Microbial seed banks: the ecological and evolutionary implications of dormancy (original) (raw)

References

1. Guppy, M. & Withers, P. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. Camb. Philos. Soc. 74, 1–40 (1999).
   Article CAS PubMed Google Scholar
2. Bradshaw, W. E., Armbruster, P. A. & Holzapfel, C. M. Fitness consequences of hibernal diapause in the pitcher-plant mosquito, Wyeomyia smithii. Ecology 79, 1458–1462 (1998).
   Article Google Scholar
3. van Bodegom, P. Microbial maintenance: a critical review on its quantification. Microb. Ecol. 53, 513–523 (2007).
   Google Scholar
4. Rees, M. Evolutionary ecology of seed dormancy and seed size. Phil. Trans. R. Soc. B 351, 1299–1308 (1996).
   Article Google Scholar
5. Cáceres, C. E. & Tessier, A. J. How long to rest: the ecology of optimal dormancy and environmental constraint. Ecology 84, 1189–1198 (2003).
   Article Google Scholar
6. Soula, B. & Menu, F. Variability in diapause duration in the chestnut weevil: mixed ESS, genetic polymorphism or bet-hedging? Oikos 100, 574–580 (2003).
   Article Google Scholar
7. Kaprelyants, A. S., Gottschal, J. C. & Kell, D. B. Dormancy in non-sporulating bacteria. FEMS Microbiol. Rev. 10, 271–285 (1993).
   Article CAS PubMed Google Scholar
8. Schubert, B. A., Lowenstein, T. K., Timofeeff, M. N. & Paker, M. A. Halophilic Archaea cultured from ancient halite, Death Valley, California. Environ. Microbiol. 12, 440–454 (2010).
   Article CAS PubMed Google Scholar
9. Lamarre, C. et al. Transcriptomic analysis of the exit from dormancy of Aspergillus fumigatus conidia. BMC Genomics 9, 417 (2008).
   Article CAS PubMed PubMed Central Google Scholar
10. Chesson, P. L. & Warner, R. R. Environmental variability promotes coexistence in lottery competitive systems. Am. Nat. 117, 923–943 (1981). The theoretical development of the storage effect and how it can influence biodiversity.
    Article Google Scholar
11. Kalamees, R. & Zobel, M. The role of the seed bank in gap regeneration in a calcareous grassland community. Ecology 83, 1017–1025 (2002).
    Article Google Scholar
12. Cole, J. J. Aquatic microbiology for ecosystem scientists: new and recycled paradigms in ecological microbiology. Ecosystems 2, 215–225 (1999).
    Article Google Scholar
13. Coates, A. R. M. (ed.) Dormancy and Low-Growth States in Microbial Disease. (Cambridge Univ. Press, Cambridge, UK, 2003).
    Book Google Scholar
14. Sussman, A. S. & Douthit, H. A. Dormancy in microbial spores. Ann. Rev. Plant Physiol. 24, 311–352 (1973).
    Article CAS Google Scholar
15. del Giorgio, P. A. & Gasol, J. M. in Microbial Ecology of the Oceans (ed. D. L. Kirchman) 243–298 (Wiley & Sons, 2008). A comprehensive review of the major concepts and techniques used to evaluate single-cell physiologicalstructure.
    Book Google Scholar
16. Stevenson, L. H. A case for bacterial dormancy in aquatic systems. Microb. Ecol. 4, 127–133 (1977). A classic paper proposing the importance of dormancy in natural ecosystems.
    Article CAS PubMed Google Scholar
17. Staley, J. T. & Konopka, A. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39, 321–346 (1985).
    Article CAS PubMed Google Scholar
18. Xu, H. S. et al. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8, 313–323 (1982).
    Article CAS PubMed Google Scholar
19. del Giorgio, P. A. & Scarborough, G. Increase in the proportion of metabolically active bacteria along gradients of enrichment in freshwater and marine plankton: implications for estimates of bacterial growth and production rates. J. Plankton Res. 17, 1905–1924 (1995).
    Article Google Scholar
20. Campbell, B., Yu, L., Straza, T. & Kirchman, D. Temporal changes in bacterial rRNA and rRNA genes in Delaware (USA) coastal waters. Aquat. Microb. Ecol. 57, 123–135 (2009).
