ULTRASTRUCTURAL ORGANIZATION OF THE BACILLUS SUBTILIS BIOFILM MATRIX IN THE STATIONARY PHASE
Abstract
Background. The ecological and geographical conditions of microorganisms (MO) can influence the ultrastructural organisation of their biofilm matrix and the accumulation of various bioactive compounds in it. Knowledge of such organisation in Arctic paleobacteria is extremely important for studying the mechanisms of biosynthesis and dispersion of biofilms formed by them, based on complex genetic programmes.
Purpose. Demonstrate the possibilities and show the main technical achievements of electron microscopy in the field of studying the biofilm matrix of palaeobacterium Bacillus sp. strain B1M isolated from waterlogged dispersed rocks that have passed into the frozen state.
Materials and methods. The object of the study was an MO of the genus Bacillus sp. isolated from water-wet dispersed rocks that had been frozen and deposited in DDBJ/EMBL/GeneBank (No. AB178889, identification No. 20040510203204.24251). Studies of cell ultrastructures were performed by analysing their ultrathin sections. Visualisation of ultrathin cell slices was carried out on electron microscope JEM-1011 (‘JEOL’, Japan) at accelerating voltage 80 kV. The values of cortisol-like steroid, serotonin-like and dopamine-like peptides were determined using ELISA technology. Statistical analysis of data was performed by using ‘IBM SPSS Statistics 21’ and Microsoft Excel programmes.
Results. It was revealed that structural heterogeneity is characteristic for the biofilm matrix organisation of Bacillus paleobacteria. On cell slices there are contacting formations in the form of long tunnelling nanotubes with an internal channel. The MO surface is covered with numerous cytoplasmic microvilli. The cell wall was found to be relatively permeable. There are numerous round vesicles surrounded by membranes around the bacterial cells. MOs actively produce cortisol-like steroid, serotonin-like and dopamine-like peptides.
Conclusion. The use of transmission electron microscopy (TEM) allowed us to identify and analyse the ultrastructural organisation of the matrix of Bacillus sp. strain B1M biofilm isolated from waterlogged dispersed rocks that have been frozen.
EDN: FQUSQS
Downloads
References
Список литературы
Воробьева Л.И., Ходжаев Е.Ю., Новикова Т.М., Мулюкин А.Л., Чудинова Е.М., Козлова А.Н., Эль-Регистан Г.И. Стрессопротекторное и перекрестное действие внеклеточного реактивирующего фактора микроорганизмов доменов бактерий, архей и эукариот // Микробиология. 2013. Т. 82, № 5. С. 588–594.
Мельников В. П. К созданию цельного образа криосферы // Криосфера Земли. 2014. Т. 18, № 4. С. 3-12.
Мохов И. И., Елисеев А. В. Моделирование глобальных климатических изменений в XX—XXIII веках при сценариях антропогенных воздействий RCP // Докл. Акад. наук. 2012. Т. 443, № 6. С. 732-736.
Николаев Ю.А., Плакунов В.К. Биопленка – “город микробов” или аналог многоклеточного организма? // Микробиология. 2007. Т. 76. № 2. С. 148-163.
Олескин А.В., Эль-Регистан Г.И., Шендеров Б.А. Межмикробные химические взаимодействия и диалог микробиота-хозяин: роль нейромедиаторов // Микробиология. 2016. Т. 85, № 1. С. 3-25.
