Antonie van Leeuwenhoek

, Volume 112, Issue 4, pp 501–512 | Cite as

Response of the microbial community associated with sweet potato (Ipomoea batatas) to Bacillus safensis and Bacillus velezensis strains

  • Jackeline Rossetti Mateus
  • Joana Montezano Marques
  • Isabella Dal’Rio
  • Renata Estebanez Vollú
  • Marcia Reed Rodrigues Coelho
  • Lucy SeldinEmail author
Original Paper


Sweet potato is a subsistence crop cultivated worldwide. Although it is generally considered tolerant to different diseases, it is quite susceptible to the fungus Plenodomus destruens that causes foot-rot disease. Plant growth-promoting bacteria associated with sweet potato remain poorly studied, but some Bacillus strains may have potential as biological control agents. Here, we evaluate the persistence of two bacterial strains—Bacillus safensis T052-76 and Bacillus velezensis T149-19—in pot experiments and assess their impact on indigenous bacterial and fungal communities associated with sweet potato. Numbers of cells of both strains introduced into pots remained stable in the rhizosphere of sweet potato over the 180-day experiment. Denaturing gradient gel electrophoresis based on the rrs gene encoding bacterial 16S rRNA and the fungal ribosomal internal transcribed spacer region showed that bands corresponding to the introduced strains were not detected in plant endosphere. PERMANOVA and non-metric multidimensional scaling statistical analyses showed that: (1) strain T052-76 altered the structure of the indigenous bacterial community (rhizosphere and soil) more than strain T149-19; (2) T052-76 slightly altered the structure of the indigenous fungal community (rhizosphere and soil) and (3) strain T149-19 did not disturb the fungal community. Our results demonstrate the stability of both Bacillus strains in the sweet potato rhizosphere and, apart from the influence of B. safensis T052-76 on the bacterial community, their limited impact on the microbial community associated with this important crop plant.


Sweet potato Bacillus safensis Bacillus velezensis Microbial community 



We are grateful to Dr. Viviane Talamine (EMBRAPA Tabuleiros Costeiros, Aracaju, SE) for providing the Plenodomus destruens strain used here.


This study was supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10482_2018_1181_MOESM1_ESM.pdf (695 kb)
Supplementary material 1 (PDF 694 kb)


