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Allolysis in bacteria

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Abstract

The review deals with the phenomenon of allolysis, i.e., lysis of a part of a bacterial population induced by a group of epigenetically differentiated cells of the same species or phylotype. Allolysis is best studied in two species of gram-positive bacteria, Streptococcus pneumoniae and Bacillus subtilis. In S. pneumoniae, allolysis is associated with the onset of the competence stage, while in B. subtilis it is associated with transition to the stage of spore formation. The mechanisms of allolysis are considered, as well as its possible role in the populational and symbiotic relationships of bacterial cells. The relation between allolysis ant the programmed death of a part of the cells within a bacterial population (apoptosis) is discussed.

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References

  1. Claverys, J.P., Prudhomme, M., and Martin, B., Induction of Competence Regulons as a General Response ao Stress in Gram-Positive Bacteria, Annu. Rev. Microbiol., 2006, vol. 60, pp. 451–475.

    Article  PubMed  CAS  Google Scholar 

  2. Petersen, F.C., Tao, L., and Scheie, A.A., DNA Binding-Uptake System: a Link Between Cell-to-Cell Communication and Biofilm Formation, J. Bacteriol., 2005, vol. 187, no. 13, pp. 4392–4000.

    Article  PubMed  CAS  Google Scholar 

  3. Moscoso, M., Garca, E., and López, R., Biofilm Formation by Streptococcus pneumoniae: Role of Choline, Extracellular DNA, and Capsular Polysaccharide in Microbial Accretion, J. Bacteriol., 2006, vol. 188, no. 22, pp. 7785–7795.

    Article  PubMed  CAS  Google Scholar 

  4. Jedrzejas, M.J., Pneumococcal Virulence Factors: Structure and Function, Microbiol. Mol. Biol. Rev., 2001, vol. 65, no. 2, pp. 187–207.

    Article  PubMed  CAS  Google Scholar 

  5. Bogaert, D., De Groot, R., and Hermans, P.W., Streptococcus pneumoniae Colonisation: the Key to Pneumococcal Disease, Lancet Infect. Dis., 2004, vol. 4, no. 3, pp. 144–154.

    Article  PubMed  CAS  Google Scholar 

  6. Dawid, S., Roche, A.M., and Weiser, J.N., The blp Bacteriocins of Streptococcus pneumoniae Mediate Intraspecies Competition Both in Vitro and in Vivo, Infect. Immun., 2007, vol. 75, no. 1, pp. 443–451.

    Article  PubMed  CAS  Google Scholar 

  7. Romero, P., López, R., and GarcHa, E., Key Role of Amino Acid Residues in the Dimerization and Catalytic Activation of the Autolysin LytA, an Important Virulence Factor in Streptococcus pneumoniae, J. Biol. Chem., 2007, vol. 282, no. 24, pp. 17729–17737.

    Article  PubMed  CAS  Google Scholar 

  8. García, P., Paz, González, M., García, E., García, J.L., and López, R., The Molecular Characterization of the First Autolytic Lysozyme of Streptococcus pneumoniae Reveals Evolutionary Mobile Domains, Mol. Microbiol., 1999, vol. 33, no. 1, pp. 128–138.

    Article  PubMed  Google Scholar 

  9. Kausmally, L., Johnsborg, O., Lunde, M., Knutsen, E., and Hövarstein, L.S., Choline-Binding Protein D (CbpD) in Streptococcus pneumoniae Is Essential for Competence-Induced Cell Lysis, J. Bacteriol., 2005, vol. 187, no. 13, pp. 4338–4345.

    Article  PubMed  CAS  Google Scholar 

  10. Pestova, E.V., Hövarstein, L.S., and Morrison, D.A., Regulation of Competence for Genetic Transformation in Streptococcus pneumoniae by an Auto-Induced Peptide Pheromone and a Two-Component Regulatory System, Mol. Microbiol., 1996, vol. 21, no. 4, pp. 853–862.

    Article  PubMed  CAS  Google Scholar 

  11. Campbell, E.A., Choi, S.Y., and Masure, H.R., A Competence Regulon in Streptococcus pneumoniae Revealed by Genomic Analysis, Mol. Microbiol., 1998, vol. 27, no. 5, pp. 929–939.

    Article  PubMed  CAS  Google Scholar 

  12. Alloing, G., Martin, B., Granadel, C., and Claverys, J.P., Development of Competence in Streptococcus pneumonaie: Pheromone Autoinduction and Control of Quorum Sensing by the Oligopeptide Permease, Mol. Microbiol., 1998, vol. 29, no. 1, pp. 75–83.

