Peculiarities of the Ontogenesis of Bacilli During Development from a Vegetative Cell to a Spore

Authors

  • V.G. Voitsekhovsky Bogomolets National Medical University, 13 Т. Shevchenko boul., Kyiv, 01601, Ukraine
  • L.V. Avdeeva Zabolotny Institute of Microbiology and Virology, NAS of Ukraine, 154 Akademika Zabolotnoho Str., Kyiv, 03143, Ukraine
  • O.B. Balko Zabolotny Institute of Microbiology and Virology, NAS of Ukraine, 154 Akademika Zabolotnoho Str., Kyiv, 03143, Ukraine https://orcid.org/0000-0003-2635-3464
  • O.I. Balko Zabolotny Institute of Microbiology and Virology, NAS of Ukraine, 154 Akademika Zabolotnoho Str., Kyiv, 03143, Ukraine

DOI:

https://doi.org/10.15407/microbiolj86.04.091

Keywords:

spore formation, factors of environment, growth, macrocycle and microcycle of bacterial development, sporogenesis regulation

Abstract

Understanding the development processes of bacteria, in particular spore-forming ones, has both fundamental and applied importance, since at various stages of this process, the cells of microorganisms perform certain functions that can be regulated by influencing certain factors depending on the tasks. Literature data and the results of our research on the influence of the composition of the nutrient medium, pH, temperature, and aeration on sporulation are analyzed in the article. It isshown that the direction of bacterial cells’ development in certain ways is determined by signals that come from the surrounding environment, affect their genome, and determine the ways of cell development – growth or sporulation. Sporogenesis can also be induced by metabolites formed during microorganism development. It is emphasized that the environmental factors that influence the sporulation of bacteria have been studied in sufficient detail. However, the mechanisms of their action remain debatable. Morphological, genetic, and biochemical changes of spore-forming bacteria under the conditions of macrocyclic and microcyclic ways of their development are also highlighted, which makes it possible to correctly understand the functioning of regulatory mechanisms in the ontogenesis of microbial cells. In particular, the data of our research on the dynamics of morphological changes in the ontogenesis of a specific individual bacterial cell are presented. In addition, factors, including specific terminal products of cell metabolism, such as antibiotics, and genetic mechanisms of sporogenesis regulation of various genera and species of bacteria are described in detail. The nature of the vast majority of "sporogenes" has not been clarified, and there are only a few hypotheses regarding the mechanism of their action. However, most of the biological regulators of sporogenesis were found in the culture liquid, which indicates the cellular nature of their action. Therefore, to obtain more convincing data on the regulation of sporogenesis, studies at the cellular level are needed.

Downloads

Download data is not yet available.

References

Anumudu, C., Hart, A., Miri, T., & Onyeaka, H. (2021). Recent Advances in the Application of the Antimicrobial Peptide Nisin in the Inactivation of Spore-Forming Bacteria in Foods. Molecules (Basel, Switzerland), 26(18), 5552. https://doi.org/10.3390/molecules26185552

Arigoni, F., Guérout-Fleury, A. M., Barák, I., & Stragier, P. (1999). The SpoIIE phosphatase, the sporulation septum and the establishment of forespore-specific transcription in Bacillus subtilis: a reassessment. Molecular microbiology, 31(5), 1407–1415. https://doi.org/10.1046/j.1365-2958.1999.01282.x

Augustyn, W., Chruściel, A., Hreczuch, W., Kalka, J., Tarka, P., & Kierat, W. (2022). Inactivation of Spores and Vegetative Forms of Clostridioides difficile by Chemical Biocides: Mechanisms of Biocidal Activity, Methods of Evaluation, and Environmental Aspects. International journal of environmental research and public health, 19(2), 750. https://doi.org/10.3390/ijerph19020750

Balko, O. I., Balko, O. B. & Avdeeva, L. V. (2020). Bacteriocins of Some Groups of Gram-Negative Bacteria. Mikrobiolohichnyi Zhurnal, 82(3), 71–84. https://doi.org/10.15407/microbiolj82.03.071

Balko, O. I., Avdeeva, L. V., Balko, O. B. (2018). Depositary Function of Pseudomonas aeruginosa Biofilm on Media with Different Carbon Source Concentration. Mikrobiolohichnyi Zhurnal, 80(6), 15–27. https://doi.org/10.15407/microbiolj80.06.015

Balko, A. B., Vidasov, V. V., & Avdeeva, L. V. (2013). Optimization of conditions of Pseudomonas aeruginosa bacteriocin induction. Mikrobiolohichnyi zhurnal (Kiev, Ukraine: 1993), 75(1), 79–85.

Balko, A. B. (2012). Characteristic, properties, prospect of application of bacteriocins. Mikrobiolohichnyi zhurnal, 74(6), 99–106.

