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Bacteria and phenoptosis

  • Phenoptosis
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Abstract

Genetically programmed death of an organism, or phenoptosis, can be found not only in animals and plants, but also in bacteria. Taking into account intrapopulational relations identified in bacteria, it is easy to imagine the importance of phenoptosis in the regulation of a multicellular bacterial community in the real world of its existence. For example, autolysis of part of the population limits the spread of viral infection. Destruction of cells with damaged DNA contributes to the maintenance of low level of mutations. Phenoptosis can facilitate the exchange of genetic information in a bacterial population as a result of release of DNA from lysed cells. Bacteria use a special “language” to transmit signals in a population; it is used for coordinated regulation of gene expression. This special type of regulation of bacterial gene expression is usually active at high densities of bacteria populations, and it was named “quorum sensing” (QS). Different molecules can be used for signaling purposes. Phenoptosis, which is carried out by toxin-antitoxin systems, was found to depend on the density of the population; it requires a QS factor, which is called the extracellular death factor. The study of phenoptosis in bacteria is of great practical importance. The components that make up the systems ensuring the programmed cell death, including QS factor, may be used for the development of drugs that will activate mechanisms of phenoptosis and promote the destruction of pathogenic bacteria. Comparative genomic analysis revealed that the genes encoding several key enzymes involved in apoptosis of eukaryotes, such as paracaspases and metacaspases, apoptotic ATPases, proteins containing NACHT leucine-rich repeat, and proteases similar to mitochondrial HtrA-like protease, have homologs in bacteria. Proteomics techniques have allowed for the first time to identify the proteins formed during phenoptosis that participate in orderly liquidation of Streptomyces coelicolor and Escherichia coli cells. Among these proteins enzymes have been found that are involved in the degradation of cellular macromolecules, regulatory proteins, and stress-induced proteins. Future studies involving methods of biochemistry, genetics, genomics, proteomics, transcriptomics, and metabolomics should support a better understanding of the “mystery” of bacterial programmed cell death; this knowledge might be used to control bacterial populations.

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Abbreviations

ALD:

apoptotic-like death

EDF:

extracellular death factor

PCD:

programmed cell death

QS:

quorum sensing

TA complex:

