Home LiteratureArticle Details
PMID: 21233850 Published · ppublish English Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Review

Microbial seed banks: the ecological and evolutionary implications of dormancy.

Nature reviews. Microbiology ·Vol. 9 ·No. 2 ·2011-00-00 ·Pages 119-30

Lennon JT, Jones SE

Abstract

Dormancy is a bet-hedging strategy used by a wide range of taxa, including microorganisms. It refers to an organism's ability to enter a reversible state of low metabolic activity when faced with unfavourable environmental conditions. Dormant microorganisms generate a seed bank, which comprises individuals that are capable of being resuscitated following environmental change. In this Review, we highlight mechanisms that have evolved in microorganisms to allow them to successfully enter and exit a dormant state, and discuss the implications of microbial seed banks for evolutionary dynamics, population persistence, maintenance of biodiversity, and the stability of ecosystem processes.

MeSH Terms
Bacterial Physiological Phenomena Biodiversity Biological Evolution Ecosystem Environment Phenotype
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lennon Jay T
W.K. Kellogg Biological Station, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, Michigan 49060, USA. [email protected]
Jones Stuart E
References (100)
100 references, click to expand
  1. The asgE locus is required for cell-cell signalling during Myxococcus xanthus development.
    Mol Microbiol. 2000 Feb;35(4):812-24 PMID: 10692158
  2. Proteomic analysis of stationary phase in the marine bacterium "Candidatus Pelagibacter ubique".
    Appl Environ Microbiol. 2008 Jul;74(13):4091-100 PMID: 18469119
  3. 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. 2001 Apr;67(4):1775-82 PMID: 11282632
  4. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory.
    PLoS Biol. 2010 Apr 27;8(4):e1000357 PMID: 20463950
  5. Microbial maintenance: a critical review on its quantification.
    Microb Ecol. 2007 May;53(4):513-23 PMID: 17333428
  6. Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling.
    FEMS Immunol Med Microbiol. 2010 Feb;58(1):39-50 PMID: 19799629
  7. Changes through time: integrating microorganisms into the study of succession.
    Res Microbiol. 2010 Oct;161(8):635-42 PMID: 20599610
  8. Nucleic acid (DNA, RNA) quantification and RNA/DNA ratio determination in marine sediments: comparison of spectrophotometric, fluorometric, and HighPerformance liquid chromatography methods and estimation of detrital DNA
    Appl Environ Microbiol. 1998 Sep;64(9):3238-45 PMID: 9726866
  9. Aerobic and anaerobic starvation metabolism in methanotrophic bacteria.
    Appl Environ Microbiol. 1995 Apr;61(4):1563-70 PMID: 16535004
  10. Transcriptomic analysis of the exit from dormancy of Aspergillus fumigatus conidia.
    BMC Genomics. 2008 Sep 16;9:417 PMID: 18796135
  11. Genetic analyses from ancient DNA.
    Annu Rev Genet. 2004;38:645-79 PMID: 15568989
  12. A case for bacterial dormancy in aquatic systems.
    Microb Ecol. 1977 Jun;4(2):127-33 PMID: 24231971
  13. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed.
    Science. 2009 Sep 18;325(5947):1541-4 PMID: 19762643
  14. Colloquium paper: resistance, resilience, and redundancy in microbial communities.
    Proc Natl Acad Sci U S A. 2008 Aug 12;105 Suppl 1:11512-9 PMID: 18695234
  15. Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins.
    Appl Environ Microbiol. 2010 Jul;76(13):4396-401 PMID: 20453147
  16. Bacterial persistence as a phenotypic switch.
    Science. 2004 Sep 10;305(5690):1622-5 PMID: 15308767
  17. Central role of the cell in microbial ecology.
    Microbiol Mol Biol Rev. 2009 Dec;73(4):712-29 PMID: 19946138
  18. Life in extreme environments.
    Nature. 2001 Feb 22;409(6823):1092-101 PMID: 11234023
  19. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats.