Barák, I., Muchová, K., & Labajová, N. (2019). Asymmetric cell division during Bacillus subtilis sporulation. Future microbiology, 14, 353–363. https://doi.org/10.2217/fmb-2018-0338

Barák, I., Prepiak, P., & Schmeisser, F. (1998). MinCD proteins control the septation process during sporulation of Bacillus subtilis. Journal of bacteriology, 180(20), 5327–5333. https://doi.org/10.1128/JB.180.20.5327-5333.1998

Berendsen, E. M., Boekhorst, J., Kuipers, O. P., & Wells-Bennik, M. H. (2016a). A mobile genetic element profoundly increases heat resistance of bacterial spores. The ISME journal, 10(11), 2633–2642. https://doi.org/10.1038/ismej.2016.59

Berendsen, E. M., Koning, R. A., Boekhorst, J., de Jong, A., Kuipers, O. P., & Wells-Bennik, M. H. (2016b). High-Level Heat Resistance of Spores of Bacillus amyloliquefaciens and Bacillus licheniformis Results from the Presence of a spoVA Operon in a Tn1546 Transposon. Frontiers in microbiology, 7, 1912. https://doi.org/10.3389/fmicb.2016.01912

Berthold-Pluta, A., Pluta, A., & Garbowska, M. (2015). The effect of selected factors on the survival of Bacillus cereus in the human gastrointestinal tract. Microbial pathogenesis, 82, 7–14. https://doi.org/10.1016/j.micpath.2015.03.015

Biliavska, L. A., Efimenko, T. A., Efremenkova, O. V., Koziritska, V. Y., & Iutynska, G. A. (2016). Identification and Antagonistic Properties of the Soil Streptomycete Streptomyces sp. 100. Mikrobiolohichnyi zhurnal (Kiev, Ukraine: 1993), 78(2), 61–73. https://doi.org/10.15407/microbiolj78.02.061

Biró, S., Birkó, Z., & van Wezel, G. P. (2000). Transcriptional and functional analysis of the gene for factor C, an extracellular signal protein involved in cytodifferentiation of Streptomyces griseus. Antonie van Leeuwenhoek, 78(3–4), 277–285. https://doi.org/10.1023/A:1010221407340

Black, M. E., & Shaevitz, J. W. (2023). Rheological Dynamics of Active Myxococcus xanthus Populations during Development. Physical review letters, 130(21), 218402. https://doi.org/10.1103/PhysRevLett.130.218402

Boix, E., Couvert, O., André, S., & Coroller, L. (2021). The synergic interaction between environmental factors (pH and NaCl) and the physiological state (vegetative cells and spores) provides new possibilities for optimizing processes to manage risk of C. sporogenes spoilage. Food microbiology, 100, 103832. https://doi.org/10.1016/j.fm.2021.103832

Bremer, E., Calteau, A., Danchin, A., Harwood, C., Helmann, J. D., Médigue, C., Palsson, B. O., Sekowska, A., Vallenet, D., Zuniga, A., & Zuniga, C. (2023). A model industrial workhorse: Bacillus subtilis strain 168 and its genome after a quarter of a century. Microbial biotechnology, 16(6), 1203–1231. https://doi.org/10.1111/1751-7915.14257

Brown, E. E., Miller, A. K., Krieger, I. V., Otto, R. M., Sacchettini, J. C., & Herman, J. K. (2019). A DNA-Binding Protein Tunes Septum Placement during Bacillus subtilis Sporulation. Journal of bacteriology, 201(16), e00287-19. https://doi.org/10.1128/JB.00287-19

Bursík, M., & Nĕmec, M. (1999). Alkaline phosphatase production during sporulation of Bacillus cereus. Folia microbiologica, 44(1), 90–92. https://doi.org/10.1007/BF02816228

Butala, M., & Dragoš, A. (2023). Unique relationships between phages and endospore-forming hosts. Trends in microbiology, 31(5), 498–510. https://doi.org/10.1016/j.tim.2022.11.009

Catinean, A., Neag, A. M., Nita, A., Buzea, M., & Buzoianu, A. D. (2019). Bacillus spp. Spores-A Promising Treatment Option for Patients with Irritable Bowel Syndrome. Nutrients, 11(9), 1968. https://doi.org/10.3390/nu11091968

Cattoni, D. I., Thakur, S., Godefroy, C., Le Gall, A., Lai-Kee-Him, J., Milhiet, P. E., Bron, P., & Nöllmann, M. (2014). Structure and DNA-binding properties of the Bacillus subtilis SpoIIIE DNA translocase revealed by single-molecule and electron microscopies. Nucleic acids research, 42(4), 2624–2636. https://doi.org/10.1093/nar/gkt1231

Cervin, M. A., Spiegelman, G. B., Raether, B., Ohlsen, K., Perego, M., & Hoch, J. A. (1998). A negative regulator linking chromosome segregation to developmental transcription in Bacillus subtilis. Molecular microbiology, 29(1), 85–95. https://doi.org/10.1046/j.1365-2958.1998.00905.x

