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Role of Iron Homeostasis in the Multispecies Biofilm Formation

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Abstract

Iron acquisition is of fundamental importance for microorganisms, since this metal is generally poorly bioavailable under natural conditions. Fe is mostly present as a ferric form in soils, which strongly limits its bioavailability, while most soil bacteria are tightly packed within multicellular communities named biofilms. This research showed that biofilm formation by a gram-positive bacterium Bacillus subtilis during the interactions with other microbial species was both essential to ensure Fe uptake from the environment and to maintain the cellular Fe homeostasis. The biofilm matrix appeared to play an important role, favoring the efficient usage of siderophores. Taken together, these results demonstrate a close link between biofilm formation and iron acquisition in B. subtilis and Escherichia coli, allowing a better comprehension of how bacteria can cope with metal limitation under environmental conditions.

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REFERENCES

  1. Ahemad, M. and Kibret, M., Mechanisms and applications of plant growth promoting rhizobacteria: current perspective, J King Saud Univ.–Science, 2014, vol. 26, pp. 1–20.

    Google Scholar 

  2. Adnan, M., Morton, G., Singh, J., and Hadi, S., Contribution of rpoS and bolA genes in biofilm formation in Escherichia coli K-12 MG1655, Mol. Cell. Biochem., 2010, vol. 342, nos. 1–2, pp. 207–213.

    Article  CAS  PubMed  Google Scholar 

  3. Abisado, R., Benomar, S., Klaus, J., Dandekar, A., and Chandle, J., Bacterial quorum sensing and microbial community interactions, mBio, 2018, vol. 9, no. 3, pp. 1–13.

    Google Scholar 

  4. Brinza, L., Vu, H.P., Shaw, S., Mosselmans, J.F.W., and Benning, L.G., Effect of Mo and V on the hydrothermal crystallization of hematite from ferrihydrite: an in situ energy dispersive X-ray diffraction and X-ray absorption spectroscopy study, Cryst. Growth Des., 2015, vol. 15, pp. 4768–4780.

    Article  CAS  Google Scholar 

  5. Beneduzi, A., Ambrosini, A., and Passaglia, L.M., Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents, Genet. Mol. Biol., 2012, vol. 35, pp. 1044–1051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Branda, S.S., Chu, F., Kearns, D.B., Losick, R., and Kolter, R., A major protein component of the Bacillus subtilis biofilm matrix, Mol. Microbiol., 2006, vol. 59, pp. 1229–1238.

    Article  PubMed  Google Scholar 

  7. Chareyre, S. and Mandin, P., Bacterial iron homeostasis regulation by sRNAs, Microbiol. Spectrum, 2018, vol. 6, no. 2, pp. RWR-0010.

    Article  Google Scholar 

  8. Cornelis, P., Wei, Q., Andrews, S.C., and Vinck, T., Iron homeostasis and management of oxidative stress response in bacteria, Metallomics, 2011, vol. 1, pp. 1–10.

    Google Scholar 

  9. Chai, Y., Kolter, R., and Losick, R., Paralogous antirepressors acting on the master regulator for biofilm formation in Bacillus subtilis, Mol. Microbiol., 2009, vol. 74, no. 4, pp. 876–887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chapman, C.M.C., Gibson, G.R., and Rowland, I., In vitro evaluation of single- and multi-strain probiotics: interspecies inhibition between probiotic strains, and inhibition of pathogens, Anaerobe, 2002, vol. 18, pp. 405–413.

    Article  Google Scholar 

  11. Doornbos, R.F., van Loon, L.C., and Bakker,M., Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere, a review, Agron. Sustain. Dev., 2012, vol. 32, pp. 227–243.

    Article  Google Scholar 

  12. De Das, J., Mishra, D., Ray, P., Tripathy, P., Beuria, T., Singh, N., and Suar, M., In vitro evaluation of anti-infective activity of a Lactobacillus plantarum strain against Salmonella enterica serovar enteritidis, Gut Pathog., 2013, vol. 5, p. 1–11.

    Google Scholar 

  13. Devi, S., Kiehler B., Haggett L., and Fujita M., Evidence that autophosphorylation of the major sporulation kinase in Bacillus subtilis is able to occur in trans, J. Bacteriol., 2015, vol. 197, no. 16, pp. 2675–2684.

    Article  CAS  PubMed  Google Scholar 

  14. Ganchev, I., Biofilm formation between Bacillus subtilis and Escherichia coli K-12 strains at acidic and oxidative stress, Sci. J. Chem., 2019, vol. 7, no. 1, pp. 15–18.

