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  • Review Article
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Microbial ageing and longevity

A Publisher Correction to this article was published on 26 September 2019

This article has been updated

Abstract

Longevity reflects the ability to maintain homeostatic conditions necessary for life as an organism ages. A long-lived organism must contend not only with environmental hazards but also with internal entropy and macromolecular damage that result in the loss of fitness during ageing, a phenomenon known as senescence. Although central to many of the core concepts in biology, ageing and longevity have primarily been investigated in sexually reproducing, multicellular organisms. However, growing evidence suggests that microorganisms undergo senescence, and can also exhibit extreme longevity. In this Review, we integrate theoretical and empirical insights to establish a unified perspective on senescence and longevity. We discuss the evolutionary origins, genetic mechanisms and functional consequences of microbial ageing. In addition to having biomedical implications, insights into microbial ageing shed light on the role of ageing in the origin of life and the upper limits to longevity.

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Fig. 1: Reproductive asymmetry enables microbial ageing.
Fig. 2: The relationship between body size and lifespan.
Fig. 3: Damage to cellular molecules during ageing.
Fig. 4: Asymmetrical reproduction in different microorganisms.

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  • 26 September 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

References

  1. Kapahi, P., Kaeberlein, M. & Hansen, M. Dietary restriction and lifespan: lessons from invertebrate models. Ageing Res. Rev. 39, 3–14 (2017).

    Article  PubMed  Google Scholar 

  2. Yuan, R., Peters, L. L. & Paigen, B. Mice as a mammalian model for research on the genetics of aging. ILAR J. 52, 4–15 (2011).

    Article  CAS  PubMed  Google Scholar 

  3. Plomion, C. et al. Oak genome reveals facets of long lifespan. Nat. Plants 4, 440–452 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Vazquez, J. M., Sulak, M., Chigurupati, S. & Lynch, V. J. A zombie LIF gene in elephants is upregulated by TP53 to induce apoptosis in response to DNA damage. Cell Rep. 24, 1765–1776 (2018).

    Article  CAS  PubMed  Google Scholar 

  5. Ruby, J. G., Smith, M. & Buffenstein, R. Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age. eLife 7, e31157 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Partridge, L. & Barton, N. H. Optimality, mutation and the evolution of ageing. Nature 362, 305–311 (1993).

    Article  CAS  PubMed  Google Scholar 

  7. Kirkwood, T. B. & Austad, S. N. Why do we age? Nature 408, 233–238 (2000).

    Article  CAS  PubMed  Google Scholar 

  8. Kirkwood, T. B. L. Asymmetry and the origins of ageing. Mech. Ageing Dev. 126, 533–534 (2005).

    Article  PubMed  Google Scholar 

  9. Bell, G. Evolutionary and nonevolutionary theories of senescence. Am. Nat. 124, 600–603 (1984).

    Article  Google Scholar 

  10. Ackermann, M., Chao, L., Bergstrom, C. T. & Doebeli, M. On the evolutionary origin of aging. Aging Cell 6, 235–244 (2007). This article presents one of the first theoretical and quantitative models for the evolution of ageing and asymmetrical reproduction in single-celled organisms.

    Article  CAS  PubMed  Google Scholar 

  11. Kirkwood, T. B. L. Understanding the odd science of aging. Cell 120, 437–447 (2005).

    Article  CAS  PubMed  Google Scholar 

  12. Johnson, L. R. & Mangel, M. Life histories and the evolution of aging in bacteria and other single-celled organisms. Mech. Ageing Dev. 127, 786–793 (2006).

    Article  CAS  PubMed  Google Scholar 

  13. Tyedmers, J., Mogk, A. & Bukau, B. Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 11, 777–788 (2010).

    Article  CAS  PubMed  Google Scholar 

  14. Kysela, D. T., Brown, P. J. B., Huang, K. C. & Brun, Y. V. Biological consequences and advantages of asymmetric bacterial growth. Annu. Rev. Microbiol. 67, 417–435 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Angert, E. R. Alternatives to binary fission in bacteria. Nat. Rev. Microbiol. 3, 214–224 (2005).

    Article  CAS  PubMed  Google Scholar 

  16. Mortimer, R. K. & Johnston, J. R. Life span of individual yeast cells. Nature 183, 1751–1752 (1959). This article presents one of the first studies documenting ageing in a microorganism.

    Article  CAS  PubMed  Google Scholar 

  17. Longo, V. D., Shadel, G. S., Kaeberlein, M. & Kennedy, B. Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab. 16, 18–31 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ackermann, M., Stearns, S. C. & Jenal, U. Senescence in a bacterium with asymmetric division. Science 300, 1920–1920 (2003).

    Article  CAS  PubMed  Google Scholar 

  19. Laney, S. R., Olson, R. J. & Sosik, H. M. Diatoms favor their younger daughters. Limnol. Oceanogr. 57, 1572–1578 (2012).