Chan, H., Taib, N., Gilmore, M. C., Mohamed, A. M. T., Hanna, K., Luhur, J., Nguyen, H., Hafiz, E., Cava, F., Gribaldo, S., Rudner, D., & Rodrigues, C. D. A. (2022). Genetic Screens Identify Additional Genes Implicated in Envelope Remodeling during the Engulfment Stage of Bacillus subtilis Sporulation. mBio, 13(5), e0173222. https://doi.org/10.1128/mbio.01732-22

Charlton, S., Moir, A. J., Baillie, L., & Moir, A. (1999). Characterization of the exosporium of Bacillus cereus. Journal of applied microbiology, 87(2), 241–245. https://doi.org/10.1046/j.1365-2672.1999.00878.x

Chary, V. K., & Piggot, P. J. (2003). Postdivisional synthesis of the Sporosarcina ureae DNA translocase SpoIIIE either in the mother cell or in the prespore enables Bacillus subtilis to translocate DNA from the mother cell to the prespore. Journal of bacteriology, 185(3), 879–886. https://doi.org/10.1128/JB.185.3.879-886.2003

Chiu, C. W., Tsai, P. J., Lee, C. C., Ko, W. C., & Hung, Y. P. (2021). Inhibition of spores to prevent the recurrence of Clostridioides difficile infection – A possibility or an improbability? Journal of microbiology, immunology, and infection = Wei mian yu gan ran za zhi, 54(6), 1011–1017. https://doi.org/10.1016/j.jmii.2021.06.002

Cho, W. I., & Chung, M. S. (2020). Bacillus spores: a review of their properties and inactivation processing technologies. Food science and biotechnology, 29(11), 1447–1461. https://doi.org/10.1007/s10068-020-00809-4

Chuiko, N. V., Chobotarov, A. Y., Kurdish, I. K. (2021). Growth and phytase activities of Bacillus subtilis IMV B-7023 during cultivation with sodium phytate. Mikrobiolohichnyi Zhurnal, 83(6), 13–19. https://doi.org/10.15407/microbiolj83.06.013

Clauwers, C., Lood, C., Van den Bergh, B., van Noort, V., & Michiels, C. W. (2017). Canonical germinant receptor is dispensable for spore germination in Clostridium botulinum group II strain NCTC 11219. Scientific reports, 7(1), 15426. https://doi.org/10.1038/s41598-017-15839-y

Corona Ramírez, A., Lee, K. S., Odriozola, A., Kaminek, M., Stocker, R., Zuber, B., & Junier, P. (2023). Multiple roads lead to Rome: unique morphology and chemistry of endospores, exospores, myxospores, cysts and akinetes in bacteria. Microbiology (Reading, England), 169(2), 001299. https://doi.org/10.1099/mic.0.001299

Davidson, P., Eutsey, R., Redler, B., Hiller, N. L., Laub, M. T., & Durand, D. (2018). Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes. PLoS genetics, 14(9), e1007470. https://doi.org/10.1371/journal.pgen.1007470

Dawes, I. W., Kay, D., & Mandelstam, J. (1971). Determining effect of growth medium on the shape and position of daughter chromosomes and on sporulation in Bacillus subtilis. Nature, 230(5296), 567–569. https://doi.org/10.1038/230567a0

Decker, S., & Maier, S. (1975). Fine structure of mesosomal involvement during Bacillus macerans sporulation. Journal of bacteriology, 121(1), 363–372. https://doi.org/10.1128/jb.121.1.363-372.1975

Dembek, M., Kelly, A., Barwinska-Sendra, A., Tarrant, E., Stanley, W. A., Vollmer, D., Biboy, J., Gray, J., Vollmer, W., & Salgado, P. S. (2018). Peptidoglycan degradation machinery in Clostridium difficile forespore engulfment. Molecular microbiology, 110(3), 390–410. https://doi.org/10.1111/mmi.14091

Dikec, J., Bechoua, N., Winckler, P., & Perrier-Cornet, J. M. (2022). Effects of pulsed near infrared light (NIR) on Bacillus subtilis spores. Journal of photochemistry and photobiology. B, Biology, 234, 112530. https://doi.org/10.1016/j.jphotobiol.2022.112530

Donnelly, M. L., Fimlaid, K. A., & Shen, A. (2016). Characterization of 4. Clostridium difficile Spores Lacking Either SpoVAC or Dipicolinic Acid Synthetase. Journal of bacteriology, 198(11), 1694–1707. https://doi.org/10.1128/JB.00986-15

Drews, G. (1999). Ferdinand Cohn, a Founder of Modern Microbiology. ASM News, 65(8), 547–553.