    Annu Rev Microbiol. 1985;39:321-46 PMID: 3904603
  20. Persister cells, dormancy and infectious disease.
    Nat Rev Microbiol. 2007 Jan;5(1):48-56 PMID: 17143318
  21. Annually reoccurring bacterial communities are predictable from ocean conditions.
    Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):13104-9 PMID: 16938845
  22. [Ultrastructure of resting cells of some non-spore-forming bacteria].
    Mikrobiologiia. 2004 Jul-Aug;73(4):516-29 PMID: 15521179
  23. Diversity predicts stability and resource use efficiency in natural phytoplankton communities.
    Proc Natl Acad Sci U S A. 2008 Apr 1;105(13):5134-8 PMID: 18375765
  24. Sporulation of Bacillus subtilis.
    Curr Opin Microbiol. 2004 Dec;7(6):579-86 PMID: 15556029
  25. Initial community evenness favours functionality under selective stress.
    Nature. 2009 Apr 2;458(7238):623-6 PMID: 19270679
  26. Nonuniform spatial patterns of respiratory activity within biofilms during disinfection.
    Appl Environ Microbiol. 1995 Jun;61(6):2252-6 PMID: 7793945
  27. Isolation and characterization of ultramicrobacteria from a gulf coast estuary.
    Appl Environ Microbiol. 1982 Mar;43(3):566-71 PMID: 16345964
  28. Microbial cell individuality and the underlying sources of heterogeneity.
    Nat Rev Microbiol. 2006 Aug;4(8):577-87 PMID: 16845428
  29. Exit from dormancy in microbial organisms.
    Nat Rev Microbiol. 2010 Dec;8(12):890-6 PMID: 20972452
  30. Isolating "uncultivable" microorganisms in pure culture in a simulated natural environment.
    Science. 2002 May 10;296(5570):1127-9 PMID: 12004133
  31. The timescale of phenotypic plasticity and its impact on competition in fluctuating environments.
    Am Nat. 2008 Nov;172(5):169-85 PMID: 18828745
  32. On resuscitation from the dormant state of Micrococcus luteus.
    Antonie Van Leeuwenhoek. 1998 Apr;73(3):237-43 PMID: 9801768
  33. Stress and how bacteria cope with death and survival.
    Crit Rev Microbiol. 2004;30(4):263-73 PMID: 15646400
  34. Ecology of the rare microbial biosphere of the Arctic Ocean.
    Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22427-32 PMID: 20018741
  35. Survival and viability of nonculturableEscherichia coli andVibrio cholerae in the estuarine and marine environment.
    Microb Ecol. 1982 Dec;8(4):313-23 PMID: 24226049
  36. Screening of Soil Bacteria for Poly-beta-Hydroxybutyric Acid Production and Its Role in the Survival of Starvation
    Microb Ecol. 1998 Jan;35(1):94-101 PMID: 9459662
  37. Intramembrane-sensing histidine kinases: a new family of cell envelope stress sensors in Firmicutes bacteria.
    FEMS Microbiol Lett. 2006 Nov;264(2):133-44 PMID: 17064367
  38. Bacterial competition: surviving and thriving in the microbial jungle.
    Nat Rev Microbiol. 2010 Jan;8(1):15-25 PMID: 19946288
  39. Microbial diversity in the deep sea and the underexplored "rare biosphere".
    Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):12115-20 PMID: 16880384
  40. Wake up! Peptidoglycan lysis and bacterial non-growth states.
    Trends Microbiol. 2006 Jun;14(6):271-6 PMID: 16675219
  41. Microbial biogeography: putting microorganisms on the map.
    Nat Rev Microbiol. 2006 Feb;4(2):102-12 PMID: 16415926
  42. Proteins of Mycobacterium bovis BCG induced in the Wayne dormancy model.
    J Bacteriol. 2001 Apr;183(8):2672-6 PMID: 11274129
  43. The contribution of species richness and composition to bacterial services.
    Nature. 2005 Aug 25;436(7054):1157-60 PMID: 16121181
  44. Resuscitation of Vibrio vulnificus from the Viable but Nonculturable State.
    Appl Environ Microbiol. 1997 Mar;63(3):1002-5 PMID: 16535534
  45. Does dormancy increase fitness of bacterial populations in time-varying environments?
    Bull Math Biol. 2008 May;70(4):1140-62 PMID: 18239978
  46. New strategies for cultivation and detection of previously uncultured microbes.
