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Environmental Science and Pollution Research

, Volume 25, Issue 30, pp 29910–29920 | Cite as

Biofilm formation is determinant in tomato rhizosphere colonization by Bacillus velezensis FZB42

  • Ameen Al-Ali
  • Jovana Deravel
  • François Krier
  • Max Béchet
  • Marc Ongena
  • Philippe Jacques
Chemistry, Activity and Impact of Plant Biocontrol products

Abstract

In this work, the behavior in tomato rhizosphere of Bacillus velezensis FZB42 was analyzed taking into account the surfactin production, the use of tomato roots exudate as substrates, and the biofilm formation. B. velezensis FZB42 and B. amyloliquefaciens S499 have a similar capability to colonize tomato rhizosphere. Little difference in this colonization was observed with surfactin non producing B. velezensis FZB42 mutant strains. B. velezensis is able to grow in the presence of root exudate and used preferentially sucrose, maltose, glutamic, and malic acids as carbon sources. A mutant enable to produce exopolysaccharide (EPS-) was constructed to demonstrate the main importance of biofilm formation on rhizosphere colonization. This mutant had completely lost its ability to form biofilm whatever the substrate present in the culture medium and was unable to efficiently colonize tomato rhizosphere.

Keywords

Rhizosphere Colonization Bacillus Lipopeptides Root exudates Biofilm 

Notes

Acknowledgements

The authors thank Dr. Rainer Borriss for kindly providing the Bacillus velezensis strains.

Funding information

This work was supported by the University of Lille 1 Sciences and Technologies, the European Funds of INTERREG IV PhytoBio Project and of INTERREG V Smartbiocontrol portfolio, BioProd project and the CPER FEDER project ALIBIOTECH. The authors thank the REALCAT platform for the use of BioLector in this work. The REALCAT platform is benefiting from a state subsidy administrated by the French National Research Agency (ANR) within the frame of the ‘Future Investments’ program (PIA), with the contractual reference ‘ANR-11-EQPX-0037’. The European Union, through the ERDF funding administered by the Hauts-de-France Region, has co-financed the platform. Centrale Lille, the CNRS, and Lille 1 University as well as the Centrale Initiatives Foundation, are thanked for their financial contributions to the acquisition and implementation of the equipment of the REALCAT platform. Ameen Al-Ali was a recipient of PhD scholarship awarded by Campus France through joint French-Iraqi governments program.

