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In vitro Evaluation of Biofilm Biomass Dynamics

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Abstract

Biofilms are dynamic structures constituted by microorganisms that grow and die, and understanding these processes may be crucial to control biofilm development in various environments. Assuming a generally accepted first order decay kinetics of biofilm mass in time, mean residence time can be calculated. Using the initial labeling of the biofilm by 13C stable isotope, we were able to determine the residence time of the carbon in physiologically active biofilms. Our data indicate that the residence time is strongly affected by nutrition and differs substantially between biofilms formed by different bacterial isolates. Moreover, the biofilm formed from mixed soil inocula showed almost the same carbon residence time as the biofilms formed from both soil inocula applied separately. This does not indicate the existence of dramatic incompatibility between members of two interacting microbial communities. In the situation when the established biofilm biomass undergoes continuous replacement by newly appearing cells, the complex biofilm admit reluctantly the newly arriving microorganisms as components of the existing community. Our study represents a new insight into the biofilm dynamics in vitro.

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REFERENCES

  1. Allocati, N., Masulli, M., Di Ilio, C., and De Laurenzi, V., Die for the community: an overview of programmed cell death in bacteria, Cell Death Dis., 2015, vol. 6, art. e1609.

  2. Bayles, K.W., The biological role of death and lysis in biofilm development, Nat. Rev. Microbiol., 2007, vol. 5, pp. 721–726.

    Article  CAS  Google Scholar 

  3. Brislawn, C.J., Graham, E.B., Dana, K., Ihardt, P., Fansler, S.J., Chrisler, W.B., Cliff, J.B., Stegen, J.C., Moran, J.J., and Bernstein, H.C., Forfeiting the priority effect: turnover defines biofilm community succession, ISME J, 2019, vol. 13, pp. 1865–1877.

    Article  Google Scholar 

  4. Burmølle, M., Hansen, L.H., and Sørensen, S.J., Establishment and early succession of a multispecies biofilm composed of soil bacteria, Microb. Ecol., 2007, vol. 54, pp. 352–362.

    Article  Google Scholar 

  5. Bystrianský, L., Hujslová, M., Hršelová, H., Řezáčová, V., Němcová, L., Šimsová, J., Gryndlerová, H., Kofroňová, O., Benada, O., and Gryndler, M., Observations on two microbial life strategies in soil: planktonic and biofilm-forming microorganisms are separable, Soil Biol. Biochem., 2019, vol. 136, art. 107535.

    Article  Google Scholar 

  6. Chao, A., Nonparametric estimation of the number of classes in a population, Scand. J. Stat., 1984, vol. 11, pp. 265–270.

    Google Scholar 

  7. Corsino, S.F., Campo, R., DiBella, G., Torregrossa, M., and Viviani, G., Study of aerobic granular sludge stability in a continuous-flow membrane bioreactor, Biores. Technol., 2016, vol. 200, pp. 1055–1059.

    Article  CAS  Google Scholar 

  8. Coyte, K.Z., Tabuteau, H., Gaffney, E.A., Foster, K.R., and Durham, W.M., Microbial competition in porous environments can select against rapid biofilm growth, Proc. Natnl. Acad. Sci. U. S. A., 2017, vol. 114, pp. E161−E170.

    Article  CAS  Google Scholar 

  9. Crotty, F.V., Blackshaw, R.P., and Murray, P.L., Differential growth of the fungus Absidia cylindrospora on 13C/15N-labeled media, R. C. Mass Spectrometry, 2011, vol. 25, pp. 1479–1484.

    CAS  Google Scholar 

  10. Deng, Y.-J. and Wang, S.Y., Synergistic growth in bacteria depends on substrate complexity, J. Microbiol., 2016, vol. 54, pp. 23–30.

    Article  Google Scholar 

  11. Gunina, A., Dippold, M., Glaser, B., and Kuzyakov, Y., Turnover of microbial groups and cell components in soil: 13C analysis of cellular biomarkers, Biogeosci., 2017, vol. 14, pp. 271–283.