Driks, A., & Eichenberger, P. (2016). The Spore Coat. Microbiology spectrum, 4(2), 10.1128/microbiolspec.TBS-0023-2016. https://doi.org/10.1128/microbiolspec.TBS-0023-2016

Dunn, G., & Mandelstam, J. (1977). Cell polarity in Bacillus subtilis: effect of growth conditions on spore positions in sister cells. Journal of general microbiology, 103(1), 201–205. https://doi.org/10.1099/00221287-103-1-201

Dworkin, J., & Losick, R. (2001). Differential gene expression governed by chromosomal spatial asymmetry. Cell, 107(3), 339–346. https://doi.org/10.1016/S0092-8674(01)00528-1

Emami, K., Guyet, A., Kawai, Y., Devi, J., Wu, L. J., Allenby, N., Daniel, R. A., & Errington, J. (2017). RodA as the missing glycosyltransferase in Bacillus subtilis and antibiotic discovery for the peptidoglycan polymerase pathway. Nature microbiology, 2, 16253. https://doi.org/10.1038/nmicrobiol.2016.253

Errington, J., & Wu, L. J. (2017). Cell cycle machinery in Bacillus subtilis. In J. Löwe, & L. A. Amos (Eds.), Prokaryotic Cytoskeletons: Filamentous Protein Polymers Active in the Cytoplasm of Bacterial and Archaeal Cells (pp. 67–101). Springer Int.

Errington J. (2003). Regulation of endospore formation in Bacillus subtilis. Nature reviews. Microbiology, 1(2), 117–126. https://doi.org/10.1038/nrmicro750

Fimlaid, K. A., Jensen, O., Donnelly, M. L., Siegrist, M. S., & Shen, A. (2015). Regulation of Clostridium difficile Spore Formation by the SpoIIQ and SpoIIIA Proteins. PLoS genetics, 11(10), e1005562. https://doi.org/10.1371/journal.pgen.1005562

Fitz-Jams, P. C., & Young, J. E. (1969). Morphology sporulation. In G. W. Gould, A. Hurst (Eds.), The bacterial spore (pp. 39–72). Academic Press.

Freese, E. B., & Freese, E. (1977). The influence of the developing bacterial spore on the mother cell. Developmental biology, 60(2), 453–462. https://doi.org/10.1016/0012-1606(77)90142-7

Freese E. (1972). Sporulation of bacilli, a model of cellular differentiation. Current topics in developmental biology, 7, 85–124. https://doi.org/10.1016/S0070-2153(08)60070-8

Galperin, M. Y., Mekhedov, S. L., Puigbo, P., Smirnov, S., Wolf, Y. I., & Rigden, D. J. (2012). Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environmental microbiology, 14(11), 2870–2890. https://doi.org/10.1111/j.1462-2920.2012.02841.x

Galperin, M. Y., Yutin, N., Wolf, Y. I., Vera Alvarez, R., & Koonin, E. V. (2022). Conservation and Evolution of the Sporulation Gene Set in Diverse Members of the Firmicutes. Journal of bacteriology, 204(6), e0007922. https://doi.org/10.1128/jb.00079-22

Gao, X., Swarge, B. N., Dekker, H. L., Roseboom, W., Brul, S., & Kramer, G. (2021). The Membrane Proteome of Spores and Vegetative Cells of the Food-Borne Pathogen Bacillus cereus. International journal of molecular sciences, 22(22), 12475. https://doi.org/10.3390/ijms222212475

Gould G. W. (2006). History of science–spores. Journal of applied microbiology, 101(3), 507–513. https://doi.org/10.1111/j.1365-2672.2006.02888.x

Gould, G. W., & Hurst, A. (1969). The bacterial spore. Academic Press.

Gudzenko, O. V., Avdiyuk, K. V., Borzova, N. V., Ivanytsia, V. О., Varbanets, L. D. (2022). Keratinase, Caseinolitic, Cellulase and β-Mananase Activities of Bacteria Isolated from the Black Sea. Mikrobiolohichnyi zhurnal (Kiev, Ukraine: 1993), 84(4), 3–8. https://doi.org/10.15407/microbiolj84.04.003

Guliy, O. I., Bunin, V. D., Balko, A. B., Volkov, A. A., Staroverov, S., Karavaeva, O., & Ignatov, O. V. (2014). Effect of Sulfonamides on the Electrophysical Properties of Bacterial Cells. Anti-Infective Agents, 12(2). 191–197. https://doi.org/10.2174/2211352512666140630171501

Henriques, A. O., Melsen, L. R., & Moran, C. P., Jr (1998). Involvement of superoxide dismutase in spore coat assembly in Bacillus subtilis. Journal of bacteriology, 180(9), 2285–2291. https://doi.org/10.1128/JB.180.9.2285-2291.1998

Hoch J. A. (2017). A Life in Bacillus subtilis Signal Transduction. Annual review of microbiology, 71, 1–19. https://doi.org/10.1146/annurev-micro-030117-020355

Hurst, A. (1969). Biosyntesis of polypeptide antibiotics. In G. W. Gould, A. Hurst (Eds.), The bacterial spore (pp. 167–182). Academic Press.