    Article  Google Scholar 

  20. Lindner, A. B., Madden, R., Demarez, A., Stewart, E. J. & Taddei, F. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl Acad. Sci. USA 105, 3076–3081 (2008). This work shows that damaged protein aggregates are associated with reproductive senescence in E. coli.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Stewart, E. J., Madden, R., Paul, G. & Taddei, F. Aging and death in an organism that reproduces by morphologically symmetric division. PLOS Biol. 3, e45 (2005). This article is one of the first studies to document ageing in a microorganism that reproduces by binary fission.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Boehm, A. et al. Genetic manipulation of glycogen allocation affects replicative lifespan in E. coli. PLOS Genet. 12, e1005974 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Coelho, M., Lade, S. J., Alberti, S., Gross, T. & Tolić, I. M. Fusion of protein aggregates facilitates asymmetric damage segregation. PLOS Biol. 12, e1001886 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Proenca, A. M., Rang, C. U., Buetz, C., Shi, C. & Chao, L. Age structure landscapes emerge from the equilibrium between aging and rejuvenation in bacterial populations. Nat. Commun. 9, 3722 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hamilton, W. D. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45 (1966).

    Article  CAS  PubMed  Google Scholar 

  26. Caswell, H. Matrix Population Models: Construction, Analysis, Interpretation (Sinauer Associates, 2001).

  27. Gibson, B., Wilson, D. J., Feil, E. & Eyre-Walker, A. The distribution of bacterial doubling times in the wild. Proc. R. Soc. B Biol. Sci. 285, 20180789 (2018).

    Article  CAS  Google Scholar 

  28. Orsi, W. D. Ecology and evolution of seafloor and subseafloor microbial communities. Nat. Rev. Microbiol. 16, 671–683 (2018).

    Article  CAS  PubMed  Google Scholar 

  29. Jørgensen, B. B. & Marshall, I. P. G. Slow microbial life in the seabed. Annu. Rev. Mar. Sci. 8, 311–332 (2016). This review examines patterns of microbial ageing and longevity in the deep biosphere environment.

    Article  Google Scholar 

  30. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article  Google Scholar 

  31. Johnson, S. S. et al. Ancient bacteria show evidence of DNA repair. Proc. Natl Acad. Sci. USA 104, 14401–14405 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Jaakkola, S. T. et al. The complete genome of a viable archaeum isolated from 123-million-year-old rock salt: genome sequence of Halobacterium hubeiense. Environ. Microbiol. 18, 565–579 (2016).

    Article  CAS  PubMed  Google Scholar 

  33. Greenblatt, C. L. et al. Micrococcus luteus—survival in amber. Microb. Ecol. 48, 120–127 (2004).

    Article  CAS  PubMed  Google Scholar 

  34. Trembath-Reichert, E. et al. Methyl-compound use and slow growth characterize microbial life in 2-km-deep subseafloor coal and shale beds. Proc. Natl Acad. Sci. USA 114, E9206–E9215 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Braun, S. et al. Microbial turnover times in the deep seabed studied by amino acid racemization modelling. Sci. Rep. 7, 5680 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Starnawski, P. et al. Microbial community assembly and evolution in subseafloor sediment. Proc. Natl Acad. Sci. USA 114, 2940–2945 (2017). This study uses metagenomics and single-cell genomics to show that population genetic patterns among deep biosphere microorganisms are consistent with preadaptation to the low-energy environment, rather than ongoing adaptive evolution.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Medawar, P. An Unsolved Problem of Biology (H. K. Lewis, 1952).

  38. Williams, G. C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (1957).

    Article  Google Scholar 

  39. Haldane, J. B. S. New Paths in Genetics (Allen & Unwin, 1941).

  40. Caswell, H. A general formula for the sensitivity of population growth rate to changes in life history parameters. Theor. Popul. Biol. 14, 215–230 (1978).

    Article  CAS  PubMed  Google Scholar 

  41. Kirkwood, T. B. L. Evolution of ageing. Nature 270, 301–304 (1977). This paper proposes the disposable soma theory of ageing.

    Article  CAS  PubMed  Google Scholar 

  42. Kennedy, B. K., Austriaco, N. R. & Guarente, L. Daughter cells of Saccharomyces cerevisiae from old mothers display a reduced life span. J. Cell Biol. 127, 1985–1993 (1994).

    Article  CAS  PubMed  Google Scholar 

  43. Szilard, L. On the nature of the aging process. Proc. Natl Acad. Sci. USA 45, 30–45 (1959).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Jazwinski, S. M. Aging and senescence of the budding yeast Saccharomyces cerevisiae. Mol. Microbiol. 4, 337–343 (1990).

    Article  CAS  PubMed  Google Scholar 

  45. Ogrodnik, M., Salmonowicz, H. & Gladyshev, V. N. Integrating cellular senescence with the concept of damage accumulation in aging: relevance for clearance of senescent cells. Aging Cell 8, e12841 (2019).

    Article  CAS  Google Scholar 

  46. Gladyshev, V. N. The origin of aging: imperfectness-driven non-random damage defines the aging process and control of lifespan. Trends Genet. 29, 506–512 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Maynard, S., Fang, E. F., Scheibye-Knudsen, M., Croteau, D. L. & Bohr, V. A. DNA damage, DNA repair, aging, and neurodegeneration. Cold Spring Harb. Perspect. Med. 5, a025130 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Kirkwood, T. B. L. Evolution of ageing. Mech. Ageing Dev. 123, 737–745 (2002).