    Article Google Scholar
21. Kamke, J., Taylor, M. W. & Schmit, S. Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. ISME J. 4, 498–508 (2010).
    Article CAS PubMed Google Scholar
22. Jones, S. E. & Lennon, J. T. Dormancy contributes to the maintenance of microbial diversity. Proc. Natl Acad. Sci. USA 107, 5881–5886 (2010).
    Article CAS PubMed PubMed Central Google Scholar
23. Logue, J. B. & Lindström, E. S. Species sorting affects bacterioplankton community composition as determined by 16S rDNA and 16S rRNA fingerprints. ISME J. 4, 728–738 (2010).
    Article CAS Google Scholar
24. Asakura, H. et al. Gene expression profile of Vibrio cholerae in the cold stress-induced viable but non-culturable state. Environ. Microbiol. 9, 869–879 (2007).
    Article CAS PubMed Google Scholar
25. Sowell, S. M. et al. Proteomic analysis of stationary phase in the marine bacterium “Candidatus Pelagibacter ubique”. Appl. Environ. Microbiol. 74, 4091–4100 (2008).
    Article CAS PubMed PubMed Central Google Scholar
26. Mascher, T. Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria. FEMS Microbiol. Lett. 264, 133–144 (2006).
    Article CAS PubMed Google Scholar
27. Boon, C., Li, R., Qi, R. & Dick, T. Proteins of Mycobacterium bovis BCG induced in the Wayne dormancy model. J. Bacteriol. 183, 2672–2676 (2001).
    Article CAS PubMed PubMed Central Google Scholar
28. Piggot, P. J. & Hilbert, D. W. Sporulation of Bacillus subtilis. Curr. Opin. Microbiol. 7, 579–586 (2004).
    Article CAS PubMed Google Scholar
29. Aertsen, A. & Michiels, C. W. Stress and how bacteria cope with death and survival. Crit. Rev. Microbiol. 30, 263–273 (2004).
    Article CAS PubMed Google Scholar
30. Garza, A. G., Harris, B. Z., Pollack, J. S. & Singer, M. The asgE locus is required for cell–cell signalling during Myxococcus xanthus development. Mol. Microbiol. 35, 812–824 (2000).
    Article CAS PubMed Google Scholar
31. Braeken, K., Moris, M., Daniels, R., Vanderleyden, J. & Michiels, J. New horizons for (p)ppGpp in bacterial and plant physiology. Trends Microbiol. 14, 45–54 (2006). A thorough review of the mechanisms by which ppGpp and pppGpp influence cell physiology.
    Article CAS PubMed Google Scholar
32. Kussell, E. & Leibler, S. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309, 2075–2078 (2005). A theoretical analysis of the conditions that select for responsive versus spontaneous initiation of dormancy.
    Article CAS PubMed Google Scholar
33. Bigger, J. W. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 2, 497–500 (1944).
    Article Google Scholar
34. Lewis, K. Persister cells, dormancy, and infectious disease. Nature Rev. Microbiol. 5, 48–56 (2007). A review on the biology of persister cells, including the genetic mechanisms regulating this form of dormancy.
    Article CAS Google Scholar
35. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L. & Leibler, S. Bacterial persistence as a phenotypic switch. Science 305, 1622–1625 (2004).
    Article CAS PubMed Google Scholar
36. Avery, S. Microbial cell individuality and the underlying sources of heterogeneity. Nature Rev. Microbiol. 4, 577–587 (2006).
    Article CAS Google Scholar
37. Gardner, A., West, S. A. & Griffin, A. S. Is bacterial persistence a social trait? PLoS ONE 2, e752 (2007).
    Article CAS PubMed PubMed Central Google Scholar
38. Kjelleberg, S., Hermansson, M., Marden, P. & Jones, G. W. The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment. Annu. Rev. Microbiol. 41, 25–49 (1987).
    Article CAS PubMed Google Scholar
39. Fagerbakke, K. M., Heldal, M. & Norland, S. Content of carbon, nitrogen, oxygen, sulfur, and phosphorus in native aquatic and cultured bacteria. Aquat. Microb. Ecol. 10, 15–27 (1996).