  1. Agarwal M, Dheeman S, Dubey RC, Kumar P, Maheshwari DK, Bajpai VK (2017) Differential antagonistic responses of Bacillus pumilus MSUA3 against Rhizoctonia solani and Fusarium oxysporum causing fungal diseases in Fagopyrum esculentum Moench. Microbiol Res 205:40–47CrossRefPubMedGoogle Scholar
  2. Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350CrossRefPubMedGoogle Scholar
  3. Cao Y, Pi H, Chandrangsu P, Li Y, Wang Y, Zhou H, Xiong H, Helmann JD, Cai Y (2018) Antagonism of two plant-growth promoting Bacillus velezensis isolates against Ralstonia solanacearum and Fusarium oxysporum. Sci Rep 8:4360CrossRefPubMedPubMedCentralGoogle Scholar
  4. Castro-Sowinski S, Herschkovitz Y, Okon Y, Jurkevitch E (2007) Effects of inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms. FEMS Microbiol Lett 276:1–11CrossRefPubMedGoogle Scholar
  5. Chen L, Heng J, Qin S, Bian K (2018) A comprehensive understanding of the biocontrol potential of Bacillus velezensis LM2303 against Fusarium head blight. PLoS ONE 13(6):e0198560CrossRefPubMedPubMedCentralGoogle Scholar
  6. Dawwam GE, Elbeltagy A, Emara HM, Abbas IH, Hassan MM (2013) Beneficial effect of plant growth promoting bacteria isolated from the roots of potato plant. Ann Agric Sci 58:195–201CrossRefGoogle Scholar
  7. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. CRC Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  8. Dunlap CA, Kim SJ, Kwon SW, Rooney AP (2016) Bacillus velezensis is not a later heterotypic synonym of Bacillus amyloliquefaciens; Bacillus methylotrophicus, Bacillus amyloliquefaciens subsp. plantarum and ‘Bacillus oryzicola’ are later heterotypic synonyms of Bacillus velezensis based on phylogenomics. Int J Syst Evol Microbiol 66:1212–1217CrossRefPubMedGoogle Scholar
  9. El Sheikha AF, Ray RC (2017) Potential impacts of bioprocessing of sweet potato: review. Crit Rev Food Sci Nutr 57:455–471CrossRefPubMedGoogle Scholar
  10. Erlacher A, Cardinale M, Grosch R, Grube M, Berg G (2014) The impact of the pathogen Rhizoctonia solani and its beneficial counterpart Bacillus amyloliquefaciens on the indigenous lettuce microbiome. Front Microbiol 5:175CrossRefPubMedPubMedCentralGoogle Scholar
  11. Farzana Y, Radziah O, Kamaruza-man S, Saad MS (2007) Effect of PGPR inoculation on growth and yield of sweet potato. J Biol Sci 7:421–424CrossRefGoogle Scholar
  12. Farzana Y, Radziah O, Kamaruza-man S, Saad MS (2009) Characterization of beneficial properties of plant growth-promoting rhizobacteria isolated from sweet potato rhizosphere. Afr J Microbiol Res 3:815–821Google Scholar
  13. Fischer SE, Jofre EC, Cordero PV, Manero FJG, Mori GB (2010) Survival of native Pseudomonas in soil and wheat rhizosphere and antagonist activity against plant pathogenic fungi. Antonie Van Leeuwenhoek 97:241–251CrossRefPubMedGoogle Scholar
  14. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhiza and rusts. Mol Ecol 2:113–118CrossRefGoogle Scholar
  15. Grosch R, Dealtry S, Schreiter S, Berg G, Mendoça-Hagler L, Smalla K (2012) Biocontrol of Rhizoctonia solani: complex interaction of biocontrol strains, pathogen and indigenous microbial community in the rhizosphere of lettuce shown by molecular methods. Plant Soil 360:343–357CrossRefGoogle Scholar
  16. Hammer Ø, Harper DAT, Ryan PD (2001) Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9–18Google Scholar
  17. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241PubMedPubMedCentralGoogle Scholar
  18. Islam S, Akanda AM, Prova A, Islam MDT, Hossain MDM (2016) Isolation and identification of plant growth promoting rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front Microbiol 6:1360CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kennedy C (1999) Bacterial diversity in agroecosystems. Agric Ecosyst Environ 74:65–76CrossRefGoogle Scholar
  20. Kumar S, Stecher G, Tamura K (2016) MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedPubMedCentralGoogle Scholar
  21. Laurie SM, Calitz FJ, Adebola PO, Lezar A (2013) Characterization and evaluation of South African sweet potato (Ipomoea batatas (L.) LAM) land races. S Afr J Bot 85:10–16CrossRefGoogle Scholar
  22. Lebot V (2009) Tropical root and tuber crops: cassava, sweet potato, yams and aroids, vol 17. Crop production science in horticulture series, chapter 13. CABI, Oxfordshire, pp 151–167Google Scholar
  23. Lopes CA, Silva JBC (1993) Management measures to control foot rot of sweet potato caused by Plenodomus destruens. Int J Pest Manag 39:72–74CrossRefGoogle Scholar
  24. Marques JM, Da Silva TF, Vollú RE, Blank AF, Ding GC, Seldin L, Smalla K (2014) Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. FEMS Microbiol Ecol 88:424–435CrossRefPubMedGoogle Scholar
  25. Marques JM, Da Silva TF, Vollú RE, De Lacerda JRM, Blank AF, Smalla K, Seldin L (2015) Bacterial endophytes of sweet potato tuberous roots affected by the plant genotype and growth stage. Appl Soil Ecol 96:273–281CrossRefGoogle Scholar