    Article  PubMed  Google Scholar 

  49. Flatt, T. & Partridge, L. Horizons in the evolution of aging. BMC Biol. 16, 93 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Austad, S. N. & Hoffman, J. M. Is antagonistic pleiotropy ubiquitous in aging biology? Evol. Med. Public Health 2018, 287–294 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Ricklefs, R. E. Insights from comparative analyses of aging in birds and mammals. Aging Cell 9, 273–284 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Sadowska-Bartosz, I. & Bartosz, G. Effect of glycation inhibitors on aging and age-related diseases. Mech. Ageing Dev. 160, 1–18 (2016).

    Article  CAS  PubMed  Google Scholar 

  53. Ricklefs, R. E. Intrinsic aging-related mortality in birds. J. Avian Biol. 31, 103–111 (2000).

    Article  Google Scholar 

  54. Ricklefs, R. E. The evolution of senescence from a comparative perspective. Funct. Ecol. 22, 379–392 (2008).

    Article  Google Scholar 

  55. Gladyshev, V. N. On the cause of aging and control of lifespan: heterogeneity leads to inevitable damage accumulation, causing aging; control of damage composition and rate of accumulation define lifespan. BioEssays 34, 925–929 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Voit, M. & Meyer-Ortmanns, H. How aging may be an unavoidable fate of dynamical systems. New J. Phys. 21, 043045 (2019).

    Article  CAS  Google Scholar 

  57. Risques, R. A. & Kennedy, S. R. Aging and the rise of somatic cancer-associated mutations in normal tissues. PLOS Genet. 14, e1007108 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Lee, M. B. et al. Defining the impact of mutation accumulation on replicative lifespan in yeast using cancer-associated mutator phenotypes. Proc. Natl Acad. Sci. USA 116, 3062–3071 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Carneiro, M. C., de Castro, I. P. & Ferreira, M. G. Telomeres in aging and disease: lessons from zebrafish. Dis. Model. Mech. 9, 737–748 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Blackburn, E. H., Epel, E. S. & Lin, J. Human telomere biology: a contributory and interactive factor in aging, disease risks, and protection. Science 350, 1193–1198 (2015).

    Article  CAS  PubMed  Google Scholar 

  61. Hu, Z. et al. Nucleosome loss leads to global transcriptional up-regulation and genomic instability during yeast aging. Genes Dev. 28, 396–408 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Zhang, K., Zheng, D.-Q., Sui, Y., Qi, L. & Petes, T. D. Genome-wide analysis of genomic alterations induced by oxidative DNA damage in yeast. Nucleic Acids Res. 47, 3521–3535 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  63. McMurray, M. A. & Gottschling, D. E. An age-induced switch to a hyper-recombinational state. Science 301, 1908–1911 (2003).

    Article  CAS  PubMed  Google Scholar 

  64. Baraibar, M. A., Ladouce, R. & Friguet, B. Proteomic quantification and identification of carbonylated proteins upon oxidative stress and during cellular aging. J. Proteom. 92, 63–70 (2013).

    Article  CAS  Google Scholar 

  65. Reverter-Branchat, G., Cabiscol, E., Tamarit, J. & Ros, J. Oxidative damage to specific proteins in replicative and chronological-aged Saccharomyces cerevisiae: common targets and prevention by calorie restriction. J. Biol. Chem. 279, 31983–31989 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Dasgupta, A., Zheng, J. & Bizzozero, O. A. Protein carbonylation and aggregation precede neuronal apoptosis induced by partial glutathione depletion. ASN Neuro 4, AN20110064 (2012).

    Article  CAS  Google Scholar 

  67. Maisonneuve, E., Ezraty, B. & Dukan, S. Protein aggregates: an aging factor involved in cell death. J. Bacteriol. 190, 6070–6075 (2008). This study shows that damaged protein aggregates are associated with survival senescence in E. coli.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Erjavec, N., Larsson, L., Grantham, J. & Nyström, T. Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev. 21, 2410–2421 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Vágási, C. I. et al. Longevity and life history coevolve with oxidative stress in birds. Funct. Ecol. 33, 152–161 (2019).

    Article  PubMed  Google Scholar 

  70. Hartl, F. U., Bracher, A. & Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature 475, 324–332 (2011).

    Article  CAS  PubMed  Google Scholar 

  71. Shafirovich, V. & Geacintov, N. E. Removal of oxidatively generated DNA damage by overlapping repair pathways. Free. Radic. Biol. Med. 107, 53–61 (2017).

    Article  CAS  PubMed  Google Scholar 

  72. Wigley, D. B. Bacterial DNA repair: recent insights into the mechanism of RecBCD, AddAB and AdnAB. Nat. Rev. Microbiol. 11, 9–13 (2013).

    Article  CAS  PubMed  Google Scholar 

  73. Wensink, M. J., Caswell, H. & Baudisch, A. The rarity of survival to old age does not drive the evolution of senescence. Evol. Biol. 44, 5–10 (2017).

    Article  PubMed  Google Scholar 

  74. Kirkwood, T. B. L. & Holliday, R. The evolution of ageing and longevity. Proc. R. Soc. B Biol. Sci. 205, 531–546 (1979).