Складнев Д.А., Мулюкин А.Л., Филиппова С.Н. и др. Моделирование процесса распространения клеток микроорганизмов и фаговых частиц из мест вытаивания мерзлотных слоев // Микробиология. 2016. Т. 85, № 5. С. 580-587. https://doi.org/10.7868/S0026365616050165
Barry R., Gitai Z. Self-assembling enzymes and the origins of the cytoskeleton // Current Opinion in Microbiology. 2011. Vol. 14 (6). P. 704-711. https://doi.org/10.1016/j.mib.2011.09.015
Blaud T.Z. Lerch G.K. Phoenix A.M., Osborn A.M. Arctic soil microbial diversity in a changing world // Research in Microbiology. 2015. Vol. 166. P. 796-813. https://doi.org/10.1016/j.resmic.2015.07.013
Brouchkov A., Melnikov V., Kalenova L., Fursova O., Pogorelko G., Potapov V. et al. Permafrost bacteria in biotechnology: Biomedical applications / Margesin R. (eds) // Psychrophiles: From Biodiversity to Biotechnology. Springer, Cham. 2017. 685 p. https://doi.org/10.1007/978-3-319-57057-0_23
Chu H., Fierer N., Lauber C.L., Caporaso J.G., Knight R., Grogan P. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes // Environ Microbiol. 2010. Vol. 12. P. 2998-3006. https://doi.org/10.1111/j.1462-2920.2010.02277.x
Dalton A. J. A study of the Golgi material of hepatic and intestinal epithelial cells with the electron microscope // Cell and Tissue Research. 1952. Vol. 36. P. 522–540. https://doi.org/10.1007/BF00347683
Eswaramoorthy P. et al. Cellular architecture mediates DivIVA ultrastructure and regulates Min activity in Bacillus subtilis // mBio. 2011. Vol. 2(6). https://doi.org/10.1128/mBio.00257-11
Fierer N., Jackson R.B. The diversity and biogeography of soil bacterial communities // Proc Natl Acad Sci USA. 2006. Vol. 103. P. 626-631. https://doi.org/10.1073/pnas.0507535103
Gilichinsky D.A., Vishnivetskaya T.A., Petrova M.A. et al. Bacteria in permafrost // Psychrophiles: from biodiversity to biotechnology / Eds. R. Margesin et al. Berlin: Rosa Springer, 2008. P. 83-102. https://doi.org/10.1007/978-3-540-74335-4_6
Hall-Stoodley L., Costerton J. W., Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases // Nat. Rev. Microbiol. 2004. Vol. 2. P. 95–108. https://doi.org/10.1038/nrmicro821
Kalenova L.F., Petrov S.A. and Sukhovei Y.G. Reparative and Immunomodulatory Potential of Low-Molecular-Weight Fractions of Secondary Metabolites of Bacillus sp. // Bulletin of experimental biology and medicine. 2022. Vol. 172 (3). P. 332-335. https://doi.org/10.1007/s10517-022-05387-5
Kalenova L.F., Petrov S.A. and Bazhin A.S. Dose-Dependent Effect of Bacillus sp. Metabolites from Permafrost on Lymphocyte Differentiation in the Thymus // Bulletin of experimental biology and medicine. 2016. Vol. 169 (1). P. 67-70. https://doi.org/10.1007/s10517-020-04826-5
Kolenbrander P.E., Andersen R.N., Blehert D.S., Egland P.G., Foster J.S., Parmer R.J. Jr. Communication among oral bacteria // Microbiol. Mol. Bio. Rev. 2002. Vol. 66. P. 486–505. https://doi.org/10.1128/mmbr.66.3.486-505.2002
Kreft J.U. Biofilms promotes altruism // Microbiology. 2004. Vol. 150. P. 2751-2760. https://doi.org/10.1099/mic.0.26829-0
Kuramitsu H.K., He X., Lux R., Anderson M.H., Shi W.Y. Interspecies interactions within oral microbial communities // Microbiol. Mol. Rev. 2007. Vol. 71. P. 653–670. https://doi.org/10.1128/mmbr.00024-07
Kreth J., Merritt J., Shi W.J., Qi F.X. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm // J. Bacteriol. 2005. Vol. 187. P. 7193–7203. https://doi.org/10.1128/JB.187.21.7193-7203.2005
Lenz P., Søgaard-Andersen L. Temporal and spatial oscillations in bacteria // Nature Reviews. Microbiology. 2011. Vol. 9 (8). P. 565-577. https://doi.org/10.1038/nrmicro2612
Malchevskiy V.A., Subbotin A.M., (...), Petrov S.A. Effect of Contamination with Perennial Permafrost Microorganisms on the Outcome of Closed Brain Neurotrauma // Bulletin of experimental biology and medicine. 2016. Vol. 161 (3). P. 388-390. https://doi.org/10.1007/s10517-016-3421-3
Mona Golmohammadzadeh, Danielle L. Sexton, Shweta Parmar, Elitza I. Tocheva Chapter One - Advanced imaging techniques: microscopy // Advances in Applied Microbiology. 2023. Vol. 122. P. 1-25. https://doi.org/10.1016/bs.aambs.2023.01.001
