[Review article] The role of biofilm formation by plant-associated beneficial bacteria in reducing the damage of plant pathogens

Document Type : Review Paper

Author

Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran.

Abstract

Beneficial bacteria protect the plants against pathogens in various strategies. Some of these strategies are included the production of secondary metabolites such as antibiotics, volatile organic compounds and siderophores, plant resistance induction and promoting the plant growth parameters. In recent years, biofilm production has been considered as one of the important features in the survival of plant beneficial bacteria. A biofilm is a community of one or more bacterial species surrounded by polymeric materials. In addition to bacteria, fungi, algae and protozoa may be found in the biofilm. Living in biofilms has many benefits for antagonistic bacteria. Biofilm protects bacteria against adverse nutritional conditions, shortage of available oxygen, high osmotic pressure, sudden changes in temperature and pH, drought stress and antimicrobial compounds such as antibiotics and chlorine compounds. In addition to enhancing the production of effective secondary metabolites in disease biocontrol in biofilm, its matrix provides complete protection of these compounds. Concerning the importance of forming complete and three–dimensional biofilms by beneficial bacteria, and its positive effects on increasing their biocontrol capability, it is suggested that this feature be considered in the screening of beneficial bacteria to select effective strains in biocontrol of plant diseases and their use in commercial production.

Keywords

References

Abd El Daim, I., Haggblom, P., Karlsson, M., Stenstrom, E. & Timmusk, S. 2015. Paenibacillus polymyxa A26 Sfp type PPTase inactivation limits bacterial antagonism against Fusarium graminearum but not of F. culmorum in kernel assay. Frontiers in Plant Science, 6: 368. doi: 10.3389/fpls.2015.00368.
Abdian, P. & Zorreguieta, A. 2016. Extracellular factors involved in biofilm matrix formation by Rhizobia. pp. 227–247. In Flemming, H.C., Neu, T.R. & Wingender, J. (eds). The Perfect Slime–Microbial Extracellular Polymeric Substances (EPS). IWA Publishing, London.
Abeer, H., Tabassum, B. & Abd–Allah, E.F. 2019. Bacillus subtilis: A plant–growth promoting rhizobacterium that also impacts biotic stress. Saudi Journal of Biological Sciences, 26: 6. doi: 10.1016/j.sjbs.2019.05.004.
Alam, K., Al Farraj, D.A., Mah–e–Fatima, S., Yameen, M.A., Elshikh, M.S., Alkufeidy, R.M., El–Zaher, A., Mustafa, M.A., Bhasme, P., Alshammari, M.K., Alkubaisi, N.A., Abbasi, A.M. & Naqvi, T.A. 2020. Anti–biofilm activity of plant derived extracts against pathogen–Pseudomonas aeruginosa PAO1. Journal of Infections and Public Health, 13: 1734–1741.
Aleti, G., Lehner, S., Bacher, M., Compant, S., Nikolic, B., Plesko, M., Schuhmacher, R., Sessitsch, A. & Brader, G.  2016. Surfactin variants mediate species–specific biofilm formation and root colonization in Bacillus. Environmental Microbiology, 18: 2634–2645.
Ansari, F.A. & Ahmad, I. 2019. Fluorescent Pseudomonas –FAP2 and Bacillus licheniformis interact positively in biofilm mode enhancing plant growth and photosynthetic attributes. Science Reports, 9: 4547. doi: 10.1038/s41598–019–40864–4.
Audrain, B., Farag, M.A., Ryu, C.M. & Ghigo, J.M. 2015. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiology Reviews, 39: 222–233.
Bais, H.P., Fall, R. & Vivanco, J.M. 2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiology, 134: 307–319.
Bisht, K., Moore, J.L., Caprioli, R.M., Skaar, E.P. & Wakeman, C.A. 2021. Impact of temperature–dependent phage expression on Pseudomonas aeruginosa biofilm formation. npj Biofilms and Microbiomes, 7: 22. doi: 10.1038/s41522–021–00194–8.