Jaiaue, P., Srimongkol, P., Thitiprasert, S., Tanasupawat, S., Cheirsilp, B., Assabumrungrat, S., & Thongchul, N. (2021). A modified approach for high-quality RNA extraction of spore-forming Bacillus subtilis at varied physiological stages. Molecular biology reports, 48(10), 6757–6768. https://doi.org/10.1007/s11033-021-06673-7

Ju, J., Luo, T., & Haldenwang, W. G. (1997). Bacillus subtilis Pro-sigmaE fusion protein localizes to the forespore septum and fails to be processed when synthesized in the forespore. Journal of bacteriology, 179(15), 4888–4893. https://doi.org/10.1128/jb.179.15.4888-4893.1997

Kerravala, Z. J., Srinivasan, V. R., & Halvorson, H. O. (1964). Endogenous factor in sporogenesis in bacteria. II. Growth and sporulation in Bacillus subtilis. Journal of bacteriology, 88(2), 374–380. https://doi.org/10.1128/jb.88.2.374-380.1964

Khanna, K., Lopez-Garrido, J., Sugie, J., Pogliano, K., & Villa, E. (2021). Asymmetric localization of the cell division machinery during Bacillus subtilis sporulation. eLife, 10, e62204. https://doi.org/10.7554/eLife.62204

Khanna, K., Lopez-Garrido, J., & Pogliano, K. (2020). Shaping an Endospore: Architectural Transformations During Bacillus subtilis Sporulation. Annual review of microbiology, 74, 361–386. https://doi.org/10.1146/annurev-micro-022520-074650

Khanna, K., Lopez-Garrido, J., Zhao, Z., Watanabe, R., Yuan, Y., Sugie, J., Pogliano, K., & Villa, E. (2019). The molecular architecture of engulfment during Bacillus subtilis sporulation. eLife, 8, e45257. https://doi.org/10.7554/eLife.45257.045

Khokhlov, A. S., Anisova, L. N., Tovarova, I. I., Kleiner, E. M., Kovalenko, I. V., Krasilnikova, O. I., Kornitskaya, E. Y., & Pliner, S. A. (1973). Effect of A-factor on the growth of asporogenous mutants of Streptomyces griseus, not producing this factor. Zeitschrift fur allgemeine Mikrobiologie, 13(8), 647–655. https://doi.org/10.1002/jobm.19730130803

Khvorova, A., Zhang, L., Higgins, M. L., & Piggot, P. J. (1998). The spoIIE locus is involved in the Spo0A-dependent switch in the location of FtsZ rings in Bacillus subtilis. Journal of bacteriology, 180(5), 1256–1260. https://doi.org/10.1128/JB.180.5.1256-1260.1998

King, N., Dreesen, O., Stragier, P., Pogliano, K., & Losick, R. (1999). Septation, dephosphorylation, and the activation of sigmaF during sporulation in Bacillus subtilis. Genes & development, 13(9), 1156–1167. https://doi.org/10.1101/gad.13.9.1156

Koopman, N., Remijas, L., Seppen, J., Setlow, P., & Brul, S. (2022). Mechanisms and Applications of Bacterial Sporulation and Germination in the Intestine. International journal of molecular sciences, 23(6), 3405. https://doi.org/10.3390/ijms23063405

Krut', V. V., Dankevych, L. A., Votselko, S. K., & Patyka, V. P. (2014). Influence of different adhesive composition on sporulation and protein synthesis by Bacillus thuringiensis collection strains. Mikrobiolohichnyi zhurnal (Kiev, Ukraine: 1993), 76(5), 34–41.

Lazarenko, L.M., Babenko, L.P., Safronova, L.A., Demchenko, O.M., Bila, V.V., Zaitseva, G.M., & Spivak, M.Ya. (2023). Antimicrobial and Immunomodulatory Action of Probiotic Composition of Bacilli on Bacterial Vaginitis in Mice. Mikrobiolohichnyi Zhurnal, 85(3), 48–60. https://doi.org/10.15407/microbiolj85.03.048

Levin, P. A., Shim, J. J., & Grossman, A. D. (1998). Effect of minCD on FtsZ ring position and polar septation in Bacillus subtilis. Journal of bacteriology, 180(22), 6048–6051. https://doi.org/10.1128/JB.180.22.6048-6051.1998

Loboda, M., Voichuk, S. I. & Biliavska, L. A. (2019). Correlation Dependence of the Antibiotic Compounds Biosynthesis and other Biologically Active Substances in Soil Streptomycetes. Mikrobiolohichnyi Zhurnal, 81(5). 36–47. https://doi.org/10.15407/microbiolj81.05.036

