogle Scholar
  28. Tindall BJ (1990) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202CrossRefGoogle Scholar
  29. Tindall BJ, Sikorski J, Smibert RM, Kreig NR (2007) Phenotypic characterization and the principles of comparative systematics. Methods Gen Mol Microbiol 3:330–393Google Scholar
  30. Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995) Remarkable N2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. J Bacteriol 177:1414–1417CrossRefGoogle Scholar
  31. Undine B, Peter K, Stefanie P, Jürgen A, Andreas U (2016) Characterization of the N2O-producing soil bacterium Rhizobium azooxidifex sp. nov. Int J Syst Evol Microbiol 66:2354–2361CrossRefGoogle Scholar
  32. Vinuesa P, Silva C, Lorite MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martínez-Romero E (2005) 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 28:702–716CrossRefGoogle Scholar
  33. Yoon JH, Kang SJ, Yi HS, Oh TK, Ryu CM (2010) Rhizobium soli sp.nov., isolated from soil. Int J Syst Evol Microbiol 60:1387–1393CrossRefGoogle Scholar
  34. Zhang XX, Li BM, Wang HS, Sui XH, Ma XT, Hong Q, Jiang RB (2012) Rhizobium petrolearium sp. nov., isolated from oil-contaminated soil. Int J Syst Evol Microbiol 62:1871–1876CrossRefGoogle Scholar
  35. Zhang L, Song M, Cao Q, Wu S, Zhao Y, Huang JW, Chen K, Li SP, Xia ZY, Jiang JD (2015a) Camelimonas fluminis sp. nov., a cyhalothrin-degrading bacterium isolated from river water. Int J Syst Evol Microbiol 65:3109–3114CrossRefGoogle Scholar
  36. Zhang L, Song M, Chen XL, Xu RJ, Chen K, Li SP, Xia ZY, Jiang JD (2015b) Devosia honganensis sp. nov., isolated from the soil of a chemical factory. Antonie Van Leeuwenhoek 108:1301–1307CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Ping Hang
    • 1
  • Long Zhang
    • 1
  • Xi-Yi Zhou
    • 1
  • Qiang Hu
    • 1
  • Jian-Dong Jiang
    • 1
    Email author
  1. 1.Department of Microbiology, Key Lab of Microbiology for Agricultural Environment, Ministry of Agriculture, College of Life SciencesNanjing Agricultural UniversityNanjingPeople’s Republic of China

Personalised recommendations