    Article  CAS  Google Scholar 

  75. Partridge, L. Evolutionary theories of ageing applied to long-lived organisms. Exp. Gerontol. 36, 641–650 (2001).

    Article  CAS  PubMed  Google Scholar 

  76. Zwaan, B. J. The evolutionary genetics of ageing and longevity. Heredity 82, 589–597 (1999).

    Article  PubMed  Google Scholar 

  77. Chao, L. A model for damage load and its implications for the evolution of bacterial aging. PLOS Genet. 6, e1001076 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Clegg, R. J., Dyson, R. J. & Kreft, J.-U. Repair rather than segregation of damage is the optimal unicellular aging strategy. BMC Biol. 12, 52 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Lin, J., Min, J. & Amir, A. Optimal segregation of proteins: phase transitions and symmetry breaking. Phys. Rev. Lett. 122, 068101 (2019). This study defines the parameter space in which symmetrical or asymmetrical allocation of beneficial or deleterious proteins is most adaptive.

    Article  CAS  PubMed  Google Scholar 

  80. Rang, C. U., Peng, A. Y., Poon, A. F. & Chao, L. Ageing in Escherichia coli requires damage by an extrinsic agent. Microbiology 158, 1553–1559 (2012).

    Article  CAS  PubMed  Google Scholar 

  81. Coelho, M. et al. Fission yeast does not age under favorable conditions, but does so after stress. Curr. Biol. 23, 1844–1852 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Wang, P. et al. Robust growth of Escherichia coli. Curr. Biol. 20, 1099–1103 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Spivey, E. C., Jones, S. K., Rybarski, J. R., Saifuddin, F. A. & Finkelstein, I. J. An aging-independent replicative lifespan in a symmetrically dividing eukaryote. eLife 6, e20340 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Nakaoka, H. & Wakamoto, Y. Aging, mortality, and the fast growth trade-off of Schizosaccharomyces pombe. PLOS Biol. 15, e2001109 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Chao, L., Rang, C. U., Proenca, A. M. & Chao, J. U. Asymmetrical damage partitioning in bacteria: a model for the evolution of stochasticity, determinism, and genetic assimilation. PLOS Comput. Biol. 12, e1004700 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Rang, C. U., Peng, A. Y. & Chao, L. Temporal dynamics of bacterial aging and rejuvenation. Curr. Biol. 21, 1813–1816 (2011).

    Article  CAS  PubMed  Google Scholar 

  87. Kirkwood, T. B. Understanding ageing from an evolutionary perspective. J. Intern. Med. 263, 117–127 (2008).

    Article  CAS  PubMed  Google Scholar 

  88. Lee, A. J. & Wallace, S. S. Hide and seek: how do DNA glycosylases locate oxidatively damaged DNA bases amidst a sea of undamaged bases? Free. Radic. Biol. Med. 107, 170–178 (2017).

    Article  CAS  PubMed  Google Scholar 

  89. Shuman, S. & Glickman, M. S. Bacterial DNA repair by non-homologous end joining. Nat. Rev. Microbiol. 5, 852–861 (2007).

    Article  CAS  PubMed  Google Scholar 

  90. Lieber, M. R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181–211 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Richarme, G. et al. Guanine glycation repair by DJ-1/Park7 and its bacterial homologs. Science 357, 208–211 (2017).

    Article  CAS  PubMed  Google Scholar 

  92. Foti, J. J., Devadoss, B., Winkler, J. A., Collins, J. J. & Walker, G. C. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336, 315–319 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Mattoo, R. U. H. & Goloubinoff, P. Molecular chaperones are nanomachines that catalytically unfold misfolded and alternatively folded proteins. Cell. Mol. Life Sci. 71, 3311–3325 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Veinger, L., Diamant, S., Buchner, J. & Goloubinoff, P. The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273, 11032–11037 (1998).

    Article  CAS  PubMed  Google Scholar 

  95. Priya, S. et al. GroEL and CCT are catalytic unfoldases mediating out-of-cage polypeptide refolding without ATP. Proc. Natl Acad. Sci. USA 110, 7199–7204 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Sharma, S. K., De Los Rios, P., Christen, P., Lustig, A. & Goloubinoff, P. The kinetic parameters and energy cost of the Hsp70 chaperone as a polypeptide unfoldase. Nat. Chem. Biol. 6, 914–920 (2010).

    Article  CAS  PubMed  Google Scholar 

  97. Fernández-Higuero, J. A., Aguado, A., Perales-Calvo, J., Moro, F. & Muga, A. Activation of the DnaK–ClpB complex is regulated by the properties of the bound substrate. Sci. Rep. 8, 5796 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Doyle, S. M. et al. Interplay between E. coli DnaK, ClpB and GrpE during protein disaggregation. J. Mol. Biol. 427, 312–327 (2015).

    Article  CAS  PubMed  Google Scholar 

  99. Seyffer, F. et al. Hsp70 proteins bind Hsp100 regulatory M domains to activate AAA+ disaggregase at aggregate surfaces. Nat. Struct. Mol. Biol. 19, 1347–1355 (2012).