Blake, C., Christensen, M.N. & Kovacs, A.T. 2021. Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Molecular Plant–Microbe Interactions Journal, 34(1): 15–25.
Bogino, P.C., Oliva, M. de.las.M., Sorroche, F.G. & Giordano, W. 2013. The role of bacterial biofilms and surface components in plant–bacterial associations. International Journal of Molecular Sciences, 14: 15838–15859.
Boyd, C.D., Smith, T.J., El–Kirat–Chatel, S., Newell, P.D., Dufrêne, Y.F. & O’Toole, G.A. 2014. Structural features of the Pseudomonas fluorescens biofilm adhesin LapA required for LapG–dependent cleavage, biofilm formation and cell surface localization.  Journal of Bacteriology, 196: 2775–2788.
Chi, M., Li, G., Liu, Y., Liu, G., Li, M., Zhang, X., Sun, Z., Sui, Y. & Liu, J. 2015. Increase in antioxidant enzyme activity, stress tolerance and biocontrol efficacy of Pichia kudriavzevii with the transition from a yeast–like to biofilm morphology. Biological Control, 90: 113–119.
Davey, M.E. & O’Toole, G.A. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews, 64: 847–867.
De la Fuente, M., Vidal, J.M., Miranda, C.D., Gonzalez, G. & Urrutia, H. 2013. Inhibition of Flavobacterium psychrophilum biofilm formation using a biofilm of the antagonist Pseudomonas fluorescens FF48. SpringerPlus, 2: 176.
Dergham, Y., Sanchez–Vizuete, P., Le Coq, D., Deschamps, J., Bridier, A., Hamze, K. & Briandet, R. 2021. Comparison of the genetic features involved in Bacillus subtilis biofilm formation using multi–culturing approaches. Microorganisms, 9: 633. doi:10.3390/ microorganisms9030633.
Diaz Herrera, S., Grossi, C., Zawoznik, M. & Groppa, M.D. 2016. Wheat seeds harbor bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiological Research, 186–187: 37–43.
Dubern, J.F. & Diggle, S.P. 2008. Quorum sensing by 2–alkyl–4–quinolones in Pseudomonas aeruginosa and other bacterial species. Molecular Biosystems, 4 (9): 882–888.
Farag, M.A., Ryu, C.M., Sumner, L.W. & Pare, P.W. 2006. GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry, 67: 2262–2268.
Fiddaman, P.J. & Rossal, S. 1994. Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. Journal of Applied Microbiology, 76: 395–405.
Flemming, H.C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S.A. & Kjelleberg, S. 2016. Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology, 14: 563–575.
Haggag, W.M. & Timmusk, S. 2008. Colonization of peanut roots by biofilm–forming Paenibacillus polymyxa initiates biocontrol against crown rot disease. Journal of Applied Microbiology, 104: 961–969.
Haque, M.M., Mosharaf, M.K., Khatun, M., Haque, M.A., Biswas, M.S., Islam, M.S., Islam, M.M., Shozib, H.B., Miah, M.M.U., Molla, A.H. & Siddiquee, M.A. 2020. Biofilm producing rhizobacteria with multiple plant growth–promoting traits promote growth of tomato under water–deficit stress. Frontiers in Microbiology, 11: 542053. doi: 10.3389/fmicb.2020.542053.
Jamil, B., Hasan, F., Hameed, A. & Ahmed, S. 2007. Isolation of Bacillus subtilis MH–4 from soil and its potential of polypeptidic antibiotic production. Pakistan Journal of Pharmaceutical Sciences, 20: 26–31.
Khelissa, S.O., Abdallah, M., Jama, C., Faille, C. & Chihib, N.E. 2017. Bacterial contamination and biofilm formation on abiotic surfaces and strategies to overcome their persistence. Journal of Materials and Environmental Science, 8 (9): 3326–3346.
Khezri, M. 2019. The effects of biofilm formation in bacteria from different perspectives. Nova Biologica Reperta, 6 (1): 70–78. (In Persian with English summary)
Khezri, M. 2017a. Biological control of wheat take–all disease using some biofilm–forming Bacillus subtilis strains. Biocontrol in Plant Protection, 5(1): 15–30. (In Persian with English summary)