References

  1. Allison DG, Sutherland IW (1987) The role of exopolysaccharides in adhesion of freshwater bacteria. J Gen Microbiol 133:1319–1327.  https://doi.org/10.1099/00221287-133-5-1319 CrossRefGoogle Scholar
  2. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681.  https://doi.org/10.1111/j.1365-3040.2009.01926.x CrossRefGoogle Scholar
  3. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319.  https://doi.org/10.1104/pp.103.028712 CrossRefGoogle Scholar
  4. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83.  https://doi.org/10.1023/A:1026290508166 CrossRefGoogle Scholar
  5. Budiharjo A, Chowdhury SP, Dietel K, Beator B, Dolgova O, Fan B, Bleiss W, Ziegler J, Schmid M, Hartman A, Borriss R (2014) Transposon mutagenesis of the plant-associated Bacillus amyloliquefaciens ssp. plantarum FZB42 revealed that the nfrA and RBAM17410 genes are involved in plant- microbe-interactions. PLoS One 9(5):e98267.  https://doi.org/10.1371/journal.pone.0098267 CrossRefGoogle Scholar
  6. Cao G, Zhang X, Zhong L, Lu Z (2011) A modified electro-transformation method for Bacillus subtilis and its application in the production of antimicrobial lipopeptides. Biotechnol Lett 33:1047–1051.  https://doi.org/10.1007/s10529-011-0531-x CrossRefGoogle Scholar
  7. Chen XH, Koumoutsi1 A, Scholz R, Eisenreich1 A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Sussmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol (9):1007–1014.  https://doi.org/10.1038/nbt1325 CrossRefGoogle Scholar
  8. Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513.  https://doi.org/10.1016/j.micres.2008.08.007 CrossRefGoogle Scholar
  9. Das BB, Dkhar MS (2011) Rhizosphere microbial populations and physico chemical properties as affected by organic and inorganic farming practices. Am Eur J Agric Environ Sci 10:140–150Google Scholar
  10. Davey ME, Caiazza NC, O'Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036.  https://doi.org/10.1128/JB.185.3.1027-1036.2003 CrossRefGoogle Scholar
  11. Deravel J, Lemiere S, Coutte F, Krier F, Van Hese N, Bechet M, Jacques P (2014) Mycosubtilin and surfactin are efficient, low ecotoxicity molecules for the biocontrol of lettuce downy mildew. Appl Microbiol Biotechnol 98:6255–6264.  https://doi.org/10.1007/s00253-014-5663-1 CrossRefGoogle Scholar
  12. Dietel K, Beator B, Budiharjo A, Fan B, Borris R (2013) Bacterial traits involved in colonization of Arabidopsis thaliana roots by Bacillus amyloliquefaciens FZB42. Plant Pathol J 29:59–66.  https://doi.org/10.5423/PPJ.OA.10.2012.0155 CrossRefGoogle Scholar
  13. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193.  https://doi.org/10.1128/CMR.15.2.167-193.2002 CrossRefGoogle Scholar
  14. Emmert EA, Handelsman J (1999) Biocontrol of plant disease: a Gram-positive perspective. FEMS Microbiol Lett 171:1–9.  https://doi.org/10.1111/j.1574-6968.1999.tb13405.x CrossRefGoogle Scholar
  15. Fan B, Chen XH, Budiharjo A, Bleiss W, Vater J, Borriss R (2011) Efficient colonization of plant roots by the plant growth promoting bacterium Bacillus amyloliquefaciens FZB42, engineered to express green fluorescent protein. J Biotechnol 151:303–311.  https://doi.org/10.1016/j.jbiotec.2010.12.022 CrossRefGoogle Scholar
  16. Fan B, Carvalhais LC, Becker A, Fedoseyenko D, von Wirén N, Borriss R (2012) Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol 12:116.  https://doi.org/10.1186/1471-2180-12-116 CrossRefGoogle Scholar
  17. Fan B, Blom J, Klenk HP, Borriss R (2017) Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis form an “operational group B. amyloliquefaciens” within the B. subtilis species complex. Front Microbiol 8:22.  https://doi.org/10.3389/fmicb.2017.00022 CrossRefGoogle Scholar
  18. Fang W, Hu JY, Ong SL (2009) Influence of phosphorus on biofilm formation in model drinking water distribution systems. J Appl Microbiol 106:1328–1335.  https://doi.org/10.1111/j.1365-2672.2008.04099.x CrossRefGoogle Scholar
  19. Farace G, Fernandez O, Jacquens L, Coutte F, Krier F, Jacques P, Clément C, Ait Barka E, Jacquard C, Dorey S (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol Plant Pathol 16(2):177–187.  https://doi.org/10.1111/mpp.12170 CrossRefGoogle Scholar
  20. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633.  https://doi.org/10.1038/nrmicro2415 CrossRefGoogle Scholar