Lopez, J. M., & Thoms, B. (1976). Beziehungenzwischen katabolischer Repression und Sporulation sci Bacillus subtilis. Arch Microbiol, 109(1–2), 181–186. https://doi.org/10.1007/BF00425133

Lopez-Garrido, J., Ojkic, N., Khanna, K., Wagner, F. R., Villa, E., Endres, R. G., & Pogliano, K. (2018). Chromosome Translocation Inflates Bacillus Forespores and Impacts Cellular Morphology. Cell, 172(4), 758–770. https://doi.org/10.1016/j.cell.2018.01.027

Loshon, C. A., Kraus, P., Setlow, B., & Setlow, P. (1997). Effects of inactivation or overexpression of the sspF gene on properties of Bacillus subtilis spores. Journal of bacteriology, 179(1), 272–275. https://doi.org/10.1128/jb.179.1.272-275.1997

Lu, S., Cutting, S., & Kroos, L. (1995). Sporulation protein SpoIVFB from Bacillus subtilis enhances processing of the sigma factor precursor Pro-sigma K in the absence of other sporulation gene products. Journal of bacteriology, 177(4), 1082–1085. https://doi.org/10.1128/jb.177.4.1082-1085.1995

Luo, Y., Korza, G., DeMarco, A. M., Kuipers, O. P., Li, Y. Q., & Setlow, P. (2021). Properties of spores of Bacillus subtilis with or without a transposon that decreases spore germination and increases spore wet heat resistance. Journal of applied microbiology, 131(6), 2918–2928. https://doi.org/10.1111/jam.15163

Mandelstam, J., & Higgs, S. A. (1974). Induction of sporulation during synchronized chromosome replication in Bacillus subtilis. Journal of bacteriology, 120(1), 38–42. https://doi.org/10.1128/jb.120.1.38-42.1974

Mandelstam, J., Sterlini, J. M., & Kay, D. (1971). Sporulation in Bacillus subtilis. Effect of medium on the form of chromosome replication and on initiation to sporulation in Bacillus subtilis. The Biochemical journal, 125(2), 635–641. https://doi.org/10.1042/bj1250635

Meeske, A. J., Rodrigues, C. D., Brady, J., Lim, H. C., Bernhardt, T. G., & Rudner, D. Z. (2016). High-Throughput Genetic Screens Identify a Large and Diverse Collection of New Sporulation Genes in Bacillus subtilis. PLoS biology, 14(1), e1002341. https://doi.org/10.1371/journal.pbio.1002341

Miyata, S., Moriyama, R., Sugimoto, K., & Makino, S. (1995). Purification and partial characterization of a spore cortex-lytic enzyme of Clostridium perfringens S40 spores. Bioscience, biotechnology, and biochemistry, 59(3), 514–515. https://doi.org/10.1271/bbb.59.514

Mocho, J. P., Coutot, R., Douglas, M., Szpiro, L., Bouchami, D., Durimel, L., Moulès, V., & Hardy, P. (2021). Assessment of Microbial Reduction by Cage Washing and Thermal Disinfection using Quantitative Biologic Indicators for Spores, Viruses and Vegetative Bacteria. Journal of the American Association for Laboratory Animal Science: JAALAS, 60(5), 529–538. https://doi.org/10.30802/AALAS-JAALAS-21-000026

Morlot, C., & Rodrigues, C. D. A. (2018). The New Kid on the Block: A Specialized Secretion System during Bacterial Sporulation. Trends in microbiology, 26(8), 663–676. https://doi.org/10.1016/j.tim.2018.01.001

Mortier, J., Cambré, A., Schack, S., Christie, G., & Aertsen, A. (2023). Impact of Protein Aggregates on Sporulation and Germination of Bacillus subtilis. Microorganisms, 11(9), 2365. https://doi.org/10.3390/microorganisms11092365

Norris, M. H., Bluhm, A. P., Metrailer, M. C., Jiranantasak, T., Kirpich, A., Hadfield, T., Ponciano, J. M., & Blackburn, J. K. (2023). Beyond the spore, the exosporium sugar anthrose impacts vegetative Bacillus anthracis gene regulation in cis and trans. Scientific reports, 13(1), 5060. https://doi.org/10.1038/s41598-023-32162-x

Pahalagedara, A. S. N. W., Gkogka, E., Ravn L. W., Hammershøj M. (2023). The growth potential and thermal resistance of bacterial spores under conditions relevant for ambient acid dairy-based products. Food Control, 152, 109841. https://doi.org/10.1016/j.foodcont.2023.109841

Paredes-Sabja, D., Setlow, B., Setlow, P., & Sarker, M. R. (2008). Characterization of Clostridium perfringens spores that lack SpoVA proteins and dipicolinic acid. Journal of bacteriology, 190(13), 4648–4659. https://doi.org/10.1128/JB.00325-08

Pedreira, T., Elfmann, C., & Stülke, J. (2022). The current state of SubtiWiki, the database for the model organism Bacillus subtilis. Nucleic acids research, 50(D1), D875–D882. https://doi.org/10.1093/nar/gkab943