    Google Scholar
40. Mulyukin, A. L. et al. Comparative study of the elemental composition of vegetative and resting microbial cells. Microbiology 71, 31–40 (2002).
    Article CAS Google Scholar
41. Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. (Princeton Univ. Press, Princeton, 2002).
    Google Scholar
42. Setlow, P. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annu. Rev. Microbiol. 49, 29–54 (1995).
    Article CAS PubMed Google Scholar
43. Morita, R. Starvation-survival of heterotrophs in the marine environment. Adv. Microb. Ecol. 6, 171–178 (1982).
    Article Google Scholar
44. Price, P. B. & Sowers, T. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Natl Acad. Sci. USA 101, 4631–4636 (2004).
    Article CAS PubMed PubMed Central Google Scholar
45. Johnson, S. S. et al. Ancient bacteria show evidence of DNA repair. Proc. Natl Acad. Sci. USA 104, 14401–14405 (2007). Strong empirical evidence for ancient (∼0.5 million years old) and viable bacteria in permafrost samples.
    Article CAS PubMed PubMed Central Google Scholar
46. Gonzalez-Pastor, J. E., Hobbs, E. C. & Losick, R. Cannibalism by sporulating bacteria. Science 301, 510–513 (2003).
    Article CAS PubMed Google Scholar
47. Rao, S. P. S., Alonso, S., Rand, L., Dick, T. & Pethe, K. The proton motive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 105, 11945–11950 (2008).
    Article CAS PubMed PubMed Central Google Scholar
48. Kadouri, D., Jurevitch, E., Okon, Y. & Castro-Sowinski, S. Ecological and agricultural significance of bacterial polyhdroxyalkanoates. Crit. Rev. Microbiol. 43, 93–100 (2005).
    Google Scholar
49. Oliver, J. D. The viable but nonculturable state in bacteria. J. Microbiol. 43, 93–100 (2005).
    PubMed Google Scholar
50. Cano, R. J. & Borucki, M. K. Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber. Science 268, 1060–1064 (1995).
    Article CAS PubMed Google Scholar
51. Renberg, I. & Nilsson, M. Dormant bacteria in lake sediments as paleoecological indicators. J. Paleolimnol. 7, 127–135 (1992).
    Article Google Scholar
52. Raghlukumar, C. et al. Buried in time: culturable fungi in a deep-sea sediment core from the Chagos Trench, Indian Ocean. Deep Sea Res. Part I Oceanogr. Res. Pap. 51, 1759–1768 (2004).
    Article CAS Google Scholar
53. Vreeland, R. H., Rosenzweig, W. D. & Powers, D. W. Isolation of 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature 407, 897–900 (2000).
    Article CAS PubMed Google Scholar
54. Rothschild, L. J. & Mancinelli, R. L. Life in extreme environments. Nature 409, 1092–1101 (2001).
    Article CAS PubMed Google Scholar
55. Pääbo, S. et al. Genetic analyses from ancient DNA. Annu. Rev. Gen. 38, 645–679 (2004).
    Article CAS Google Scholar
56. Hebsgaard, M. B., Phillips, M. J. & Willerslev, E. Geologically ancient DNA: fact or artefact? Trends Microbiol. 13, 212–220 (2005).
    Article CAS PubMed Google Scholar
57. Dworkin, J. & Shah, I. M. Exit from dormancy in microbial organisms. Nature Rev. Microbiol. 8, 890–896 (2010).
    Article CAS Google Scholar
58. Setlow, P. Spore germination. Curr. Opin. Microbiol. 6, 550–556 (2003).
    Article CAS PubMed Google Scholar
59. Whitesides, M. D. & Oliver, J. D. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. Appl. Environ. Microbiol. 63, 1002–1005 (1997).
    CAS PubMed PubMed Central Google Scholar
60. Bogosian, G. & Bourneuf, E. V. A matter of bacterial life and death. EMBO Rep. 2, 770–774 (2001).
    Article CAS PubMed PubMed Central Google Scholar
61. Servais, P., Agogue, H., Courties, C., Joux, F. & Lebaron, P. Are the actively respiring cells (CTC+) those responsible for bacterial production in aquatic environments? FEMS Microbiol. Ecol. 35, 171–179 (2001).