  21. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189:7945–7947.  https://doi.org/10.1128/JB.00858-07 CrossRefGoogle Scholar
  22. Garcia-Gutierrez L, Zeriouh H, Romero D, Cubero J, Vicente A, Perez-Garcia A (2013) The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate-and salicylic acid-dependent defence responses. Microb Biotechnol 6:264–274.  https://doi.org/10.1111/1751-7915.12028 CrossRefGoogle Scholar
  23. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica:1–15.  https://doi.org/10.6064/2012/963401 CrossRefGoogle Scholar
  24. Hsueh YH, Somers EB, Lereclus D, Wong ACL (2006) Biofilm formation by Bacillus cereus is influenced by PlcR, a pleiotropic regulator. Appl Environ Microbiol 72:5089–5092.  https://doi.org/10.1128/AEM.00573-06 CrossRefGoogle Scholar
  25. Idris EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Borriss R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148:2097–2109.  https://doi.org/10.1099/00221287-148-7-2097 CrossRefGoogle Scholar
  26. Idris EE, Bochow H, Ross H, Borriss R (2004) Use of Bacillus subtilis as biocontrol agent. VI. Phytohormone-like action of culture filtrates prepared from plant growth-promoting Bacillus amyloliquefaciens FZB24, FZB42, FZB45 and Bacillus. Z Pflanzenkrankh Pflanzenschutz 111:583–597.  https://doi.org/10.1111/j.1574-6968.1999.tb13405.x CrossRefGoogle Scholar
  27. Jacques P, Hbid C, Destain J, Razafindralambo H, Paquot M, De Pauw E and Thonart P (1999) Optimization of biosurfactant lipopeptide production from Bacillus subtilis S499 by Plackett-Burman design. In Twentieth Symposium on Biotechnology for Fuels and Chemicals. Humana Press, pp 223–233Google Scholar
  28. Julkowska D, Obuchowski M, Holland IB, Séror SJ (2004) Branched swarming patterns on a synthetic medium formed by wild-type Bacillus subtilis strain 3610: detection of different cellular morphologies and constellations of cells as the complex architecture develops. Microbiology 150:1839–1849.  https://doi.org/10.1099/mic.0.27061-0 CrossRefGoogle Scholar
  29. Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266.  https://doi.org/10.1094/PHYTO.2004.94.11.1259 CrossRefGoogle Scholar
  30. Kohler J, Caravaca F, Carrasco L, Roldan A (2007) Interactions between a plant growth-promoting rhizobacterium, an AM fungus and a phosphate-solubilizing fungus in the rhizosphere of Lactuca sativa. Appl Soil Ecol 35:480–487.  https://doi.org/10.1016/j.apsoil.2006.10.006 CrossRefGoogle Scholar
  31. Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, Franke P, Vater J, Borris R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186:1084–1096.  https://doi.org/10.1128/JB.186.4.1084-1096.2004 CrossRefGoogle Scholar
  32. Leclerc H (2003) Relationships between common water bacteria and pathogens in drinking-water. Heterotrophic Plate Counts and Drinking-water Safety. IWA Publishing, London, pp 80–118Google Scholar
  33. Leclere V, Marti R, Béchet M, Fickers P, Jacques P (2006) The lipopeptides mycosubtilin and surfactin enhance spreading of Bacillus subtilis strains by their surface active properties. Arch Microbiol 186:475–483.  https://doi.org/10.1007/s00203-006-0163-z CrossRefGoogle Scholar
  34. Ling N, Raza W, Ma J, Huang Q, Shen Q (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Europ J Soil Biol 47:374–379.  https://doi.org/10.1016/j.ejsobi.2011.08.009 CrossRefGoogle Scholar
  35. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556.  https://doi.org/10.1146/annurev.micro.62.081307.162918 CrossRefGoogle Scholar
  36. Maget-Dana R, Thimon L, Peypoux F, Ptak M (1992) Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74:1047–1051.  https://doi.org/10.1016/0300-9084(92)90002-V CrossRefGoogle Scholar
  37. Makarewicz O, Dubrac S, Msadek T, Borriss R (2006) Dual role of the PhoPP response regulator: Bacillus amyloliquefaciens FZB45 phytase gene transcription is directed by positive and negative interactions with the phyC promoter. J Bacteriol 188:6953–6965.  https://doi.org/10.1128/JB.00681-06 CrossRefGoogle Scholar
  38. Mayer C, Moritz R, Kirschner C, Borchard W, Maibaum R, Wingender J, Flemming HC (1999) The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int J Biol Macromol 26:3–16.  https://doi.org/10.1016/S0141-8130(99)00057-4 CrossRefGoogle Scholar