    Article  PubMed  CAS  Google Scholar 

  13. Prozorov, A.A., Competence Pheromones in Bacteria, Mikrobiologiya, 2001, vol. 70, no. 1, pp. 5–14 [Microbiology (Engl. Transl.), vol. 70, no. 1, pp. 1–9].

    CAS  Google Scholar 

  14. Peterson, S.N., Sung, C.K., Cline, R., Desai, B.V., Snesrud, E.C., Luo, P., Walling, J., Li, H., Mintz, M., Tsegaye, G., Burr, P.C., Do, Y., Ahn, S., Gilbert, J., Fleischmann, R.D., and Morrison, D.A., Identification of Competence Pheromone Responsive Genes in Streptococcus pneumoniae by Use of DNA Microarrays, Mol. Microbiol., 2004, vol. 51, no. 4, pp. 1051–1070.

    Article  PubMed  CAS  Google Scholar 

  15. Pozzi, G., Masala, L., Iannelli, F., Manganelli, R., Havarstein, L.S., Piccoli, L., Simon, D., and Morrison, D.A., Competence for Genetic Transformation in Encapsulated Strains of Streptococcus pneumoniae: Two Allelic Variants of the Peptide Pheromone, J. Bacteriol., 1996, vol. 178, no. 20, pp. 6087–6090.

    PubMed  CAS  Google Scholar 

  16. Håvarstein, L.S., Hakenbeck, R., and Gaustad, P., Natural Competence in the Genus Streptococcus: Evidence That Streptococci Can Change Pherotype by Interspecies Recombinational Exchanges, J. Bacteriol., 1997, vol. 179, no. 21, pp. 6589–6594.

    PubMed  Google Scholar 

  17. Håvarstein, L.S., Gaustad, P., Nes, I.F., and Morrison, D.A., Identification of the Streptococcal Competence-Pheromone Receptor, Mol. Microbiol., 1996, vol. 21, no. 4, pp. 863–869.

    Article  PubMed  Google Scholar 

  18. Ottolenghi, E. and Hotchkiss, R.D., Appearance of Genetic Transforming Activity in Pneumococcal Cultures, Science, 1960, vol. 132, pp. 1257–1258.

    PubMed  CAS  Google Scholar 

  19. Prozorov, A.A., Transformatsiya u bakterii (Transformation in Bacteria), Moscow: Nauka, 1988.

    Google Scholar 

  20. Steinmoen, H., Knutsen, E., and Håvarstein, L.S., Induction of Natural Competence in Streptococcus pneumoniae Triggers Lysis and DNA Release from a Subfraction of the Cell Population, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, no. 11, pp. 7681–7686.

    Article  PubMed  CAS  Google Scholar 

  21. Steinmoen, H., Teigen, A., and Håvarstein, L.S., Competence-Induced Cells of Streptococcus pneumoniae Lyse Competence-Deficient Cells of the Same Strain During Cocultivation, J. Bacteriol., 2003, vol. 185, no. 24, pp. 7176–7183.

    Article  PubMed  CAS  Google Scholar 

  22. Moscoso, M. and Claverys, J.P., Release of DNA into the Medium by Competent Streptococcus pneumoniae: Kinetics, Mechanism and Stability of the Liberated DNA, Mol. Microbiol., 2004, vol. 54, no. 3, pp. 783–794.

    Article  PubMed  CAS  Google Scholar 

  23. Guiral, S., Mitchell, T.J., Martin, B., and Claverys, J.P., Competence-Programmed Predation of Noncompetent Cells in the Human Pathogen Streptococcus pneumoniae: Genetic Requirements, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, no. 24, pp. 8710–8715.

    Article  PubMed  CAS  Google Scholar 

  24. Håvarstein, L.S., Martin, B., Johnsborg, O., Granadel, C., and Claverys, J.P., New Insights Into the Pneumococcal Fratricide: Relationship to Clumping and Identification of a Novel Immunity Factor, Mol. Microbiol., 2006, vol. 59, no. 4, pp. 1297–1307.

    Article  PubMed  Google Scholar 

  25. Claverys, J.P. and Håvarstein, L.S., Cannibalism and Fratricide: Mechanisms and Raisons d’être, Nat. Rev. Microbiol., 2007, vol. 5, no. 3, pp. 219–229.