Khezri, M. 2017b. Effect of biofilm by plant probiotic rhizobacteria on root colonization and growth of wheat. Biological Control of Pest and Plant Diseases, 6(1): 93–102. (In Persian with English summary)
Khezri, M. 2016. Influence of some environmental and nutritional conditions on biofilm formation of probiotic Bacillus subtilis strains. Biological Control of Pest and Plant Diseases, 4(2): 157–165. (In Persian with English summary)
Khezri, M., Ahmadzadeh, M., Salehi Jozani, Gh. & Sharifi, R. 2016a. A new gene involving in biofilm formation of Bacillus subtilis. Modern Genetics Journal, 11(2): 245–259. (In Persian with English summary)
Khezri, M., Ahmadzadeh, M. & Salehi–Jouzani, Gh. 2016b. Fusarium culmorum affects expression of biofilm formation key genes in Bacillus subtilis. Brazilian Journal of Microbiology, 47: 47–54.
Khezri, M., Ahmadzadeh, M., Salehi–Jouzani, Gh., Behboudi, K., Ahangaran, A., Mousivand, M. & Rahimian, H. 2011. Characterization of some biofilm–forming Bacillus subtilis and evaluation of their biocontrol potential against Fusarium culmorum. Journal of Plant Pathology, 93: 373–382.
Kovács, A.T., Smits, W.K., Miron´czuk, A.M. & Kuipers, O.P. 2009. Ubiquitous late competence genes in Bacillus species indicate the presence of functional DNA uptake machineries. Environmental Microbiology, 11: 1911–1922.
Krober, M., Verwaaijen, B., Wibberg, D., Winkler, A., Puhler, A. & Schluter, A. 2016. Comparative transcriptome analysis of the biocontrol strain Bacillus amyloliquefaciens FZB42 as response to biofilm formation analyzed by RNA sequencing. Journal of Biotechnology, 231: 212–223.
Mark, G.L., Dow, J.M., Kiely, P.D., Higgins, H., Haynes, J., Baysse, C., Abbas, A., Foley, T., Franks, A., Morrissey, J. & O'Gara, F. 2005. Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe–plant interactions. Proceedings of the National Academy of Sciences of the United States of America, 102: 17454–17459.
Melville, S. & Craig, L. 2013. Type IV pili in gram–positive bacteria. Microbiology and Molecular Biology Reviews, 77: 323–341.
Molina, M.A., Ramos, J.L. & Urgel, M. E. 2003. Plant–associated biofilms. Reviews in Environmental Science and Biotechnology, 2: 99–108.
Morcillo, R.J.L. & Manzanera, M. 2021. The effects of plant–associated bacterial exopolysaccharides on plant abiotic stress tolerance. Metabolites, 11: 337. doi: 10.3390/metabo11060337.
Morikawa, M. 2006. Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. Journal of Bioscience and Bioengineering, 101: 1–8.
Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J. L. & Thonart, P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental Microbiology, 9: 1084–1090.
Pandin, C., Le Coq, D., Canette, A., Aymerich, S. & Briandet, R. 2017. Should the biofilm mode of life be taken into consideration for microbial biocontrol agents? Microbial Biotechnology, 10(4): 719–734.
Prigent–Combaret, C., Vidal, O., Dorel, C. & Lejeune, P. 1999. Abiotic surface sensing and biofilm–dependent regulation of gene expression in Escherichia coli. Journal of Bacteriology, 181: 5993–6002.
Prigent–Combaret, C., Zghidi–Abouzid, O., Effantin, G., Lejeune, P., Reverchon, S. & Nasser, W. 2012. The nucleoid–associated protein Fis directly modulates the synthesis of cellulose, an essential component of pellicle–biofilms in the phytopathogenic bacterium Dickeya dadantii. Molecular Microbiology, 86: 172–186.
Prindle, A., Liu, J., Asally, M., Ly, S., Garcia–Ojalvo, J. & Suel, G.M. 2015. Ion channels enable electrical communication in bacterial communities. Nature, 527: 59–63.
Rajendran, A. & Hu, B. 2016. Mycoalgae biofilm: development of a novel platform technology using algae and fungal cultures. Biotechnology for Biofuels, 9: 112.