  39. Molinatto G, Puopoloa G, Sonego P, Moretto M, Engelen K, Viti C, Ongena M, Pertota I (2016) Complete genome sequence of Bacillus amyloliquefaciens subsp. plantarum S499, a rhizobacterium that triggers plant defences and inhibits fungal phytopathogens. J Biotechnol 238:56–59.  https://doi.org/10.1016/j.jbiotec.2016.09.013 CrossRefGoogle Scholar
  40. Nongkhlaw FMW, Joshi SR (2014) Distribution pattern analysis of epiphytic bacteria on ethnomedicinal plant surfaces: a micrographical and molecular approach. J Microscopy Ultrastructure 2:34–40.  https://doi.org/10.1016/j.jmau.2014.02.003 CrossRefGoogle Scholar
  41. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125.  https://doi.org/10.1016/j.tim.2007.12.009 CrossRefGoogle Scholar
  42. Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Thonart P (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090.  https://doi.org/10.1111/j.1462-2920.2006.01202.x CrossRefGoogle Scholar
  43. Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils 51:403–415.  https://doi.org/10.1007/s00374-015-0996-1 CrossRefGoogle Scholar
  44. Ramey BE, Koutsoudi M, von Bodman SB, Fuqua C (2004) Biofilm formation in plant–microbe associations. Curr Opin Microbiol 7:602–609.  https://doi.org/10.1016/j.mib.2004.10.014 CrossRefGoogle Scholar
  45. Rudrappa T, Quinn WJ, Stanley-Wall NR, Bais HP (2007) A degradation product of the salicylic acid pathway triggers oxidative stress resulting in down-regulation of Bacillus subtilis biofilm formation on Arabidopsis thaliana roots. Planta 226:283–297.  https://doi.org/10.1007/s00425-007-0480-8 CrossRefGoogle Scholar
  46. Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30Google Scholar
  47. Scholz R, Vater J, Budiharjo A, Wang Z, He Y, Dietel K, Borriss R (2014) Amylocyclicin, a novel circular bacteriocin produced by Bacillus amyloliquefaciens FZB42. J Bacteriol 196:1842–1852.  https://doi.org/10.1128/JB.01474-14 CrossRefGoogle Scholar
  48. Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3–9.  https://doi.org/10.1099/00221287-147-1-3 CrossRefGoogle Scholar
  49. Swiecilo A, Zych-Wezyk I (2013) Bacterial stress response as an adaptation to life in a soil environment. Pol J Environ Stud 6:1577–1587Google Scholar
  50. Tan S, Yang C, Mei X, Shen S, Raza W, Shen Q, Xu Y (2013) The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl Soil Ecol 64:15–22.  https://doi.org/10.1016/j.apsoil.2012.10.011 CrossRefGoogle Scholar
  51. Van Loon LC, Bakker PAHM (2005) Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: PGPR: biocontrol and biofertilization. Springer, Netherlands, pp 39–66CrossRefGoogle Scholar
  52. Vancura V, Hanzlikova A (1972) Root exudates of plants: IV. Differences in chemical composition of seed and seedlings exudates. Plant Soil 36:271–282CrossRefGoogle Scholar
  53. Vancura V, Hovadik A (1965) Root exudates of plants: II. Composition of root exudates of some vegetables. Plant Soil 22:21–32CrossRefGoogle Scholar
  54. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586.  https://doi.org/10.1023/A:1026037216893 CrossRefGoogle Scholar
  55. Watnick PI, Kolter R (1999) Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol 34:586–595.  https://doi.org/10.1046/j.1365-2958.1999.01624.x CrossRefGoogle Scholar
  56. Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens 1. Annu Rev Phytopathol 40:309–348.  https://doi.org/10.1146/annurev.phyto.40.030402.110010 CrossRefGoogle Scholar
  57. Zhang GQ, Bao P, Zhang Y, Deng AH, Chen N, Wen TY (2011) Enhancing electro-transformation competency of recalcitrant Bacillus amyloliquefaciens by combining cell-wall weakening and cell-membrane fluidity disturbing. Anal Biochem 409:130–137.  https://doi.org/10.1016/j.ab.2010.10.013 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Ameen Al-Ali
    • 1
    • 2
  • Jovana Deravel
    • 1
  • François Krier
    • 1
  • Max Béchet
    • 1
  • Marc Ongena
    • 3
  • Philippe Jacques
    • 1
    • 3
  1. 1.Université Lille, INRA, ISA, Université Artois, Université Littoral Côte d’Opale, EA 7394-ICV Institut Charles ViolletteLilleFrance
  2. 2.College of Agriculture-Soil, Water and Environmental Research DepartmentAl-Qasim Green UniversityBabylonIraq
  3. 3.Terra Teaching and Research Centre, Microbial Processes and Interactions (MiPI)Gembloux Agro-Bio Tech, University of LiegeGemblouxBelgium

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