    Article  PubMed  CAS  Google Scholar 

  26. Claverys, J.P., Martin, B., and Håvarstein, L.S., Competence-Induced Fratricide in Streptococci, Mol. Microbiol., 2007, vol. 64, no. 6, pp. 1423–1433.

    Article  PubMed  CAS  Google Scholar 

  27. Martner, A., Dahlgren, C., Paton, J.C., and Wold, A.E., Pneumolysin Released During Streptococcus pneumoniae Autolysis Is a Potent Activator of Intracellular Oxygen Radical Production in Neutrophils, Infect. Immun., 2008, vol. 76, no. 9, pp. 4079–4087.

    Article  PubMed  CAS  Google Scholar 

  28. Johnsborg, O., Eldholm, V., Bjørnstad, M.L., and Håvarstein, L.S., A Predatory Mechanism Dramatically Increases the Efficiency of Lateral Gene Transfer in Streptococcus pneumoniae and Related Commensal Species, Mol. Microbiol., 2008, vol. 69, no. 1 P, pp. 245–253.

    Article  PubMed  CAS  Google Scholar 

  29. Henriques-Normark, B., Blomberg, C., Dagerhamn, J., Bättig, P., and Normark, S., The Rise and Fall of Bacterial Clones: Streptococcus pneumoniae, Nat. Rev. Microbiol., 2008, vol. 6, no. 11, pp. 827–837.

    Article  PubMed  CAS  Google Scholar 

  30. Gilmore, M.S. and Haas, W., The Selective Advantage of Microbial Fratricide, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, no. 24, pp. 8401–8402.

    Article  PubMed  CAS  Google Scholar 

  31. Kreth, J., Merritt, J., Shi, W., and Qi, F., Co-Ordinated Bacteriocin Production and Competence Evelopment: a Possible Mechanism for Taking up DNA from Neighbouring Species, Mol. Microbiol., 2005, vol. 57, no. 2, pp. 392–404.

    Article  PubMed  CAS  Google Scholar 

  32. Hilbert, D.W. and Piggot, P.J., Compartmentalization of Gene Expression During Bacillus subtilis Spore Formation, Microbiol. Mol. Biol. Rev., 2004, vol. 68, no. 2, pp. 234–262.

    Article  PubMed  CAS  Google Scholar 

  33. Dworkin, J. and Losick, R., Developmental Commitment in a Bacterium, Cell, 2005, vol. 121, no. 3, pp. 401–409.

    Article  PubMed  CAS  Google Scholar 

  34. Molle, V., Fujita, M., Jensen, S.T., Eichenberger, P., González-Pastor, J.E., Liu, J.S., and Losick, R., The Spo0A Regulon of Bacillus subtilis, Mol. Microbiol., 2003, vol. 50, no. 5, pp. 1683–1701.

    Article  PubMed  CAS  Google Scholar 

  35. Fawcett, P., Eichenberger, P., Losick, R., and Youngman, P., The Transcriptional Profile of Early to Middle Sporulation in Bacillus subtilis, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 14, pp. 8063–8068.

    Article  PubMed  CAS  Google Scholar 

  36. Bischofs, I.B., Hug, J.A., Liu, A.W., Wolf, D.M., and Arkin, A.P., Complexity in Bacterial Cell-Cell Communication: Quorum Signal Integration and Subpopulation Signaling in the Bacillus subtilis Phosphorelay, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, no. 16, pp. 6459–6464.

    Article  PubMed  CAS  Google Scholar 

  37. Fujita, M., González-Pastor, J.E., and Losick, R., High- and Low-Threshold Genes in the Spo0A Regulon of Bacillus subtilis, J. Bacteriol., 2005, vol. 187, no. 4, pp. 1357–1368.

    Article  PubMed  CAS  Google Scholar 

  38. González-Pastor, J.E., Hobbs, E.C., and Losick, R., Cannibalism by Sporulating Bacteria, Science, 2003, vol. 301, no. 5632, pp. 510–513.

    Article  PubMed  Google Scholar 

  39. Smith, T.J., Blackman, S.A., and Foster, S.J., Autolysins of Bacillus subtilis: Multiple Enzymes with Multiple Functions, Microbiology (UK), 2000, vol. 146.

  40. Ellermeier, C.D., Hobbs, E.C., Gonzalez-Pastor, J.E., and Losick, R., A Three-Protein Signaling Pathway Governing Immunity to a Bacterial Cannibalism Toxin, Cell, 2006, vol. 124, no. 3, pp. 549–559.