    Article  CAS  Google Scholar 

  15. Grandchamp, G., Caro, L., and Shank, E., Pirated siderophores promote sporulation in Bacillus subtilis, Appl. Environ. Microbiol., 2017, vol. 83, p. e03293-16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Guelke, M., Blanckenburg, F., Schoenberg, R., Staubwasser, M., and Stuetzel., H., Determining the stable Fe isotope signature of plant-available iron in soils, Chem. Geol., 2010, vol. 277, pp. 269–280.

    Article  CAS  Google Scholar 

  17. Gambino, M., Marzano, V., Villa, F., Vitali, A., Vannini, C., Landini, P., and Cappitelli, F., Effects of sub-lethal doses of silver nanoparticles on Bacillus subtilis planktonic and sessile cells, J. Appl. Microbiol., 2015, vol. 118, pp. 1103–1115.

    Article  CAS  PubMed  Google Scholar 

  18. Heydorn, A., Nielsen, A., Hentzer, M., Sternberg, C., Givskov, M., Ersbøll, B., and Molin, S., Quantification of biofilm structures by thenovel computer program COMSTAT, Microbiology (SGM), 2000, vol. 146, pp. 2395–2407.

    Article  CAS  PubMed  Google Scholar 

  19. Kobayashi, K., SlrR/SlrA controls the initiation of biofilm formation in Bacillus subtilis, Mol. Microbiol., 2012, vol. 69, pp. 1399–1410.

    Article  Google Scholar 

  20. Lopez D., Vlamakis, H., and Kolter, R., Generation of multiple cell types in Bacillus subtilis, FEMS Microbiol. Rev., 2009, vol. 33, pp. 152–163.

    Article  CAS  PubMed  Google Scholar 

  21. Lopez, D, Vlamakis, H, and Kolter, R., Biofilms, Cold Spring Harb. Perspect. Biol., 2010, vol. 2, no. 7, pp. 1–5.

    Article  Google Scholar 

  22. Liu, S., Wu, N., Zhang, S., Yuan, Y., Zhang, W., and Zhang, Y., Variable persister gene interactions with (p)ppGpp for persister formation in Escherichia coli, Front. Microbiol., 2017, vol. 8, pp. 1795–1806.

    Article  PubMed  PubMed Central  Google Scholar 

  23. McLoon, A.L., Guttenplan, S.B., Kearns, D.B., Kolter, R., and Losick, R., Tracing the domestication of a biofilm-forming bacterium, J. Bacteriol., 2011, vol. 193, pp. 2027–2034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Massé, E. and Gottesman, S., A small RNA regulates the expression of genes involvedin iron metabolism in Escherichia coli, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, no. 7, pp. 4620–4625.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mika, F., Busse, S., Possling, A., Berkholz, J., Tschowri, N., Sommerfeldt, N., Pruteanu, M., and Hengge, R., Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli, Mol. Microbiol., 2014, vol. 84, no.1, pp. 51–65.

    Article  Google Scholar 

  26. Nandy S., Bapat, P., and Venkatesh, K., Sporulating bacteria prefers predation to cannibalism in mixed cultures, FEBS Lett., 2007, vol. 581, pp. 151–156.

    Article  CAS  PubMed  Google Scholar 

  27. Neilands, J.B., Siderophores: structure and function of microbial iron transport compounds, J. Biol. Chem., 1995, vol. 270, pp. 26 723–26 726.

    Article  Google Scholar 

  28. Oknin, H., Steinberg, D., and Shemesh, M., Magnesium ions mitigate biofilm formation of Bacillus species viadownregulation of matrix genes expression, Front. Microbiol., 2015, vol. 6, pp. 1–7.

    Article  Google Scholar 

  29. Ogasawara, H., Yamada, K., Kori, A., Yamamoto, K., and Ishihama, A., Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors, Microbiology (SGM), 2011,vol. 156, pp. 2470–2483.

    Article  Google Scholar 

  30. Oh, E., Andrews, K., and Jeon, B., Enhanced biofilm formation by ferrous and ferric iron through oxidative stress in Campylobacter jejuni, Front. Microbiol., 2018, vol. 9, pp. 1204. https://doi.org/10.3389/fmicb.2018.01204

    Article  PubMed  PubMed Central  Google Scholar 

  31. Pandey, M., Talwar, S., and Bose, S., Iron homeostasis in Mycobacterium tuberculosis is essential for persistence, Scientific Reports, 2018, vol. 8, p. 17359. https://doi.org/10.1038/s41598-018-35012-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Pelchovich, G., Omer-Bendori, S., and Gophna, U., Menaquinone and iron are essential for complex colony development in Bacillus subtilis, PLoS One, 2013, vol. 8, p. e79488.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rajkumar, M., Prasad, M., and Freitas, H., Potential of siderophore-producing bacteria for improving heavy metal phytoextraction, Trends Biotechnol., 2010, vol. 28, pp. 142–149.