Raza, W., Ling, N., Yang, L., Huang, Q. & Shen, Q. 2016. Response of tomato wilt pathogen Ralstonia solanacearum to the volatile organic compounds produced by a biocontrol strain Bacillus amyloliquefaciens SQR–9. Scientific Reports, 6: 24856.
Rendueles, O. & Ghigo, J.M. 2015. Mechanisms of competition in biofilm communities. Microbiology Spectrum, 3: 3. doi: 10.1128/microbiolspec. MB–0009–2014.
Rieusset, L., Rey, M., Muller, D., Vacheron, J., Gerin, F., Dubost, A., Comte, G. & Prigent–Combaret, C. 2020. Secondary metabolites from plant–associated Pseudomonas are overproduced in biofilm. Microbial Biotechnology, 13(5): 1562–1580.
Sabuquillo, P. & Cubero, J. 2021. Biofilm formation in Xanthomonas arboricola pv. pruni: structure and development. Agronomy, 11: 546. doi: 10.3390/agronomy11030546.
Selin, C., Habibian, R., Poritsanos, N., Athukorala, S.N.P., Fernando, D. & de Kievit, T.R. 2010. Phenazines are not essential for Pseudomonas chlororaphis PA23 biocontrol of Sclerotinia sclerotiorum, but do play a role in biofilm formation. FEMS Microbiology Ecology, 71: 73–83.
Sheppard, D.C. & Howell, P.L. 2016. Biofilm exopolysaccharides of pathogenic fungi: lessons from bacteria. Journal of Biological Chemistry, 291: 12529–12537.
Soares, R.O., Fedi, A.C., Reiter, K.C., Caierão, J. & d'Azevedo, P.A. 2014. Correlation between biofilm formation and gelE, esp, and agg genes in Enterococcus spp. clinical isolates. Virulence, 5: 634–637.
Stanley, N.R., Britton, R.A., Grossman, A.D. & Lazazzera, B.A. 2003. Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. Journal of Bacteriology, 185: 1951–1957. 38.
Timmusk, S., Copolovici, D., Copolovici, L., Teder, T., Nevo, E. & Behers, L. 2019. Paenibacillus polymyxa biofilm polysaccharides antagonise Fusarium graminearum. 9: 662. doi: 10.1038/s41598–018–37718–w.
Wang, X., Koehler, S.A., Wilking, J.N., Sinha, N.N., Cabeen, M.T., Srinivasan, S., Seminara, A., Rubinstein, S., Sun, Q., Brenner, M.P. & Weitz, D.A. 2016. Probing phenotypic growth in expanding Bacillus subtilis biofilms. Applied Microbiology and Biotechnology, 100: 4607–4615.
Wu, K., Fang, Z., Guo, R., Pan, B., Shi, W., Yuan, S., Guan, H., Gong, M., Shen, B. & Shen, Q. 2015. Pectin enhances bio–control efficacy by inducing colonization and secretion of secondary metabolites by Bacillus amyloliquefaciens SQY 162 in the rhizosphere of tobacco. PLoS ONE, 10: e 0127418.
Xu, S., Yang, N., Zheng, S., Yan, F., Jiang, C., Yu, Y., Guo, J., Chai, Y. & Chen, Y. 2017. The spo0A–sinI–sinR regulatory circuit plays an essential role in biofilm formation, nematicidal, activities, and plant protection in Bacillus cereus AR156. Molecular Plant–Microbe Interactions Journal, 30(8): 603–619.
Yadav, M.K. 2017. Role of biofilms in environment pollution and control. pp: 377–398. In: Patra, J., Vishnuprasad, C. & D’as, G. (eds.). Microbial Biotechnology. Springer Nature, Singapore.
Zhang, N., Yang, D., Wang, D., Miao, Y., Shao, J., Zhou, X., Xu, Z., Li, Q., Feng, H., Li, S., Shen, Q. & Zhang, R. 2015. Whole transcriptomic analysis of the plant–beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 during enhanced biofilm formation regulated by maize root exudates. BMC Genomics, 16: 685.
Zhu, M.L., Wu, X.Q., Wang, Y.H. & Dai, Y. 2020. Role of biofilm formation by Bacillus pumilus HR10 in biocontrol against pine seedling damping–off disease caused by Rhizoctonia solani. Forests, 11: 652. doi:10.3390/f11060652.Zhou, H., Luo, C., Fang, X., Xiang, Y., Wang, X., Zhang, R. & Chen, Z. 2016. Loss of gltb inhibits biofilm formation and biocontrol efficiency of Bacillus subtilis Bs916 by altering the production of c–polyglutamate and three lipopeptides. PLoS ONE, 11: 1–20.

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