    Article  CAS  PubMed  Google Scholar 

  100. Diamant, S., Ben-Zvi, A. P., Bukau, B. & Goloubinoff, P. Size-dependent disaggregation of stable protein aggregates by the DnaK chaperone machinery. J. Biol. Chem. 275, 21107–21113 (2000).

    Article  CAS  PubMed  Google Scholar 

  101. Goloubinoff, P., Mogk, A., Zvi, A. P. B., Tomoyasu, T. & Bukau, B. Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl Acad. Sci. USA 96, 13732–13737 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119–130 (2011).

    Article  CAS  PubMed  Google Scholar 

  103. Bradley, J. A., Amend, J. P. & LaRowe, D. E. Survival of the fewest: microbial dormancy and maintenance in marine sediments through deep time. Geobiology 17, 43–59 (2019).

    Article  PubMed  Google Scholar 

  104. LaRowe, D. E. & Amend, J. P. Power limits for microbial life. Front. Microbiol. 6, 718 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  105. Milo, R. & Phillips, R. Cell Biology by the Numbers (Garland Science, 2016).

  106. Rang, C. U., Proenca, A., Buetz, C., Shi, C. & Chao, L. Minicells as a damage disposal mechanism in Escherichia coli. mSphere 3, e00428–18 (2018). This study shows how disposal of damaged protein aggregates through minicell formation can help E. coli to avoid senescence.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Farley, M. M., Hu, B., Margolin, W. & Liu, J. Minicells, back in fashion. J. Bacteriol. 198, 1186–1195 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Winkler, J. et al. Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J. 29, 910–923 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Coquel, A.-S. et al. Localization of protein aggregation in Escherichia coli is governed by diffusion and nucleoid macromolecular crowding effect. PLOS Comput. Biol. 9, e1003038 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Hoffman, H. & Frank, M. E. Time-lapse photomicrography of the formation of a free spherical granule in an Escherichia coli cell end. J. Bacteriol. 86, 1075–1078 (1963).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Jamroskovic, J., Pavlendová, N., Muchová, K., Wilkinson, A. J. & Barák, I. An oscillating Min system in Bacillus subtilis influences asymmetrical septation during sporulation. Microbiol. Read. Engl. 158, 1972–1981 (2012).

    Article  CAS  Google Scholar 

  112. Patrick, J. E. & Kearns, D. B. MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol. Microbiol. 70, 1166–1179 (2008).

    Article  CAS  PubMed  Google Scholar 

  113. Bergmiller, T. et al. Biased partitioning of the multidrug efflux pump AcrAB–TolC underlies long-lived phenotypic heterogeneity. Science 356, 311–315 (2017).

    Article  CAS  PubMed  Google Scholar 

  114. Vedel, S., Nunns, H., Košmrlj, A., Semsey, S. & Trusina, A. Asymmetric damage segregation constitutes an emergent population-level stress response. Cell Syst. 3, 187–198 (2016).

    Article  CAS  PubMed  Google Scholar 

  115. Liu, B. et al. The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140, 257–267 (2010).

    Article  CAS  PubMed  Google Scholar 

  116. Spokoini, R. et al. Confinement to organelle-associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Rep. 2, 738–747 (2012). This study reveals important mechanisms in the active segregation of damage at cell division in the budding yeast S. cerevisiae.

    Article  CAS  PubMed  Google Scholar 

  117. Coelho, M. & Tolić, I. M. Asymmetric damage segregation at cell division via protein aggregate fusion and attachment to organelles. BioEssays 37, 740–747 (2015).

    Article  CAS  PubMed  Google Scholar 

  118. Curtis, P. D. & Brun, Y. V. Getting in the loop: regulation of development in Caulobacter crescentus. Microbiol. Mol. Biol. Rev. 74, 13–41 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Obuchowski, P. L. & Jacobs-Wagner, C. PflI, a protein involved in flagellar positioning in Caulobacter crescentus. J. Bacteriol. 190, 1718–1729 (2008).

    Article  CAS  PubMed  Google Scholar 

  120. Davis, N. J. et al. De- and repolarization mechanism of flagellar morphogenesis during a bacterial cell cycle. Genes Dev. 27, 2049–2062 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Huitema, E., Pritchard, S., Matteson, D., Radhakrishnan, S. K. & Viollier, P. H. Bacterial birth scar proteins mark future flagellum assembly site. Cell 124, 1025–1037 (2006).

    Article  CAS  PubMed  Google Scholar 

  122. Lam, H., Schofield, W. B. & Jacobs-Wagner, C. A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124, 1011–1023 (2006).

    Article  CAS  PubMed  Google Scholar 

  123. Hussain, S. et al. MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis. eLife 7, e32471 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Ursell, T. S. et al. Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization. Proc. Natl Acad. Sci. USA 111, E1025–E1034 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. de Pedro, M. A., Quintela, J. C., Höltje, J. V. & Schwarz, H. Murein segregation in. Escherichia coli. J. Bacteriol. 179, 2823–2834 (1997).

    PubMed  Google Scholar 

  126. Ettema, T. J. G., Lindås, A.-C. & Bernander, R. An actin-based cytoskeleton in archaea. Mol. Microbiol. 80, 1052–1061 (2011).