toxin-antitoxin complex

References

  1. Skulachev, V. P. (1997) Biochemistry (Moscow), 62, 1191–1195.

    CAS  Google Scholar 

  2. Skulachev, V. P. (1999) Biochemistry (Moscow), 64, 1418–1426.

    CAS  Google Scholar 

  3. Longo, V. D., Mitteldorf, J., and Skulachev, V. P. (2005) Nat. Rev. Genet., 6, 886–872.

    Article  Google Scholar 

  4. Skulachev, V. P. (2012) Biochemistry (Moscow), 77, 689–706.

    Article  CAS  Google Scholar 

  5. Oleskin, A. V. (2001) Soros Obrazovat. Zh., 8, 7–12.

    Google Scholar 

  6. Gordeeva, A. V., Labas, Y. A., and Zvyagilskaya, R. A. (2004) Biochemistry (Moscow), 69, 1055–1066.

    Article  CAS  Google Scholar 

  7. Prozorov, A. A., and Danilenko, V. N. (2010) Microbiology (Moscow), 79, 129–140.

    Article  CAS  Google Scholar 

  8. Lee, H. H., Molla, M. N., Cantor, C. R., and Collins, J. J. (2010) Nature, 467, 82–85.

    Article  PubMed  CAS  Google Scholar 

  9. Tanouchi, Y., Pai, A., Buchler, N. E., and You, L. (2012) Mol. Syst. Biol., 8, 626.

    Article  PubMed  Google Scholar 

  10. Reuven, P., and Avigdor, E. (2011) Curr. Opin. Genet. Dev., 21, 759–767.

    Article  PubMed  CAS  Google Scholar 

  11. Khmel, I. A. (2006) Microbiology (Moscow), 75, 390–397.

    Article  CAS  Google Scholar 

  12. Khmel, I. A., and Metlitskaya, A. Z. (2006) Mol. Biol. (Moscow), 40, 169–182.

    Article  CAS  Google Scholar 

  13. Waters, C., and Bassler, B. (2005) Annu. Rev. Cell Dev. Biol., 21, 319–346.

    Article  PubMed  CAS  Google Scholar 

  14. Miller, M. B., and Bassler, B. L. (2001) Annu. Rev. Microbiol., 55, 165–199.

    Article  PubMed  CAS  Google Scholar 

  15. Shpakov, A. O. (2009) Microbiology (Moscow), 78, 133–143.

    Article  CAS  Google Scholar 

  16. Carmona-Fontaine, C., and Xavier, J. B. (2012) Mol. Syst. Biol., 8, 627–628.

    Article  PubMed  Google Scholar 

  17. Mittenhuber, G. (1999) J. Mol. Microbiol. Biotechnol., 1, 295–302.

    PubMed  CAS  Google Scholar 

  18. Hayes, F. (2003) Science, 301, 1496–1499.

    Article  PubMed  CAS  Google Scholar 

  19. Pandey, D. P., and Gerdes, K. (2005) Nucleic Acids Res., 33, 966–976.

    Article  PubMed  CAS  Google Scholar 

  20. Gerdes, K., and Wagner, E. G. (2007) Curr. Opin. Microbiol., 10, 117–124.

    Article  PubMed  CAS  Google Scholar 

  21. Fozo, E. M., Hemm, M. R., and Storz, G. (2008) Microbiol. Mol. Biol. Rev., 72, 579–589.

    Article  PubMed  CAS  Google Scholar 

  22. Fineran, P. C., Blower, T. R., Foulds, I. J., Humphreys, D. P., Lilley, K. S., and Salmond, G. P. (2009) Proc. Natl. Acad. Sci. USA, 106, 894–899.

    Article  PubMed  CAS  Google Scholar 

  23. Gerdes, K., Christensen, S. K., and Lobner-Olesen, A. (2005) Nat. Rev. Microbiol., 3, 371–382.

    Article  PubMed  CAS  Google Scholar 

  24. Yamaguchi, Y., Park, J. H., and Inouye, M. (2011) Annu. Rev. Genet., 45, 61–79.

    Article  PubMed  CAS  Google Scholar 

  25. Mutschler, H., Gebhardt, M., Shoeman, R. L., and Meinhart, A. (2011) PLoS Biol., 9, e1001033.

    Article  PubMed  CAS  Google Scholar 

  26. Aizenman, E., Engelberg-Kulka, H., and Glaser, G. (1996) Proc. Natl. Acad. Sci. USA, 93, 6059–6063.

    Article  PubMed  CAS  Google Scholar 

  27. Mittenhuber, G. (1999) J. Mol. Microbiol. Biotechnol., 1, 295–302.

    PubMed  CAS  Google Scholar 

  28. Engelberg-Kulka, H., Hazan, R., and Amitai, S. (2005) J. Cell Sci., 118, 4327–4332.

    Article  PubMed  CAS  Google Scholar 

  29. Zhang, Y., Zhang, J., Hoeflich, K. P., Ikura, M., Qing, G., and Inouye, M. (2003) Mol. Cell, 12, 913–923.

    Article  PubMed  CAS  Google Scholar 

  30. Zhang, Y., Zhang, J., Hara, H., Kato, I., and Inouye, M. (2005) J. Biol. Chem., 280, 3143–3150.

    Article  PubMed  CAS  Google Scholar 

  31. Hazan, R., Sat, B., and Engelberg-Kulka, H. (2004) J. Bacteriol., 186, 3663–3669.

    Article  PubMed  CAS  Google Scholar 

  32. Hayes, F. (2003) Science, 301, 1496–1499.

    Article  PubMed  CAS  Google Scholar 

  33. Gerdes, K., Christensen, S. K., and Lobner-Olesen, A. (2005) Nat. Rev. Microbiol., 3, 371–382.

    Article  PubMed  CAS  Google Scholar 

  34. Pandey, D. P., and Gerdes, K. (2005) Nucleic Acids Res., 33, 966–976.

    Article  PubMed  CAS  Google Scholar 

  35. Makarova, K., Wolf, Y., and Koonin, E. (2009) Biol. Direct., 4, 19.

    Article  PubMed  Google Scholar 

  36. Leplae, R., Geeraerts, D., Hallez, R., Guglielmini, J., Dreze, P., and van Melderen, L. (2011) Nucleic Acids Res., 39, 5513–5525.

    Article  PubMed  CAS  Google Scholar 

  37. Yamaguchi, Y., and Inouye, M. (2011) Nat. Rev. Microbiol., 9, 779–790.

    Article  PubMed  CAS  Google Scholar 

  38. Maisonneuve, E., Shakespeare, L. J., Jorgensen, M. G., and Gerdes, K. (2011) Proc. Natl. Acad. Sci. USA, 108, 13206–13211.

    Article  PubMed  CAS  Google Scholar 

  39. Kolodkin-Gal, I., Hazan, R., Gaathon, A., Carmeli, S., and Engelberg-Kulka, H. (2007) Science, 318, 652–655.

    Article  PubMed  CAS  Google Scholar 

  40. Kolodkin-Gal, I., and Engelberg-Kulka, H. (2008) J. Bacteriol., 190, 3169–3175.

    Article  PubMed  CAS  Google Scholar 

  41. Amitai, S., Kolodkin-Gal, I., Hananya-Meltabashi, M., Sacher, A., and Engelberg-Kulka, H. (2009) PLoS Genet., 5, e1000390; doi: 10.1371/journal.pgen.1000390.

  42. Belitsky, M., Avshalom, H., Erental, A., Yelin, I., Kumar, S., London, N., Sperber, M., Schueler-Furman, O., and Engelberg-Kulka, H. (2011) Mol. Cell, 41, 625–635.