Neufeld J.D., Mohn W.W. Unexpectedly high bacterial diversity in Arctic tundra relative to boreal forest soils, revealed by serial analysis of ribosomal sequence tags // Appl Environ Microbiol. 2005. Vol. 71. P. 5710–5718. https://doi.org/10.1128/AEM.71.10.5710-5718.2005
Petrov S.A., Subbotin A.M., (...), Narushko M.V. Influence of the Microbiota of the Cryolithozone Paleoecosystems on the Behavioral Functions of the Nervous System of Chickens Gallus gallus // Bulletin of experimental biology and medicine. 2021. Vol. 171 (2). P. 234-237. https://doi.org/10.1007/s10517-021-05201-8
Pilhofer M., Jensen G.J. The bacterial cytoskeleton: More than twisted filaments // Current Opinion in Cell Biology. 2013. Vol. 25 (1). P. 125-133. https://doi.org/10.1016/j.ceb.2012.10.019
Reynolds E. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy // J. Cell Biol. 1963. Vol. 17. P. 208–212. https://doi.org/10.1083/jcb.17.1.208
Sekowska A., Masson J.B., Celani A., Vergassola M. Repulsion and metabolic switches in the collective behavior of bacterial colonies // Biophysical J. 2009. Vol. 97. P. 688–697. https://doi.org/10.1016/j.bpj.2009.04.018
Thanbichler M., Shapiro L. Getting organized-How bacterial cells move proteins and DNA // Nature Reviews Microbiology. 2008. Vol. 6 (1). P. 28-40, https://doi.org/10.1038/nrmicro1795
Webb J.S., Givskov M., Kjelleberg S. Bacterial biofilms: Prokaryotic adventures in multicellularity // Curr. Opin. Microbiol. 2003. Vol. 6. P. 578–585. https://doi.org/10.1016/j.mib.2003.10.014
References
Vorobyeva L.I., Hodjaev E.Y., Novikova T.M., Mullukin A.L., Chudinova E.M., Kozlova A.N., El-Registan G.I. Stress-protective and cross-talk effect of extracellular reactivating factor of microbial domains of bacteria, archaea and eukaryotes. Microbiology, 2013, vol. 82, no. 5, pp. 588-594.
Melnikov V. P. Toward the Creation of a Whole Image of the Cryosphere. Earth's Cryosphere, 2014, vol. 18, no. 4, pp. 3-12.
Mokhov I.I., Eliseev A.. V. Modeling of global climatic changes in the XX-XXIII centuries under scenarios of anthropogenic impacts RCP. Dokl. Acad. of Sciences, 2012, vol. 443, no. 6, pp. 732-736.
Nikolaev Yu.A., Plakunov V.K. Biofilm - a “city of microbes” or an analog of a multicellular organism? Microbiology, 2007, vol. 76, no. 2, pp. 148-163.
Oleskin A.V., El-Registan G.I., Shenderov B.A. Intermicrobial chemical interactions and microbiota-host dialog: the role of neurotransmitters. Microbiology, 2016, vol. 85, no. 1, pp. 3-25.
Skladnev D.A., Mullukin A.L., Filippova S.N. et al. Modeling of the process of microbial cells and phage particles spreading from permafrost layer thawing sites. Microbiology, 2016, vol. 85, no. 5, pp. 580-587. https://doi.org/10.7868/S0026365616050165
Barry R., Gitai Z. Self-assembling enzymes and the origins of the cytoskeleton. Current Opinion in Microbiology, 2011, vol. 14 (6), pp. 704-711. https://doi.org/10.1016/j.mib.2011.09.015
Blaud T.Z. Lerch G.K. Phoenix A.M., Osborn A.M. Arctic soil microbial diversity in a changing world. Research in Microbiology, 2015, vol. 166, pp. 796-813. https://doi.org/10.1016/j.resmic.2015.07.013
Brouchkov A., Melnikov V., Kalenova L., Fursova O., Pogorelko G., Potapov V. et al. Permafrost bacteria in biotechnology: Biomedical applications / Margesin R. (eds). Psychrophiles: From Biodiversity to Biotechnology. Springer, Cham. 2017, 685 p. https://doi.org/10.1007/978-3-319-57057-0_23
Chu H., Fierer N., Lauber C.L., Caporaso J.G., Knight R., Grogan P. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol, 2010, vol. 12, pp. 2998-3006. https://doi.org/10.1111/j.1462-2920.2010.02277.x
Dalton A. J. A study of the Golgi material of hepatic and intestinal epithelial cells with the electron microscope. Cell and Tissue Research., 1952, vol. 36, pp. 522–540. https://doi.org/10.1007/BF00347683
Eswaramoorthy P. et al. Cellular architecture mediates DivIVA ultrastructure and regulates Min activity in Bacillus subtilis. mBio, 2011, vol. 2(6). https://doi.org/10.1128/mBio.00257-11
Fierer N., Jackson R.B. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA, 2006, vol. 103, pp. 626-631. https://doi.org/10.1073/pnas.0507535103