    Article  CAS  PubMed  Google Scholar 

  127. Rokney, A. et al. E. coli transports aggregated proteins to the poles by a specific and energy-dependent process. J. Mol. Biol. 392, 589–601 (2009).

    Article  CAS  PubMed  Google Scholar 

  128. Govers, S. K., Dutre, P. & Aertsen, A. In vivo disassembly and reassembly of protein aggregates in. Escherichia coli. J. Bacteriol. 196, 2325–2332 (2014).

    PubMed  Google Scholar 

  129. Neeli-Venkata, R. et al. Robustness of the process of nucleoid exclusion of protein aggregates in. Escherichia coli. J. Bacteriol. 198, 898–906 (2016).

    CAS  PubMed  Google Scholar 

  130. Parry, B. R. et al. The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity. Cell 156, 183–194 (2014).

    Article  CAS  PubMed  Google Scholar 

  131. Henderson, K. A., Hughes, A. L. & Gottschling, D. E. Mother–daughter asymmetry of pH underlies aging and rejuvenation in yeast. eLife 3, e03504 (2014). This study elucidates the role of cytosolic pH in S. cerevisiae ageing.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Aufschnaiter, A. & Büttner, S. The vacuolar shapes of ageing: from function to morphology. Biochim. Biophys. Acta Mol. Cell Res. 1866, 957–970 (2019).

    Article  CAS  PubMed  Google Scholar 

  133. Hughes, A. L. & Gottschling, D. E. An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492, 261–265 (2012). This study demonstrates that ageing-associated changes in vacuolar pH causes senescence in S. cerevisiae.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Veatch, J. R., McMurray, M. A., Nelson, Z. W. & Gottschling, D. E. Mitochondrial dysfunction leads to nuclear genome instability via an iron-sulfur cluster defect. Cell 137, 1247–1258 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  135. Scheckhuber, C. Q. et al. Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models. Nat. Cell Biol. 9, 99–105 (2007).

    Article  CAS  PubMed  Google Scholar 

  136. Sinclair, D. A. & Guarente, L. Extrachromosomal rDNA circles—a cause of aging in yeast. Cell 91, 1033–1042 (1997). One of the first studies to specifically identify a type of ageing-associated molecular damage that causes senescence of a cell.

    Article  CAS  PubMed  Google Scholar 

  137. Kaeberlein, M., McVey, M. & Guarente, L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 13, 2570–2580 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Laun, P. et al. Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol. Microbiol. 39, 1166–1173 (2001).

    Article  CAS  PubMed  Google Scholar 

  139. Aguilaniu, H., Gustafsson, L., Rigoulet, M. & Thomas, N. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299, 1751–1753 (2003).

    Article  CAS  PubMed  Google Scholar 

  140. Longo, V. D. & Kennedy, B. K. Sirtuins in aging and age-related disease. Cell 126, 257–268 (2006).

    Article  CAS  PubMed  Google Scholar 

  141. Moore, D. L. & Jessberger, S. Creating age asymmetry: consequences of inheriting damaged goods in mammalian cells. Trends Cell Biol. 27, 82–92 (2017). This paper summarizes recent findings that asymmetrical cell divisions are associated with ageing and senescence in multicellular organisms.

    Article  PubMed  Google Scholar 

  142. Ogrodnik, M. et al. Dynamic JUNQ inclusion bodies are asymmetrically inherited in mammalian cell lines through the asymmetric partitioning of vimentin. Proc. Natl Acad. Sci. USA 111, 8049–8054 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Shoemaker, W. R. & Lennon, J. T. Evolution with a seed bank: the population genetic consequences of microbial dormancy. Evol. Appl. 11, 60–75 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  144. Finkel, S. E. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat. Rev. Microbiol. 4, 113–120 (2006).

    Article  CAS  PubMed  Google Scholar 

  145. Finkel, S. E. & Kolter, R. Evolution of microbial diversity during prolonged starvation. Proc. Natl Acad. Sci. USA 96, 4023–4027 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Kram, K. E. et al. Adaptation of Escherichia coli to long-term serial passage in complex medium: evidence of parallel evolution. mSystems 2, e00192–16 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  147. Zinser, E. R. & Kolter, R. Escherichia coli evolution during stationary phase. Res. Microbiol. 155, 328–336 (2004).

    Article  CAS  PubMed  Google Scholar 

  148. Windels, E. M. et al. Bacterial persistence promotes the evolution of antibiotic resistance by increasing survival and mutation rates. ISME J. 13, 1239–1251 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Kumar, S. & Engelberg-Kulka, H. Quorum sensing peptides mediating interspecies bacterial cell death as a novel class of antimicrobial agents. Curr. Opin. Microbiol. 21, 22–27 (2014).

    Article  CAS  PubMed  Google Scholar 

  150. Chan, W. T., Balsa, D. & Espinosa, M. One cannot rule them all: are bacterial toxins–antitoxins druggable? FEMS Microbiol. Rev. 39, 522–540 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  151. Kumar, S., Kolodkin-Gal, I. & Engelberg-Kulka, H. Novel quorum-sensing peptides mediating interspecies bacterial cell death. mBio 4, e00314–13 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Ayrapetyan, M., Williams, T. & Oliver, J. D. The relationship between the viable but nonculturable state and antibiotic persister cells. J. Bacteriol. 200, e00249–18 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Levin-Reisman, I. et al. Antibiotic tolerance facilitates the evolution of resistance. Science 355, 826–830 (2017).