    Article CAS PubMed Google Scholar
62. Kaprelyants, A. S., Mukamolova, G. V. & Kell, D. B. Estimation of dormant Micrococcus luteus cells by penicillin lysis and by resuscitation in cell-free spent culture medium at high dilution. FEMS Microbiol. Lett. 115, 347–352 (1994).
    Article Google Scholar
63. Mukamolova, G. V., Yanopolskaya, N. D., Kell, D. B. & Kaprelyants, A. S. On resuscitation from the dormant state of Micrococcus luteus. Antonie Van Leeuwenhoek 73, 237–243 (1998).
    Article CAS PubMed Google Scholar
64. Mukamolova, G. V., Kaprelyants, A. S., Young, D. I., Young, M. & Kell, D. B. A bacterial cytokine. Proc. Natl Acad. Sci. USA 95, 8916–8921 (1998). This article describes the isolation of a quorum sensing protein that is responsible for resuscitating dormant bacteria.
    Article CAS PubMed PubMed Central Google Scholar
65. Keep, N. H., Ward, J. M., Cohen-Gonsaud, M. & Henderson, B. Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends Microbiol. 14, 271–276 (2006).
    Article CAS PubMed Google Scholar
66. Ravagnani, A., Finan, C. L. & Young, M. A novel firmicute protein family related to the actinobacterial resuscitation-promoting factors by non-orthologous domain displacement. BMC Genomics 6, 39 (2005).
    Article CAS PubMed PubMed Central Google Scholar
67. Epstein, S. S. Microbial awakenings. Nature 457, 1083 (2009).
    Article CAS PubMed Google Scholar
68. Prosser, J. I. et al. The role of ecological theory in microbial ecology. Nature Rev. Microbiol. 5, 384–392 (2007).
    Article CAS Google Scholar
69. MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography. (Princeton Univ. Press, Princeton, 1967).
    Google Scholar
70. Lomolino, M. V., Riddle, B. R. & Brown, J. H. Biogeography. 3rd edn (Sinauer Associates, Sunderland, Massachusetts, 2006).
    Google Scholar
71. Martiny, J. B. H. et al. Microbial biogeography: putting microorganisms on the map. Nature Rev. Microbiol. 4, 102–112 (2006).
    Article CAS Google Scholar
72. Baas Becking, L. G. M. Geobiologie of Inleiding Tot de Milleukeunde (Van Stockum & Zoon, 1934) (in Dutch).
    Google Scholar
73. Hubert, C. et al. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science 325, 1541–1544 (2009).
    Article CAS PubMed Google Scholar
74. Locey, K. Synthesizing traditional biogeography with microbial ecology: the importance of dormancy. J. Biogeogr. 37, 1835–1841 (2010).
    Google Scholar
75. Horner-Devine, M. C., Lage, M., Hughes, J. B. & Bohannan, B. J. M. A taxa–area relationship for bacteria. Nature 432, 750–753 (2004). This article provides empirical evidence demonstrating that bacterial populations have biogeographical distributions.
    Article CAS PubMed Google Scholar
76. Pernthaler, J. Predation on prokaryotes in the water column and its ecological implications. Nature Rev. Microbiol. 3, 537–546 (2005).
    Article CAS Google Scholar
77. Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nature Rev. Microbiol. 8, 15–25 (2010).
    Article CAS Google Scholar
78. Anderson, D. M. et al. Alexandrium fundyense cyst dynamics in the Gulf of Maine. Deep Sea Res. Part II Top. Stud. Oceanogr. 52, 2522–2542 (2005).
    Article Google Scholar
79. Bazzaz, F. A. Physiological ecology of plant succession. Annu. Rev. Ecol. Syst. 10, 351–371 (1979).
    Article Google Scholar
80. Fierer, N., Nemergut, D., Knight, R. & Craine, J. M. Changes through time: integrating microorganisms into the study of succession. Res. Microbiol. 161, 635–642 (2010).
    Article PubMed Google Scholar
81. Skoglund, J. The role of seed banks in vegetation dynamics and restoration of dry tropical ecosystems. J. Veg. Sci. 3, 357–360 (1992).