    Article  CAS  Google Scholar 

  12. Hall-Stoodley, L., Costerton, J.W., and Stoodley, P., Bacterial biofilms: from the natural environment to infectious diseases, Nat. Rev. Microbiol., 2004, vol. 2, pp. 95–108.

    Article  CAS  Google Scholar 

  13. Mackay, D. and Webster, E., Environmental persistence of chemicals, Env. Sci. Pollut. Res., 2006, vol. 13, pp. 43–49.

    Article  CAS  Google Scholar 

  14. Mai, T.L. and Conner, D.E., Effect of temperature and growth media on the attachment of Listeria monocytogenes to stainless steel, Int. J. Food Microbiol., 2007, vol. 120, pp. 282–286.

    Article  CAS  Google Scholar 

  15. Marquardt, D., An algorithm for least-squares estimation of nonlinear parameters, SIAM J. Appl. Math., 1963, vol. 11, pp. 431–441.

    Article  Google Scholar 

  16. Martin, M., Hölscher, T., Dragoš, A., Cooper, V.S., and Kovács, A.T., Laboratory evolution of microbial interactions in bacterial biofilms, J. Bacteriol., 2016, vol. 198, pp. 2564−2571.

    Article  CAS  Google Scholar 

  17. Nikolayev, Y.A. and Plakunov, V.K., Biofilm—“city of microbes” or an analogue of multicellular organisms?, Microbiology (Moscow), 2007, vol. 76, pp. 125–138.

    Article  Google Scholar 

  18. Olsen, N.M.C., Røder, H.L., Russel, J., Madsen, J.S., Sørensen, S.J., and Burmølle, M., Priority of early colonizers but no effect on cohabitants in a synergistic biofilm community, Front. Microbiol., 2019, vol. 10, art. 1949.

    Article  Google Scholar 

  19. Plakunov, V.K., Mart’yanov, S.V., Teteneva, N.A., and Zhurina, M. V., A universal method for quantitative characterization of growth and metabolic activity of microbial biofilms in static models, Microbiology (Moscow), 2016, vol. 85, pp. 509–513.

    Article  CAS  Google Scholar 

  20. Press, W.H., Teukolsky, S.A., Vetterling, W.T., and Flannery, B.P., Numerical Recipes in C, Cambridge: Cambridge Univ. Press, 1992. 2nd ed.

    Google Scholar 

  21. Rahman, A., Mosquera, M., Thomas, W., Jimenez, J.A., Bott, C., Wett, B., Al-Omari, A., Murthy, S., Riffat, R., and De Clippeleir, H., Impact of aerobic famine and feast condition on extracellular polymeric substance production in high-rate contact stabilization systems, Chem. Eng. J., 2017, vol. 328, pp. 74–86.

    Article  CAS  Google Scholar 

  22. Ren, D., Madsen, J.S., Sørensen, S.J., and Burmølle, M., High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation, ISME J., 2015, vol. 9, pp. 81–89.

    Article  CAS  Google Scholar 

  23. Rollemberg, S.L.D., de Barros, A.N., Lira, V.N.S.A., Firmino, P.I.M., and dos Santos, A.B., Comparison of the dynamics, biokinetics and microbial diversity between activated sludge flocs and aerobic granular sludge, Biores. Technol., 2019, vol. 294, art. 122106.

    Article  CAS  Google Scholar 

  24. Røder, H.L., Sørensen, S.J., and Burmølle, M., Studying bacterial multispecies biofilms: where to start?, Trends Microbiol., 2016, vol. 24, art. 6.

    Article  Google Scholar 

  25. Seneviratne, G., Zavahir, J.S., Bandara, W.M.M.S., and Weerasekara, M.L.M.A.W., Fungal–bacterial biofilms: their development for novel biotechnological applications. World J. Microbiol. Biotechnol., 2008, vol. 24, pp. 739–743.