    Article  CAS  PubMed  Google Scholar 

  154. Yaakov, G., Lerner, D., Bentele, K., Steinberger, J. & Barkai, N. Coupling phenotypic persistence to DNA damage increases genetic diversity in severe stress. Nat. Ecol. Evol. 1, 0016 (2017).

    Article  Google Scholar 

  155. Pu, Y. et al. ATP-dependent dynamic protein aggregation regulates bacterial dormancy depth critical for antibiotic tolerance. Mol. Cell 73, 143–156.e4 (2019).

    Article  CAS  PubMed  Google Scholar 

  156. Fuentealba, L. C., Eivers, E., Geissert, D., Taelman, V. & De Robertis, E. M. Asymmetric mitosis: unequal segregation of proteins destined for degradation. Proc. Natl Acad. Sci. USA 105, 7732–7737 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  157. Rujano, M. A. et al. Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLOS Biol. 4, e417 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Moore, D. L., Pilz, G. A., Arauzo-Bravo, M. J., Barral, Y. & Jessberger, S. A mechanism for the segregation of age in mammalian neural stem cells. Science 349, 1334–1338 (2015). This study demonstrates that asymmetrical allocation of damage can promote the proliferation of stem cells in the brain of a mammal.

    Article  CAS  Google Scholar 

  159. Koleva, K. Z. & Hellweger, F. L. From protein damage to cell aging to population fitness in E. coli: insights from a multi-level agent-based model. Ecol. Model. 301, 62–71 (2015).

    Article  Google Scholar 

  160. England, J. L. Statistical physics of self-replication. J. Chem. Phys. 139, 121923 (2013).

    Article  CAS  PubMed  Google Scholar 

  161. Christner, B. C., Mosley-Thompson, E., Thompson, L. G. & Reeve, J. N. Bacterial recovery from ancient glacial ice. Environ. Microbiol. 5, 433–436 (2003).

    Article  CAS  PubMed  Google Scholar 

  162. Carey, J. R. Insect biodemography. Annu. Rev. Entomol. 46, 79–110 (2001).

    Article  CAS  PubMed  Google Scholar 

  163. Ricklefs, R. E. Life-history connections to rates of aging in terrestrial vertebrates. Proc. Natl Acad. Sci. USA 107, 10314–10319 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  164. Baudisch, A. The pace and shape of ageing. Methods Ecol. Evol. 2, 375–382 (2011).

    Article  Google Scholar 

  165. Jones, O. R. et al. Diversity of ageing across the tree of life. Nature 505, 169–173 (2014).

    Article  CAS  PubMed  Google Scholar 

  166. Yang, Y. et al. Temporal scaling of aging as an adaptive strategy of Escherichia coli. Sci. Adv. 5, eaaw2069 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  167. Jo, M. C., Liu, W., Gu, L., Dang, W. & Qin, L. High-throughput analysis of yeast replicative aging using a microfluidic system. Proc. Natl Acad. Sci. USA 112, 9364–9369 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Bouwhuis, S., Choquet, R., Sheldon, B. C. & Verhulst, S. The forms and fitness cost of senescence: age-specific recapture, survival, reproduction, and reproductive value in a wild bird population. Am. Nat. 179, E15–E27 (2012).

    Article  PubMed  Google Scholar 

  169. Nedelcu, A. M., Driscoll, W. W., Durand, P. M., Herron, M. D. & Rashidi, A. On the paradigm of altruistic suicide in the unicellular world. Evolution 65, 3–20 (2011).

    Article  PubMed  Google Scholar 

  170. Longo, V. D., Mitteldorf, J. & Skulachev, V. P. Programmed and altruistic ageing. Nat. Rev. Genet. 6, 866–872 (2005).

    Article  CAS  PubMed  Google Scholar 

  171. Hamilton, W. D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16 (1964).

    Article  CAS  PubMed  Google Scholar 

  172. West, S. A., Griffin, A. S. & Gardner, A. Social semantics: how useful has group selection been? J. Evol. Biol. 21, 374–385 (2008).

    Article  Google Scholar 

  173. Webb, J. S. et al. Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185, 4585–4592 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Rice, K. C. et al. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl Acad. Sci. USA 104, 8113–8118 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Zetzmann, M. et al. DNase-sensitive and -resistant modes of biofilm formation by Listeria monocytogenes. Front. Microbiol. 6, 1428 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  176. Okshevsky, M. & Meyer, R. L. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit. Rev. Microbiol. 41, 341–352 (2015).

    Article  CAS  PubMed  Google Scholar 

  177. Thomas, V. C., Thurlow, L. R., Boyle, D. & Hancock, L. E. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J. Bacteriol. 190, 5690–5698 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Fabrizio, P. et al. Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J. Cell Biol. 166, 1055–1067 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Herker, E. et al. Chronological aging leads to apoptosis in yeast. J. Cell Biol. 164, 501–507 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Fabrizio, P. & Longo, V. D. Chronological aging-induced apoptosis in yeast. Biochim. Biophys. Acta Mol. Cell Res. 1783, 1280–1285 (2008).