Plaga, W., Stamm, I., & Schairer, H. U. (1998). Intercellular signaling in Stigmatella aurantiaca: purification and characterization of stigmolone, a myxobacterial pheromone. Proceedings of the National Academy of Sciences of the United States of America, 95(19), 11263–11267. https://doi.org/10.1073/pnas.95.19.11263

Pogliano, J., Osborne, N., Sharp, M. D., Abanes-De Mello, A., Perez, A., Sun, Y. L., & Pogliano, K. (1999). A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Molecular microbiology, 31(4), 1149–1159. https://doi.org/10.1046/j.1365-2958.1999.01255.x

Popham, D. L., Gilmore, M. E., & Setlow, P. (1999). Roles of low-molecular-weight penicillin-binding proteins in Bacillus subtilis spore peptidoglycan synthesis and spore properties. Journal of bacteriology, 181(1), 126–132. https://doi.org/10.1128/JB.181.1.126-132.1999

Qin, Y., Angelini, L. L., & Chai, Y. (2022). Bacillus subtilis Cell Differentiation, Biofilm Formation and Environmental Prevalence. Microorganisms, 10(6), 1108. https://doi.org/10.3390/microorganisms10061108

Romanovskaya, V. A., Rokitko, P. V., Gladka, G. V., & Tashyrev, A. B. (2016). Resistance to Dehydratation of Extremophilic Bacteria from Antarctic Region and Hypersaline Reservoirs. Mikrobiolohichnyi Zhurnal (Kiev, Ukraine: 1993), 78(2), 74–79. https://doi.org/10.15407/microbiolj78.02.074

Rybalchenko, N. P., Kharkhota, M. A. & Avdeeva, L. V. (2019). Influence of Cultivation Conditions on Lysing Activity of Bacillus amiloliquefaciens Strain IMV-7571. Mikrobiolohichnyi Zhurnal, 81(2). 25–35. https://doi.org/10.15407/microbiolj81.02.025

Sadoff H. L. (1973). Comparative aspects of morphogenesis in three prokaryotic genera. Annual review of microbiology, 27, 133–153. https://doi.org/10.1146/annurev.mi.27.100173.001025

Scepankova, H., Pinto, C. A., Estevinho, L. M., & Saraiva, J. A. (2022). High-Pressure-Based Strategies for the Inactivation of Bacillus subtilis Endospores in Honey. Molecules (Basel, Switzerland), 27(18), 5918. https://doi.org/10.3390/molecules27185918

Secaira-Morocho, H., Castillo, J. A., & Driks, A. (2020). Diversity and evolutionary dynamics of spore-coat proteins in spore-forming species of Bacillales. Microbial genomics, 6(11), mgen000451. https://doi.org/10.1099/mgen.0.000451

Serrano, M., Zilhão, R., Ricca, E., Ozin, A. J., Moran, C. P., Jr, & Henriques, A. O. (1999). A Bacillus subtilis secreted protein with a role in endospore coat assembly and function. Journal of bacteriology, 181(12), 3632–3643. https://doi.org/10.1128/JB.181.12.3632-3643.1999

Setlow P. (2006). Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. Journal of applied microbiology, 101(3), 514–525. https://doi.org/10.1111/j.1365-2672.2005.02736.x

Seyler, R. W., Jr, Henriques, A. O., Ozin, A. J., & Moran, C. P. (1997). Assembly and interactions of cotJ-encoded proteins, constituents of the inner layers of the Bacillus subtilis spore coat. Molecular microbiology, 25(5), 955–966. https://doi.org/10.1111/j.1365-2958.1997.mmi532.x

Smirnova, T. A., Minenkova, I. B., Orlova, M. V., Lecadet, M. M., & Azizbekyan, R. R. (1996). The crystal-forming strains of Bacillus laterosporus. Research in microbiology, 147(5), 343–350. https://doi.org/10.1016/0923-2508(96)84709-7

Smith, T. J., & Foster, S. J. (1995). Characterization of the involvement of two compensatory autolysins in mother cell lysis during sporulation of Bacillus subtilis 168. Journal of bacteriology, 177(13), 3855–3862. https://doi.org/10.1128/jb.177.13.3855-3862.1995

Srinivasan V. R. (1966). Sporogen–an "inductor" for bacterial cell division. Nature, 209(5022), 537. https://doi.org/10.1038/209537a0

Srinivasan, V. R. (1965). Intracellular regulation of sporulation of bacteria. In L. L. Campbell, & H. O. Halvorson (Eds.), Spore. Am Soc Microbiol. pp. 64–74.