  26. Massol-Deya AA, Odelson DA, Hickey RF, Tiedje JM (1995) Bacterial community fingerprinting of amplified 16S and 16S-23S ribosomal DNA gene sequences and restriction endonuclease analysis (ARDRA). In: Akkermans ADL, Van Elsas JD, Bruijn FJ (eds) Molecular microbiology ecology manual. Kluwer Academic Publishers, Dordrecht, pp 1–18Google Scholar
  27. Mayer FL, Kronstad JW (2017) Disarming fungal pathogens: Bacillus safensis inhibits virulence factor production and biofilm formation by Cryptococcus neoformans and Candida albicans. mBio 8(5):e01537-17CrossRefPubMedPubMedCentralGoogle Scholar
  28. Monteiro JM, Vollú RE, Coelho MRR, Alviano CS, Blank AF, Seldin L (2009) Culture-dependent and -independent approaches to analyze the bacterial community of different genotypes of Chrysopogon zizanioides (L.) Roberty (vetiver) rhizospheres. J Microbiol 47:363–370CrossRefPubMedGoogle Scholar
  29. Müller H, Berg C, Landa BB, Auerbach A, Moissl-Eichinger C, Berg G (2015) Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Front Microbiol 6:138CrossRefPubMedPubMedCentralGoogle Scholar
  30. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial population by denaturing gradient gel eletrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700PubMedPubMedCentralGoogle Scholar
  31. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  32. Nübel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNA in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643CrossRefPubMedPubMedCentralGoogle Scholar
  33. Palazzini JM, Dunlap CA, Bowman MJ, Chulze SN (2016) Bacillus velezensis RC 218 as a biocontrol agent to reduce Fusarium head blight and deoxynivalenol accumulation: genome sequencing and secondary metabolite cluster profiles. Microbiol Res 192:30–36CrossRefPubMedGoogle Scholar
  34. Pereira RB, Fernandes FR, Pinheiro JB (2011) Recomendações para manejo da podridão-do-pé em batata-doce, in: Comunicado Técnico no 79, Embrapa Hortaliças, Brasília, DFGoogle Scholar
  35. Probanza A, Lucas García JA, Ruiz Palomino M, Ramos B, Gutiérrez Mañero FJ (2002) Pinus pinea L. seedling growth and bacterial rhizosphere structure after inoculation with PGPR Bacillus (B. licheniformis CECT 5106 and B. pumilus CECT 5105). Appl Soil Ecol 20:75–84CrossRefGoogle Scholar
  36. Rais A, Jabeen Z, Shair F, Hafeez FY, Hassan MN (2017) Bacillus spp., a bio-control agent enhances the activity of antioxidant defense enzymes in rice against Pyricularia oryzae. PLoS One 12(11):e0187412CrossRefPubMedPubMedCentralGoogle Scholar
  37. Reddy PP (2015) Plant protection in tropical root and tuber crops. Springer, New Delhi, p 331CrossRefGoogle Scholar
  38. Rooney AP, Price NP, Ehrhardt C, Swezey JL, Bannan JD (2009) Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquosorum subsp. nov. Int J Syst Evol Microbiol 59:2429–2436CrossRefPubMedGoogle Scholar
  39. Ryder MH, Pankhurst CE, Rovira AD, Correll RL, Ophel Keller KM (1994) Detection of introduced bacteria in the rhizosphere using marker genes and DNA probes. In: O’Gara F, Dowling D, Boesten B (eds) Molecular ecology of rhizosphere microorganisms. VCH Publishers, Weinheim, pp 29–47CrossRefGoogle Scholar
  40. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  41. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  42. Scherwinski K, Grosch R, Berg G (2008) Effect of bacterial antagonists on lettuce: active biocontrol of Rhizoctonia solani and negligible, short-term effects on non-target microorganisms. FEMS Microbiol Ecol 64:106–116CrossRefPubMedGoogle Scholar
  43. Silva JBC, Lopes CA, Magalhães JS (2008) Batata-doce (Ipomoea batatas), in: Sistemas de Produção no 6, versão eletrônica. Embrapa Hortaliças, Brasília, DFGoogle Scholar
  44. Smit E, Leeflang P, Glandorf B, Van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65:2614–2621PubMedPubMedCentralGoogle Scholar
  45. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  46. Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int 2013:863240CrossRefPubMedPubMedCentralGoogle Scholar
  47. Troxler J, Svercel M, Natsch A, Zala M, Keel C, Moënne-Loccoz Y, Défago G (2012) Persistence of a biocontrol Pseudomonas inoculant as high populations of culturable and non-culturable cells in 200-cm-deep soil profiles. Soil Biol Biochem 44:122–129CrossRefGoogle Scholar
  48. Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21(5):573CrossRefPubMedCentralGoogle Scholar
  49. Versalovic J, Schneider M, De Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40Google Scholar
  50. White TJ, Bruns TD, Lee SB, Taylor JW (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  51. Xiang N, Lawrence KS, Kloepper JW, Donald PA, McInroy JA (2017) Biological control of Heterodera glycines by spore-forming plant growth-promoting rhizobacteria (PGPR) on soybean. PLoS ONE 12(7):e0181201CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Laboratório de Genética Microbiana, Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de GóesUniversidade Federal do Rio de Janeiro, Centro de Ciências da SaúdeRio de JaneiroBrazil
  2. 2.Instituto de Ciências Biológicas, Centro de Genômica e Biologia de SistemasUniversidade Federal do ParáBelémBrazil
  3. 3.Empresa Brasileira de Pesquisa AgropecuáriaCentro Nacional de Pesquisa de AgrobiologiaSeropédicaBrazil

Personalised recommendations