    Article Google Scholar
82. Fuhrman, J. A. et al. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc. Natl Acad. Sci. USA 103, 13104–13109 (2006).
    Article CAS PubMed PubMed Central Google Scholar
83. Jones, S. E., Chiu, C. Y., Kratz, T. K., Shade, A. & McMahon, K. D. Typhoons initiate predictable change in aquatic bacterial communities. Limnol. Oceanogr. 53, 1319–1326 (2008).
    Article Google Scholar
84. Breitbart, M. & Rohwer, F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278–284 (2005).
    Article CAS PubMed Google Scholar
85. Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc. Natl Acad. Sci. USA 103, 12115–12120 (2006).
    Article CAS PubMed PubMed Central Google Scholar
86. Galand, P. E., Casamayor, E. O., Kirchman, D. L. & Lovejoy, C. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc. Natl Acad. Sci. USA 106, 22427–22432 (2009).
    Article CAS PubMed PubMed Central Google Scholar
87. Scheckenbach, F., Hausmann, K., Wylezich, C., Weitere, M. & Arndt, H. Large-scale paterns in biodiversity of microbial eukaryotes from the abyssal sea floor. Proc. Natl Acad. Sci. USA 107, 115–120 (2010).
    Article CAS PubMed Google Scholar
88. Lawton, J., Daily, G. & Newton, I. Population dynamic principles (and discussion). Phil. Trans. R. Soc. B 344, 61–68 (1994).
    Article Google Scholar
89. Pedrós-Alió, C. Marine microbial diversity: can it be determined? Trends Microbiol. 14, 257–263 (2006).
    Article CAS PubMed Google Scholar
90. Achtman, M. & Wagner, M. Microbial diversity and the genetic nature of microbial species. Nature Rev. Microbiol. 6, 431–440 (2008).
    Article CAS Google Scholar
91. Zengler, K. Central role of the cell in microbial ecology. Microbiol. Mol. Biol. Rev. 73, 712–729 (2009).
    Article CAS PubMed PubMed Central Google Scholar
92. Schmidt, T. M. & Konopka, A. E. Physiological and ecological adaptations of slow-growing, heterotrophic microbes and consequences for cultivation. Microbiol. Monogr. 10, 101–120 (2009).
    Article Google Scholar
93. Kaeberlein, T., Lewis, K. & Epstein, S. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296, 1127–1129 (2002).
    Article CAS PubMed Google Scholar
94. Stevenson, B. S., Eichorst, S. A., Wertz, J. T., Schmidt, T. M. & Breznak, J. A. New strategies for cultivation and detection of previously uncultured microbes. Appl. Environ. Microbiol. 70, 4748–4755 (2004).
    Article CAS PubMed PubMed Central Google Scholar
95. Bloomfield, S. F., Stewart, G., Dodd, C. E. R., Booth, I. R. & Power, E. G. M. The viable but non-culturable phenomenon explained? Microbiology 144, 1–3 (1998).
    Article CAS PubMed Google Scholar
96. Esteban, G. F. & Finlay, B. J. Cryptic freshwater ciliates in a hypersaline lagoon. Protist 154, 411–418 (2003).
    Article PubMed Google Scholar
97. Bruns, A., Cypionka, H. & Overmann, J. Cyclic AMP and acyl homoserine lactons increase the cultivation efficiency of heterotrophic bacteria from the central Baltic Sea. Appl. Environ. Microbiol. 68, 3978–3987 (2002).
    Article CAS PubMed PubMed Central Google Scholar
98. Bell, T., Newman, J. A., Silverman, B. W., Turner, S. L. & Lilley, A. K. The contribution of species richness and composition to bacterial services. Nature 436, 1157–1160 (2005).
    Article CAS PubMed Google Scholar
99. Ptacnik, R. et al. Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proc. Natl Acad. Sci. USA 105, 5134–5138 (2008).
    Article CAS PubMed PubMed Central Google Scholar
100. Parnell, J. J., Crowl, T. A., Weimer, B. C. & Pfrender, M. E. Biodiversity in microbial communities: system scale patterns and mechanisms. Mol. Ecol. 18, 1455–1462 (2009).