    Article  PubMed  CAS  Google Scholar 

  41. López, D., Vlamakis, H., Losick, R., and Kolter, R., Cannibalism Enhances Biofilm Development in Bacillus subtilis, Mol. Microbiol., 2009, vol. 74, no. 3, pp. 609–618.

    Article  PubMed  Google Scholar 

  42. 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, no. 4, pp. 1229–1238.

    Article  PubMed  CAS  Google Scholar 

  43. Vlamakis, H., Aguilar, C., Losick, R., and Kolter, R., Control of Cell Fate by the Formation of an Architecturally Complex Bacterial Community, Genes Dev., 2008, vol. 22, no. 7, pp. 945–953.

    Article  PubMed  CAS  Google Scholar 

  44. Allenby, N.E., Watts, C.A., Homuth, G., Prágai, Z., Wipat, A., Ward, A.C., and Harwood, C.R., Phosphate Starvation Induces the Sporulation Killing Factor of Bacillus subtilis, J. Bacteriol., 2006, vol. 188, no. 14, pp. 5299–5303.

    Article  PubMed  CAS  Google Scholar 

  45. Nandy, S.K., Bapat, P.M., and Venkatesh, K.V., Sporulating Bacteria Prefers Predation to Cannibalism in Mixed Cultures, FEBS Lett., 2007, vol. 581, no. 1, pp. 51–56.

    Article  Google Scholar 

  46. Engelberg-Kulka, H. and Hazan, R., Microbiology. Cannibals Defy Starvation and Avoid Sporulation, Science, 2003, vol. 301, no. 5632, pp. 467–468.

    Article  PubMed  CAS  Google Scholar 

  47. Stragier, P., To Kill but Not Be Killed: a Delicate Balance, Cell, 2006, vol. 124, no. 3, pp. 461–463.

    Article  PubMed  CAS  Google Scholar 

  48. Rice, K.C. and Bayles, K.W., Molecular Control of Bacterial Death and Lysis, Microbiol. Mol. Biol. Rev., 2008, vol. 72, no. 1, pp. 85–109.

    Article  PubMed  CAS  Google Scholar 

  49. Dubnau, D. and Losick, R., Bistability in Bacteria, Mol. Microbiol., 2006, vol. 61, no. 3, pp. 564–572.

    Article  PubMed  CAS  Google Scholar 

  50. Veening, J.W., Smits, W.K., and Kuipers, O.P., Bistability, Epigenetics, and Bet-Hedging in Bacteria, Annu. Rev. Microbiol., 2008, vol. 62, pp. 193–210.

    Article  PubMed  CAS  Google Scholar 

  51. Davidson, C.J. and Surette, M.G., Individuality in Bacteria, Ann. Rev. Genet., 2008, vol. 42, pp. 253–268.

    Article  PubMed  CAS  Google Scholar 

  52. Gardner, A. and Kümmerli, R., Social Evolution: This Microbe Will Self-Destruct, Curr. Biol., 2008, vol. 18, no. 21, pp. R1021–R1023.

    Article  PubMed  CAS  Google Scholar 

  53. Pandey, D.P. and Gerdes, K., Toxin-Antitoxin Loci Are Highly Abundant in Free-Living but Lost from Host-Associated Prokaryotes, Nucleic Acids Res., 2005, vol. 33, no. 3, pp. 966–976.

    Article  PubMed  CAS  Google Scholar 

  54. Prozorov, A.A. and Danilenko, V.N., Toxin-Antitoxin Systems in Bacteria: Apoptotic Tools or Metabolic Regulators?, Mikrobiologiya, 2010, vol. 79, no. 2, pp. 238–250 [Microbiology (Engl. Transl.), vol. 79, no. 2, pp. 129–140].

    Google Scholar 

  55. Van Melderen, L. and Saavedra, De Bast, M., Bacterial Toxin-Antitoxin Systems: More Than Selfish Entities?, PLoS Genet., 2009, vol. 5, no. 3, pp. 1–6.

    Google Scholar 

  56. Nieto, C., Pellicer, T., Balsa, D., Christensen, S.K., Gerdes, K., and Espinosa, M., The Chromosomal relBE2 Toxin-Antitoxin Locus of Streptococcus pneumoniae: Characterization and Use of a Bioluminescence Resonance Energy Transfer Assay to Detect Toxin-Antitoxin Interaction, Mol. Microbiol., 2006, vol. 59, no. 4, pp. 1280–1296.

    Article  PubMed  CAS  Google Scholar 

  57. Wireman, J.W. and Dworkin, M., Morphogenesis and Developmental Interactions in Myxobacteria, Science, 1975, vol. 189, no. 4202, pp. 516–523.