    Article  PubMed  Google Scholar 

  34. Römheld, V. and Marschner, H., Evidence for a specific uptake system for iron phytosiderophores in roots of grasses, Plant Physiol., 1986, vol. 80, no. 1, pp. 175–180.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Romero, D., Vlamakis, H., Losick, R., and Kolter, R., An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms, Mol. Microbiol., 2011, vol. 80, pp. 1155–1168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Rendueles, O., Travier, L., Latour-Lambert, P., Fontaine, T., Magnus, J., Denamur, E., and Ghigo, J., Screening of Escherichia coli species biodiversity reveals new biofilm-associated antiadhesion polysaccharides, Mbio, 2011, vol. 2, pp. 11–43.

    Article  Google Scholar 

  37. Stein, T., Bacillus subtilis antibiotics: structures, syntheses andspecific functions, Mol Microbiol., 2005, vol. 56, p. 845–857.

    Article  CAS  PubMed  Google Scholar 

  38. Shemesh, M. and Chai, Y., A combination of glycerol and manganese promotes biofilm formation in Bacillus subtilis via histidine kinase kind signaling, J. Bacteriol., 2013, vol.195, pp. 2747–2754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Stanley, N., and Lazazzera, B., Environmental signals and regulatory pathways that influence biofilm formation, Mol. Microbiol., 2004, vol. 52, no. 4, pp. 917–924.

    Article  CAS  PubMed  Google Scholar 

  40. Somerton, B., Flint, S., Palmer, J., Brooks, J., and Lindsay, D., Preconditioning with cations increases the attachment of Anoxybacillus flavithermus and Geobacillus species to stainless steel, Appl. Environ. Microbiol., 2013, vol. 79, pp. 4186–4190.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Soldano, A., Yao, H., Chandler, J. R., and Rivera M., Inhibiting iron mobilization from bacterioferritin in Pseudomonas aeruginosa impairs biofilm formation irrespective of environmental iron availability, ACS Infect. Dis., 2020, vol. 6, pp. 447−458.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Sugita, H., Mizuki, H., and Itoi, S., Diversity of siderophore-producing bacteria isolated from the intestinal tracts of fish along the Japanese coast, Aquac. Res., 2012, vol. 43, pp. 481–488.

    Article  Google Scholar 

  43. Sokolova, T.A., Tolpeshta, I.I., and Topunova, I.V., Biotite weathering in podzolic soil under conditions of a model field experiment, Euras. Soil Sci., 2010, vol. 43, pp. 1150–1158.

    Article  Google Scholar 

  44. Thomine, S. and Lanquar, V., Iron transport and signaling in plants, in Transporters and Pumps in Plant Signaling, Geisler, M. and Venema, K., Eds., Signaling and Communication in Plants, 2011, vol. 7, pp. 99–131.

    Google Scholar 

  45. Verhamme, D.T., Murray, E.J., and Stanley-Wall, N.R., DegU and Spo0A jointly control transcription of two loci required for complex colony development by Bacillus subtilis, J. Bacteriol., 2009, vol. 191, pp. 100–108.

    Article  CAS  PubMed  Google Scholar 

  46. Wei, I., and Chu, M., Mn2+ improves surfactin productionby Bacillus subtilis, Biotechnol. Lett., 2007, vol. 24, pp. 479–482.

    Article  Google Scholar 

  47. Wei, Y.H., Lai, C.C., and Chang, J.S., Using taguchi experimental design methods to optimize trace element composition for enhanced surfactin production by Bacillus subtilis ATC 21332, Process Biochem., 2004, vol.42, pp. 40–45.

    Article  Google Scholar 

  48. Yadav, S., Kaushik, R., Saxena, A.K., and Arora, D.K., Diversity and phylogeny of plant growth-promoting bacilli from moderately acidic soil, J. Basic Microbiol., 2011, vol. 51, pp. 98–106.

    Article  CAS  PubMed  Google Scholar 

  49. Zhu, B. and Stülke, J., From genes and proteins to functional network annotation of the model organism Bacillus subtilis, Nucleic Acids Res., 2018, vol. 46, pp. 743–748.

    Article  Google Scholar 

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Funding

This research was supported by the Bulgarian Ministry of Education and Science under the National Program “Young Scientists and Postdoctoral Students-2.”

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Correspondence to Ivo Ganchev.

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The author declares that he has no conflicts of interest. The author declares no conflicts of interest. This article does not contain any studies involving human participants or animals performed by any of the authors.

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Ganchev, I. Role of Iron Homeostasis in the Multispecies Biofilm Formation. Microbiology 92, 675–685 (2023). https://doi.org/10.1134/S002626172360163X

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  • DOI: https://doi.org/10.1134/S002626172360163X

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