    Article  PubMed  CAS  Google Scholar 

  43. Zhang, Y., Zhu, L., Zhang, J., and Inouye, M. (2005) J. Biol. Chem., 280, 26080–26088.

    Article  PubMed  CAS  Google Scholar 

  44. Erental, A., Sharon, I., and Engelberg-Kulka, H. (2012) PLoS Biol., 10, e1001281; doi: 10.1371/journal.pbio.1001281.

  45. Engelberg-Kulka, H., Sat, B., Reches, M., Amitai, S., and Hazan, R. (2004) Trends Microbiol., 12, 66–71.

    Article  PubMed  CAS  Google Scholar 

  46. Koonin, E. V., and Aravind, L. (2002) Cell Death Differ., 9, 394–404.

    Article  PubMed  CAS  Google Scholar 

  47. Frade, J. M., and Michaelidis, T. M. (1997) Bioessays, 19, 827–832.

    Article  PubMed  CAS  Google Scholar 

  48. Koksharova, O. A. (2010) Microbiology, 79, 721–734.

    Article  CAS  Google Scholar 

  49. Bidle, K. D., and Falkowski, P. G. (2004) Nat. Rev. Microbiol., 2, 643–655.

    Article  PubMed  CAS  Google Scholar 

  50. Berman-Frank, I., Bidle, K., Haramaty, L., and Falkowski, P. (2004) Limnol. Oceanogr., 49, 997–1005.

    Article  Google Scholar 

  51. Moharikar, S., D’Souza, J. S., Kulkarni, A. B., and Rao, B. J. (2006) J. Phycol., 42, 423–433.

    Article  CAS  Google Scholar 

  52. Segovia, M., Haramaty, L., Berges, J. A., and Falkowski, P. G. (2003) Plant Physiol., 132, 99–105.

    Article  PubMed  CAS  Google Scholar 

  53. Vardi, A., Berman-Frank, I., Rozenberg, T., Hadas, O., Kaplan, A., and Levine, A. (1999) Curr. Biol., 9, 1061–1064.

    Article  PubMed  CAS  Google Scholar 

  54. Thornberry, N. A., and Lazebnik, Y. (1998) Science, 281, 1312–1316.

    Article  PubMed  CAS  Google Scholar 

  55. Uren, A. G., O’Rourke, K., Pisabarro, M. T., Seshagiri, S., Koonin, E. V., and Dixit, V. M. (2000) Mol. Cell, 6, 961–967.

    PubMed  CAS  Google Scholar 

  56. Madeo, F., Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S. J., Wesselborg, S., and Frohlich, K.-U. (2002) Mol. Cell, 9, 911–917.

    Article  PubMed  CAS  Google Scholar 

  57. Szallies, A., Kubata, B. K., and Duszenko, M. (2002) FEBS Lett., 517, 144–150.

    Article  PubMed  CAS  Google Scholar 

  58. Kusters, J. G., Gerrits, M. M., van Strijp, J. A., and Vandenbroucke-Grauls, C. M. (1997) Infect. Immun., 65, 3672–3679.

    PubMed  CAS  Google Scholar 

  59. Ning, S. B., Guo, H. L., Wang, L., and Song, Y. C. (2002) J. Appl. Microbiol., 93, 15–28.

    Article  PubMed  CAS  Google Scholar 

  60. Gautam, S., and Sharma, A. (2002) Mol. Microbiol., 44, 393–401.

    Article  PubMed  CAS  Google Scholar 

  61. Bayles, K. W. (2003) Trends Microbiol., 11, 306–311.

    Article  PubMed  CAS  Google Scholar 

  62. Manteca, A., Fernandez, M., and Sanchez, J. (2006) Res. Microbiol., 157, 143–152.

    Article  PubMed  CAS  Google Scholar 

  63. Leipe, D. D., Koonin, E. V., and Aravind, L. (2004) J. Mol. Biol., 343, 1–28.

    Article  PubMed  CAS  Google Scholar 

  64. Manteca, A., Mader, U., Connolly, B. A., and Sanchez, J. (2006) Proteomics, 6, 6008–6022.

    Article  PubMed  CAS  Google Scholar 

  65. He, Y. W., and Zhang, L. H. (2008) FEMS Microbiol. Rev., 32, 842–857.

    Article  PubMed  CAS  Google Scholar 

  66. Tao, F., He, Y. W., Wu, D. H., Swarup, S., and Zhang, L. H. (2010) J. Bacteriol., 192, 1020–1029.

    Article  PubMed  CAS  Google Scholar 

  67. Amitai, S., Kolodkin-Gal, I., Hananya-Meltabashi, M., Sacher, A., and Engelberg-Kulka, H. (2009) PLoS Genet., 5, e1000390.

    Article  PubMed  Google Scholar 

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Correspondence to O. A. Koksharova.

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Original Russian Text © O. A. Koksharova, 2013, published in Biokhimiya, 2013, Vol. 78, No. 9, pp. 1229–1238.

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Koksharova, O.A. Bacteria and phenoptosis. Biochemistry Moscow 78, 963–970 (2013). https://doi.org/10.1134/S0006297913090010

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