     Article PubMed Google Scholar
101. Wittebolle, L. et al. Initial community evenness favours functionality under selective stress. Nature 458, 623–626 (2009).
     Article CAS PubMed Google Scholar
102. Naeem, S. Species redundancy and ecosystem reliability. Conserv. Biol. 12, 39–45 (1998).
     Article Google Scholar
103. Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl Acad. Sci. USA 96, 1463–1468 (1999).
     Article CAS PubMed PubMed Central Google Scholar
104. Cottingham, K. L., Brown, B. L. & Lennon, J. T. Biodiversity may regulate the temporal variability of ecological systems. Ecol. Lett. 4, 72–85 (2001).
     Article Google Scholar
105. Micheli, F. et al. The dual nature of community variability. Oikos 85, 161–169 (1999).
     Article Google Scholar
106. Allison, S. D. & Martiny, J. B. H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl Acad. Sci. USA 105, 11512–11519 (2008).
     Article CAS PubMed PubMed Central Google Scholar
107. Kalisz, S. & McPeek, M. A. Demography of an age-structred annual: resampled projection matrices, elasticity analyses, and seed bank effects. Ecology 73, 1082–1093 (1992).
     Article Google Scholar
108. Gonzalez, A. & Loreau, M. The causes and consequences of compensatory dynamics in ecological communities. Annu. Rev. Ecol. Evol. Syst. 40, 393–414 (2009).
     Article Google Scholar
109. Gouhier, T. C., Guichard, F. & Gonzalez, A. Synchrony and stability of food webs in metacommunities. Am. Nat. 175, E16–E34 (2010).
     Article PubMed Google Scholar
110. Malik, T. & SMith, H. L. Does dormancy increase fitness of bacterial populations in time-varying environments? Bull. Math. Biol. 70, 1140–1162 (2008).
     Article PubMed Google Scholar
111. Chrzanowski, T. H. & Simek, K. Prey-size selection by freshwater flagellated protozoa. Limnology 35, 1429–1436 (1990).
     Google Scholar
112. Pearl, S., Gabay, C., Kishony, R., Oppenheim, A. & Balaban, N. Q. Nongenetic individuality in the host–phage interaction. PLoS Biol. 6, e120 (2008).
113. Donato, J. J. et al. Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins. Appl. Environ. Microbiol. 76, 4396–4401 (2010).
     Article CAS PubMed PubMed Central Google Scholar
114. Warnecke, F. et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560–565 (2007).
     Article CAS PubMed Google Scholar
115. Martin, H. G. et al. Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities. Nature Biotech. 24, 1263–1269 (2006).
     Article CAS Google Scholar
116. Kana, B. D. & Mizrahi, V. Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling. FEMS Immunol. Med. Microbiol. 58, 39–50 (2010).
     Article CAS PubMed Google Scholar
117. Caswell, H. Phenotypic plasticity in life-history traits: demographic effects and evolutionary consequences. Am. Zool. 23, 35–46 (1983).
     Article Google Scholar
118. Maughan, H. Rates of molecular evolution in bacteria are relatively constant despite spore dormancy. Evolution 61, 280–288 (2007).
     Article CAS PubMed Google Scholar
119. Chevin, L. M., Lande, R. & Mace, G. M. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, e1000357 (2010).
     Article CAS PubMed PubMed Central Google Scholar
120. Thompson, J. N., Nuismer, S. L. & Gomulkiewicz, R. Coevolution and maladaptation. Integr. Comp. Biol. 42, 381–387 (2002).
     Article PubMed Google Scholar
121. Snell-Rood, E. C., Van Dyken, J. D., Cruickshank, T., Wade, M. J. & Moczek, A. P. Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. Bioessays 32, 71–81 (2010).
     Article CAS PubMed PubMed Central Google Scholar
122. Masel, J., King, O. D. & Maughan, H. The loss of adaptive plasticity during long periods of environmental stasis. Am. Nat. 169, 38–46 (2007).
     Article PubMed Google Scholar
123. Stomp, M. et al. The timescale of phenotypic plasticity and its impact on competition in fluctuating environments. Am. Nat. 172, e169–e185 (2008).