    Article  PubMed  CAS  Google Scholar 

  58. Kaiser, D., Signaling in Myxobacteria, Annu. Rev. Microbiol., 2004, vol. 58, pp. 75–98.

    Article  PubMed  CAS  Google Scholar 

  59. Berleman, J.E. and Kirby, J.R., Deciphering the Hunting Strategy of a Bacterial Wolfpack, FEMS Microbiol. Rev., 2009, vol. 33, no. 5, pp. 942–957.

    Article  PubMed  CAS  Google Scholar 

  60. Zhang, H., Dong, H., Zhao, J., Hu, W., and Li, Y.Z., Characterization of Developmental Autolysis in Myxobacterial Fruiting Body Morphogenesis with Profiling of Amino Acids Using Capillary Electrophoresis Method, Amino Acids, 2005, vol. 28, no. 3, pp. 319–325.

    Article  PubMed  CAS  Google Scholar 

  61. Nariya, H. and Inouye, M., MazF, an MRNA Interferase, Mediates Programmed Cell Death During Multicellular Myxococcus Development, Cell, 2008, vol. 132, no. 1, pp. 55–66.

    Article  PubMed  CAS  Google Scholar 

  62. Kalakoutskii, L.V. and Agre, N.S., Comparative Aspects of Development and Differentiation in Actinomycetes, Bacteriol. Rev., 1976, vol. 40, no. 2, pp. 469–524.

    PubMed  CAS  Google Scholar 

  63. Hodson, D., Differentiation in Actinomycetes, in Procaryotic Structure and Function: a New Perspective, Mohan, S. et al., Eds., Cambrige Univ. Press, 1992, pp. 407–440.

  64. Manteca, A., Fernández, M., and Sánchez, J., A Death Round Affecting a Young Compartmentalized Mycelium Precedes Aerial Mycelium Dismantling in Confluent Surface Cultures of Streptomyces antibioticus, Microbiology (UK), 2005, vol. 151, no. 11, pp. 3689–3697.

    CAS  Google Scholar 

  65. Manteca, A., Fernandez, M., and Sánchez, J., Cytological and Biochemical Evidence for an Early Cell Dismantling Event in Surface Cultures of Streptomyces antibioticus, Res. Microbiol., 2006, vol. 157, no. 2, pp. 143–152.

    Article  PubMed  CAS  Google Scholar 

  66. Elizarov, S.M. and Danilenko, V.N., Multiple Phosphorylation of Membrane-Associated Calcium-Dependent Protein Serine/Threonine Kinase in Streptomyces fradiae, FEMS Microbiol. Lett., 2001, vol. 202, no. 1, pp. 135–138.

    Article  PubMed  CAS  Google Scholar 

  67. Petrícková, K. and Petrícek, M., Eukaryotic-Type Protein Kinases in Streptomyces coelicolor: Variations on a Common Theme, Microbiology (UK), 2003, vol. 149, no. 7, pp. 1609–1621.

    Article  Google Scholar 

  68. Danilenko, V.N., Mironov, V.A., and Elizarov, S.M., Calcium as a Regulator of Intracellular Processes in Actinomycetes: A Review, Prikl. Biokhim. Mikrobiol., 2005, vol. 41, no. 2, pp. 319–329 [Appl. Biochem. Microbiol. (Engl. Transl.), vol. 41, no. 4, pp. 319–329].

    CAS  Google Scholar 

  69. Kennelly, P.J., Protein Kinases and Protein Phosphatases in Prokaryotes: a Genomic Perspective, FEMS Microbiol. Lett., 2002, vol. 206, no. 1, pp. 1–8.

    Article  PubMed  CAS  Google Scholar 

  70. Echenique, J., Kadioglu, A., Romao, S., Andrew, P.W., and Trombe, M.C., Protein Serine/Threonine Kinase StkP Positively Controls Virulence and Competence in Streptococcus pneumoniae, Infect. Immun., 2004, vol. 72, no. 4, pp. 2434–2437.

    Article  PubMed  CAS  Google Scholar 

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Original Russian Text © A.A. Prozorov, V.N. Danilenko, 2011, published in Mikrobiologiya, 2011, Vol. 80, No. 1, pp. 3–12.

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Prozorov, A.A., Danilenko, V.N. Allolysis in bacteria. Microbiology 80, 1–9 (2011). https://doi.org/10.1134/S0026261711010139

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