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

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.