     Article Google Scholar
124. Maughan, H., Birky, C. W. Jr & Nicholson, W. L. Transcriptome divergence and the loss of plasticity in Bacillus subtilis after 6,000 generations of evolution under relaxed selection for sporulation. J. Bacteriol. 191, 428–433 (2009).
     Article CAS PubMed Google Scholar
125. Huang, C. T., Yu, F. P., McFeters, G. A. & Stewart, P. S. Nonuniform spatial patterns of respiratory activity within biofilms during disinfection. Appl. Environ. Microbiol. 61, 2252–2256 (1995).
     CAS PubMed PubMed Central Google Scholar
126. Madigan, M. T., Mortinko, J. M., Dunlap, P. V. & Clark, D. P. Brock Biology of Microorganisms 12th edn (Pearson Bejamin-Cummings, San Francisco, 2009).
     Google Scholar
127. Novitsky, J. A. & Morita, R. Y. Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine Vibrio. Appl. Environ. Microbiol. 32, 617–622 (1976).
     CAS PubMed Google Scholar
128. Macdonell, M. T. & Hood, M. A. Isolation and characterization of ultra-microbacteria from a Gulf-Coast estuary. Appl. Environmen. Microbiol. 43, 566–571 (1982).
     CAS Google Scholar
129. Choi, J. W., Sherr, E. B. & Sherr, B. F. Relation between presence absence of a visible nucleoid and metabolic activity in bacterioplankton cells. Limnol. Oceanogr. 41, 1161–1168 (1996).
     Article Google Scholar
130. Lebaron, P., Servais, P., Agogue, H., Courties, C. & Joux, F. Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl. Environ.Microbiol. 67, 1775–1782 (2001).
     Article CAS PubMed PubMed Central Google Scholar
131. Dell'Anno, A., Fabiano, M., Duineveld, G. C. A., Kok, A. & Danovaro, R. Nucleic acid (DNA, RNA) quantification and RNA/DNA ratio determination in marine sediments: comparison of spectrophotometric, fluorometric, and high-performance liquid chromotography methods and estimation of detrital DNA. Appl. Environ. Microbiol. 64, 3238–3245 (1998).
     CAS PubMed PubMed Central Google Scholar
132. Suzina, N. E. et al. Ultrastructure of resting cells of some non-spore-forming bacteria. Microbiology 73, 435–447 (2004).
     Article CAS Google Scholar
133. Kieft, T. L., Wilch, E., O'Connor, K., Ringelberg, D. B. & White, D. C. Survival and phospholipid fatty acid profiles of surface and subsurface bacteria in natural sediment microcosms. Appl. Environ. Microbiol. 63, 1531–1542 (1997).
     CAS PubMed PubMed Central Google Scholar
134. Linder, K. & Oliver, J. D. Membrane fatty-acid and virulence changes in the viable but nonculturable state of Vibrio vulnificus. Appl.Environ. Microbiol. 55, 2837–2842 (1989).
     CAS PubMed PubMed Central Google Scholar
135. Archuleta, R. J., Hoppes, P. Y. & Primm, T. P. Mycobacterium avium enters a state of metabolic dormancy in response to starvation. Tuberculosis 85, 147–158 (2005).
     Article CAS PubMed Google Scholar
136. Roslev, P. & King, G. M. Aerobic and anaerobic starvation metabolism in methanotrophic bacteria. Appl. Environ. Microbiol. 61, 1563–1570 (1995).
     CAS PubMed PubMed Central Google Scholar
137. Chaiyanan, S., Grim, C., Maugel, T., Huq, A. & Colwell, R. R. Ultrastructure of coccoid viable but non-culturable Vibrio cholerae. Environ. Microbiol. 9, 393–402 (2007).
     Article PubMed Google Scholar
138. Wang, J. G. & Bakken, L. R. Screening of soil bacteria for poly-β-hydroxybutyric acid production and its role in the survival of starvation. Microb. Ecol. 35, 94–101 (1998).
     Article CAS PubMed Google Scholar
139. Wiebe, W. J. & Bancroft, K. Use of adenylate energy charge ratio to measure growth state of natural microbial communities. Proc. Natl Acad. Sci. USA 72, 2112–2115 (1975).
     Article CAS PubMed PubMed Central Google Scholar

Download references