Stephens C. (1998). Bacterial sporulation: a question of commitment? Current biology: CB, 8(2), R45–R48. https://doi.org/10.1016/S0960-9822(98)70031-4

Stragier, P., & Losick, R. (1996). Molecular genetics of sporulation in Bacillus subtilis. Annual review of genetics, 30, 297–341. https://doi.org/10.1146/annurev.genet.30.1.297

Sun, G., Yang, M., Jiang, L., & Huang, M. (2021). Regulation of pro-σK activation: a key checkpoint in Bacillus subtilis sporulation. Environmental microbiology, 23(5), 2366–2373. https://doi.org/10.1111/1462-2920.15415

Szulmajster, J. (1973). Initiation of bacterial sporogenesis, Svmp Soc Gen Microbiol, 23, 45–84.

Tocheva, E. I., Ortega, D. R., & Jensen, G. J. (2016). Sporulation, bacterial cell envelopes and the origin of life. Nature reviews. Microbiology, 14(8), 535–542. https://doi.org/10.1038/nrmicro.2016.85

Todosiichuk, T. S., Klochko, V. V., Savchuk, Ya. I. & Kobzysta, O. P. (2019). New Antibiotic Substances of the Streptomyces albus Enzybiotic Complex. Mikrobiolohichnyi Zhurnal, 81(5), 62–72. https://doi.org/10.15407/microbiolj81.05.062

Toukabri, H., Lereclus, D., & Slamti, L. (2023). A Sporulation-Independent Way of Life for Bacillus thuringiensis in the Late Stages of an Infection. mBio, 14(3), e0037123. https://doi.org/10.1128/mbio.00371-23

Vanek Z., & Winter, V. (1977a). Microbial differentiation, sporulation and metabolism of metabolites. Mikrobiolohichnyi Zhurnal, 39(3), 275–280.

Vanek Z., & Winter, V. (1977b). Regulatory processes during reproduction, sporulation and synthesis of metabolites in microorganisms. Mikrobiolohichnyi Zhurnal, 39(1), 683–695.

Vidwans, S. J., Ireton, K., & Grossman, A. D. (1995). Possible role for the essential GTP-binding protein Obg in regulating the initiation of sporulation in Bacillus subtilis. Journal of bacteriology, 177(11), 3308–3311. https://doi.org/10.1128/jb.177.11.3308-3311.1995

Voitsekhovsky, V. G. (1982). Study of the development of opportunistic spore-forming bacteria. Author's abstract. dis PhD. 03.00.07. 24 p. [In Ukrainian].

Wahia, H., Zhang, L., Zhou, C., Mustapha, A. T., Fakayode, O. A., Amanor-Atiemoh, R., Ma, H., & Dabbour, M. (2022). Pulsed multifrequency thermosonication induced sonoporation in Alicyclobacillus acidoterrestris spores and vegetative cells. Food research international (Ottawa, Ont.), 156, 111087. https://doi.org/10.1016/j.foodres.2022.111087

Willis, C., Errington, J., & Wu, L. J. (2020). Cohesion of Sister Chromosome Termini during the Early Stages of Sporulation in Bacillus subtilis. Journal of bacteriology, 202(20), e00296-20. https://doi.org/10.1128/JB.00296-20

Wu, L. J., Feucht, A., & Errington, J. (1998). Prespore-specific gene expression in Bacillus subtilis is driven by sequestration of SpoIIE phosphatase to the prespore side of the asymmetric septum. Genes & development, 12(9), 1371–1380. https://doi.org/10.1101/gad.12.9.1371

Wu, L. J., & Errington, J. (1998). Use of asymmetric cell division and spoIIIE mutants to probe chromosome orientation and organization in Bacillus subtilis. Molecular microbiology, 27(4), 777–786. https://doi.org/10.1046/j.1365-2958.1998.00724.x

Wu, L. J., & Errington, J. (1997). Septal localization of the SpoIIIE chromosome partitioning protein in Bacillus subtilis. The EMBO journal, 16(8), 2161–2169. https://doi.org/10.1093/emboj/16.8.2161

Wu, L. J., Lewis, P. J., Allmansberger, R., Hauser, P. M., & Errington, J. (1995). A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis. Genes & development, 9(11), 1316–1326. https://doi.org/10.1101/gad.9.11.1316

Zheng, L., Abhyankar, W., Ouwerling, N., Dekker, H. L., van Veen, H., van der Wel, N. N., Roseboom, W., de Koning, L. J., Brul, S., & de Koster, C. G. (2016). Bacillus subtilis Spore Inner Membrane Proteome. Journal of proteome research, 15(2), 585–594. https://doi.org/10.1021/acs.jproteome.5b00976

Downloads

Published

2024-09-03

How to Cite

Voitsekhovsky, V., Avdeeva, L., Balko, O., & Balko, O. (2024). Peculiarities of the Ontogenesis of Bacilli During Development from a Vegetative Cell to a Spore. Mikrobiolohichnyi Zhurnal, 86(4), 91-105. https://doi.org/10.15407/microbiolj86.04.091