    Article  CAS  Google Scholar 

  181. Bar-Zeev, E., Avishay, I., Bidle, K. D. & Berman-Frank, I. Programmed cell death in the marine cyanobacterium Trichodesmium mediates carbon and nitrogen export. ISME J. 7, 2340–2348 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Aizenman, E., Engelberg-Kulka, H. & Glaser, G. An Escherichia coli chromosomal ‘addiction module’ regulated by guanosine [corrected] 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc. Natl Acad. Sci. USA 93, 6059–6063 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Engelberg-Kulka, H., Hazan, R. & Amitai, S. mazEF: a chromosomal toxin–antitoxin module that triggers programmed cell death in bacteria. J. Cell Sci. 118, 4327–4332 (2005).

    Article  CAS  PubMed  Google Scholar 

  184. Erental, A., Kalderon, Z., Saada, A., Smith, Y. & Engelberg-Kulka, H. Apoptosis-like death, an extreme SOS response in Escherichia coli. mBio 5, e01426–14 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Erental, A., Sharon, I. & Engelberg-Kulka, H. Two programmed cell death systems in Escherichia coli: an apoptotic-like death Is inhibited by the mazEF-mediated death pathway. PLOS Biol. 10, e1001281 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Dwyer, D. J., Camacho, D. M., Kohanski, M. A., Callura, J. M. & Collins, J. J. Antibiotic-induced bacterial cell death exhibits physiological and biochemical hallmarks of apoptosis. Mol. Cell 46, 561–572 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Engelberg-Kulka, H., Amitai, S., Kolodkin-Gal, I. & Hazan, R. Bacterial programmed cell death and multicellular behavior in bacteria. PLOS Genet. 2, e135 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Szathmáry, E. & Smith, J. M. The major evolutionary transitions. Nature 374, 227–232 (1995).

    Article  PubMed  Google Scholar 

  189. de Magalhães, J. P. & Costa, J. A database of vertebrate longevity records and their relation to other life-history traits. J. Evol. Biol. 22, 1770–1774 (2009).

    Article  PubMed  Google Scholar 

  190. Bakshi, S. et al. Nonperturbative imaging of nucleoid morphology in live bacterial cells during an antimicrobial peptide attack. Appl. Environ. Microbiol. 80, 4977–4986 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Lee, K.-C., Webb, R. I. & Fuerst, J. A. The cell cycle of the planctomycete Gemmata obscuriglobus with respect to cell compartmentalization. BMC Cell Biol. 10, 4 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Tocheva, E. I. et al. Peptidoglycan transformations during Bacillus subtilis sporulation. Mol. Microbiol. 88, 673–686 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Brun, Y. V. & Janakiraman R. in Prokaryotic Development. (eds Brun, Y. V. & Shimkets, L. J.) 297–317 (ASM Press, 2000)

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Acknowledgements

The authors acknowledge D. A. Schwartz (Indiana University), N. I. Wisnoski (Indiana University), M. Coelho (Harvard University), A. Amir (Harvard University), J. Lin (Harvard University) and J. Min (Harvard University) for critical feedback on earlier versions of this manuscript along with the National Science Foundation (1442246, J.T.L.) and a US Army Research Office Grant (W911NF-14-1-0411, J.T.L.) for financial support.

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R.Z.M.-R. and J.T.L. conceived and wrote the manuscript.

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Correspondence to Jay T. Lennon.

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Nature Reviews Microbiology thanks A. Amir, together with J. Lin and J. Min, and M. Coelho for their contribution to the peer review of this work.

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Available code and data: https://github.com/LennonLab/MicroLong

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Glossary

Senescence

Decreasing survival and/or reproductive ability of an individual during ageing.

Longevity

The ability of an organism to maintain the homeostatic conditions necessary to remain viable over time.

Life history

The set of adaptive traits, such as size, growth rate, extrinsic mortality rate, age to maturity and age-specific fecundity, that characterize the life course of a typical individual of a particular species.

Replicative ageing

A type of ageing in which age is measured in units of divisions of an individual cell, rather than units of time.

Trade-offs

Physical or genetic constraints that prevent the simultaneous optimization of multiple traits by natural selection.

Damage

Structural modifications to cellular macromolecules that accumulate during ageing.

Extrinsic mortality

Environment-related causes of death that occur independently of organismal vigour or age.

Intrinsic mortality

Ageing-related causes of death, due to accumulation of macromolecular damage, which occur independently of the external environment.

Disposable soma theory

Life history-based theory for the evolution of senescence emphasizing constraints of resource allocation. This theory proposes that senescence evolves because it is adaptive to allocate fewer resources to repair in order to allocate more resources to reproduction.

Asymmetrical reproduction

A reproductive event that results in a distinct mother individual, a distinct offspring individual and a difference in age between them.

Programmed cell death

(PCD) Cell death that is caused by factors encoded in the genome of the organism.

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Moger-Reischer, R.Z., Lennon, J.T. Microbial ageing and longevity. Nat Rev Microbiol 17, 679–690 (2019). https://doi.org/10.1038/s41579-019-0253-y

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