Gilichinsky D.A., Vishnivetskaya T.A., Petrova M.A. et al. Bacteria in permafrost. Psychrophiles: from biodiversity to biotechnology / Eds. R. Margesin et al. Berlin: Rosa Springer, 2008, pp. 83-102. https://doi.org/10.1007/978-3-540-74335-4_6
Hall-Stoodley L., Costerton J. W., Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol., 2004, vol. 2, pp. 95–108. https://doi.org/10.1038/nrmicro821
Kalenova L.F., Petrov S.A. and Sukhovei Y.G. Reparative and Immunomodulatory Potential of Low-Molecular-Weight Fractions of Secondary Metabolites of Bacillus sp. Bulletin of experimental biology and medicine, 2022, vol. 172 (3), pp. 332-335. https://doi.org/10.1007/s10517-022-05387-5
Kalenova L.F., Petrov S.A. and Bazhin A.S. Dose-Dependent Effect of Bacillus sp. Metabolites from Permafrost on Lymphocyte Differentiation in the Thymus. Bulletin of experimental biology and medicine, 2016, vol. 169 (1), pp. 67-70. https://doi.org/10.1007/s10517-020-04826-5
Kolenbrander P.E., Andersen R.N., Blehert D.S., Egland P.G., Foster J.S., Parmer R.J. Jr. Communication among oral bacteria. Microbiol. Mol. Bio. Rev., 2002, vol. 66, pp. 486–505. https://doi.org/10.1128/mmbr.66.3.486-505.2002
Kreft J.U. Biofilms promotes altruism. Microbiology, 2004, vol. 150, pp. 2751-2760. https://doi.org/10.1099/mic.0.26829-0
Kuramitsu H.K., He X., Lux R., Anderson M.H., Shi W.Y. Interspecies interactions within oral microbial communities. Microbiol. Mol. Rev., 2007, vol. 71, pp. 653–670. https://doi.org/10.1128/mmbr.00024-07
Kreth J., Merritt J., Shi W.J., Qi F.X. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J. Bacteriol., 2005, vol. 187, pp. 7193–7203. https://doi.org/10.1128/JB.187.21.7193-7203.2005
Lenz P., Søgaard-Andersen L. Temporal and spatial oscillations in bacteria. Nature Reviews. Microbiology, 2011, vol. 9 (8), pp. 565-577. https://doi.org/10.1038/nrmicro2612
Malchevskiy V.A., Subbotin A.M., (...), Petrov S.A. Effect of Contamination with Perennial Permafrost Microorganisms on the Outcome of Closed Brain Neurotrauma. Bulletin of experimental biology and medicine, 2016, vol. 161 (3), pp. 388-390. https://doi.org/10.1007/s10517-016-3421-3
Mona Golmohammadzadeh, Danielle L. Sexton, Shweta Parmar, Elitza I. Tocheva Chapter One - Advanced imaging techniques: microscopy. Advances in Applied Microbiology, 2023, vol. 122, pp. 1-25. https://doi.org/10.1016/bs.aambs.2023.01.001
Neufeld J.D., Mohn W.W. Unexpectedly high bacterial diversity in Arctic tundra relative to boreal forest soils, revealed by serial analysis of ribosomal sequence tags. Appl Environ Microbiol., 2005, vol. 71, pp. 5710–5718. https://doi.org/10.1128/AEM.71.10.5710-5718.2005
Petrov S.A., Subbotin A.M., (...), Narushko M.V. Influence of the Microbiota of the Cryolithozone Paleoecosystems on the Behavioral Functions of the Nervous System of Chickens Gallus gallus. Bulletin of experimental biology and medicine, 2021, vol. 171 (2), pp. 234-237. https://doi.org/10.1007/s10517-021-05201-8
Pilhofer M., Jensen G.J. The bacterial cytoskeleton: More than twisted filaments. Current Opinion in Cell Biology, 2013, vol. 25 (1), pp. 125-133. https://doi.org/10.1016/j.ceb.2012.10.019
Reynolds E. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol., 1963, vol. 17, pp. 208–212. https://doi.org/10.1083/jcb.17.1.208
Sekowska A., Masson J.B., Celani A., Vergassola M. Repulsion and metabolic switches in the collective behavior of bacterial colonies. Biophysical J., 2009, vol. 97, pp. 688–697. https://doi.org/10.1016/j.bpj.2009.04.018
Thanbichler M., Shapiro L. Getting organized-How bacterial cells move proteins and DNA. Nature Reviews Microbiology, 2008, vol. 6 (1), pp. 28-40, https://doi.org/10.1038/nrmicro1795
Webb J.S., Givskov M., Kjelleberg S. Bacterial biofilms: Prokaryotic adventures in multicellularity. Curr. Opin. Microbiol., 2003, vol. 6, pp. 578–585. https://doi.org/10.1016/j.mib.2003.10.014
Copyright (c) 2024 Sergei A. Petrov, Vladimir A. Malchevski, Andrei M. Subbotin, Alexandr S. Bazhin, Maxim V. Naruchko
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