    Article  CAS  Google Scholar 

  26. She, P., Wang, Y., Liu, Y., Tan, F., Chen, L., Luo, Z., and Wu, Y., Effects of exogenous glucose on Pseudomonas aeruginosa biofilm formation and antibiotic resistance, Microbiol. Open, 2019, vol. 2019, art. 8e933.

  27. Stone, W., Kroukamp, O., Korber, D.R., McKelvie, J., and Wolfaardt, G.M., Microbes at surface-air interfaces: the metabolic harnessing of relative humidity, surface hygroscopicity, and oligotrophy for resilience, Front. Microbiol., 2016, vol 7, art. 1563.

    Article  Google Scholar 

  28. Valentine, D.L., Chidthaisong, A., Rice, A., Reeburgh, W.S., and Tyler, S.C., Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens, Geochim. Cosmochim. Acta, 2004, vol. 68, pp. 1571–1590.

    Article  CAS  Google Scholar 

  29. Vick, S.H.W., Greenfield, P., Pinetown, K.L., Sherwood, N., Gong, S., Tetu, S.G., Midgley, D.J., and Paulsen, I.T., Succession patterns and physical niche partitioning in microbial communities from subsurface coal seams, iScience, 2019, vol. 12, pp. 152–167.

  30. Visvalingam, J., Wang, H., Ells, T.C., and Yang, X.Q., Facultative anaerobes shape multispecies biofilms composed of meat processing surface bacteria and Escherichia coli O157:H7 or Salmonella enterica serovar typhimurium, Appl. Environ. Microbiol., 2019, vol. 85, art. e01123-19.

    Article  CAS  Google Scholar 

  31. Webb, J.S., Givskov, M., and Kjelleberg, S., Bacterial biofilms: prokaryotic adventures in multicellularity, Curr. Opinion Microbiol., 2003a, vol. 6, pp. 578–585.

    Article  CAS  Google Scholar 

  32. Webb, J.S., Thompson, L.S., James, S., Charlton, T., Tolker-Nielsen, T., Koch, B., Givskov, M., and Kjelleberg, S., Cell death in Pseudomonas aeruginosa biofilm development, J. Bacteriol., 2003b, vol. 185, pp. 4585–4592.

    Article  CAS  Google Scholar 

  33. Zhao, R., Song, Y., Dai, Q., Kang, Y., Pan, J., Zhu, L., Zhang, L., Wang, Y., and Shen, X., A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis, Sci. Rep., 2017, vol. 7, art. 639.

    Article  Google Scholar 

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FUNDING

The work was supported by the Czech Science Foundation, grant number 17-09946S.

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Authors and Affiliations

  1. Faculty of Science, Jan Evangelista Purkyně University in Ústí nad Labem, 40096, Ústí nad Labem, Czech Republic

    M. Gryndler, L. Bystrianský & H. Malinská

  2. Institute of Microbiology, v.v.i., Academy of Sciences of the Czech Republic, 14220, Prague 4, Czech Republic

    H. Gryndlerová, M. Hujslová & H. Hršelová

  3. Institute of Physics, v.v.i., Czech Academy of Sciences, 18221, Prague 8, Czech Republic

    D. Šimsa

  4. Applied Physics, Department of Engineering Sciences and Mathematics, Luleå University of Technology, 97187, Luleå, Sweden

    D. Šimsa

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  1. M. Gryndler
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  2. H. Gryndlerová
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  3. M. Hujslová
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  4. L. Bystrianský
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  5. H. Malinská
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Correspondence to M. Gryndler.

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The authors declare that they have no conflict of interests. They further declare that this work does not violate any aspect of the human rights or dignity. Animals were not used in the experiments.

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Gryndler, M., Gryndlerová, H., Hujslová, M. et al. In vitro Evaluation of Biofilm Biomass Dynamics. Microbiology 90, 656–665 (2021). https://doi.org/10.1134/S0026261721050064

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