    Appl Environ Microbiol. 2004 Aug;70(8):4748-55 PMID: 15294811
  47. Gene expression profile of Vibrio cholerae in the cold stress-induced viable but non-culturable state.
    Environ Microbiol. 2007 Apr;9(4):869-79 PMID: 17359259
  48. Spore germination.
    Curr Opin Microbiol. 2003 Dec;6(6):550-6 PMID: 14662349
  49. Cannibalism by sporulating bacteria.
    Science. 2003 Jul 25;301(5632):510-3 PMID: 12817086
  50. The viable but non-culturable phenomenon explained?
    Microbiology (Reading). 1998 Jan;144 ( Pt 1):1-3 PMID: 9467894
  51. Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons.
    ISME J. 2010 Apr;4(4):498-508 PMID: 20054355
  52. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite.
    Nature. 2007 Nov 22;450(7169):560-5 PMID: 18033299
  53. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis.
    Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1463-8 PMID: 9990046
  54. Transcriptome divergence and the loss of plasticity in Bacillus subtilis after 6,000 generations of evolution under relaxed selection for sporulation.
    J Bacteriol. 2009 Jan;191(1):428-33 PMID: 18952793
  55. Marine microbial diversity: can it be determined?
    Trends Microbiol. 2006 Jun;14(6):257-63 PMID: 16679014
  56. The viable but nonculturable state in bacteria.
    J Microbiol. 2005 Feb;43 Spec No:93-100 PMID: 15765062
  57. The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 2008 Aug 19;105(33):11945-50 PMID: 18697942
  58. Halophilic Archaea cultured from ancient halite, Death Valley, California.
    Environ Microbiol. 2010 Feb;12(2):440-54 PMID: 19840101
  59. Ecological and agricultural significance of bacterial polyhydroxyalkanoates.
    Crit Rev Microbiol. 2005;31(2):55-67 PMID: 15986831
  60. Biodiversity in microbial communities: system scale patterns and mechanisms.
    Mol Ecol. 2009 Apr;18(7):1455-62 PMID: 19298265
  61. Nongenetic individuality in the host-phage interaction.
    PLoS Biol. 2008 May 20;6(5):e120 PMID: 18494559
  62. Metabolic depression in animals: physiological perspectives and biochemical generalizations.
    Biol Rev Camb Philos Soc. 1999 Feb;74(1):1-40 PMID: 10396183
  63. Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal.
    Nature. 2000 Oct 19;407(6806):897-900 PMID: 11057666
  64. A taxa-area relationship for bacteria.
    Nature. 2004 Dec 9;432(7018):750-3 PMID: 15592412
  65. Cryptic freshwater ciliates in a hypersaline lagoon.
    Protist. 2003 Oct;154(3-4):411-8 PMID: 14658497
  66. Is bacterial persistence a social trait?
    PLoS One. 2007 Aug 15;2(8):e752 PMID: 17710151
  67. Microbial diversity and the genetic nature of microbial species.
    Nat Rev Microbiol. 2008 Jun;6(6):431-40 PMID: 18461076
  68. Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio.
    Appl Environ Microbiol. 1976 Oct;32(4):617-22 PMID: 984833
  69. Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber.
    Science. 1995 May 19;268(5213):1060-4 PMID: 7538699
  70. Are the actively respiring cells (CTC+) those responsible for bacterial production in aquatic environments?
    FEMS Microbiol Ecol. 2001 Apr;35(2):171-179 PMID: 11295456
  71. Predation on prokaryotes in the water column and its ecological implications.
    Nat Rev Microbiol. 2005 Jul;3(7):537-46 PMID: 15953930
  72. Dormancy in non-sporulating bacteria.
    FEMS Microbiol Rev. 1993 Apr;10(3-4):271-85 PMID: 8318260
  73. New horizons for (p)ppGpp in bacterial and plant physiology.
    Trends Microbiol. 2006 Jan;14(1):45-54 PMID: 16343907
  74. A novel firmicute protein family related to the actinobacterial resuscitation-promoting factors by non-orthologous domain displacement.
    BMC Genomics. 2005 Mar 17;6:39 PMID: 15774001
  75. Mycobacterium avium enters a state of metabolic dormancy in response to starvation.
    Tuberculosis (Edinb). 2005 May;85(3):147-58 PMID: 15850753
  76. Microbial awakenings.
    Nature. 2009 Feb 26;457(7233):1083 PMID: 19242455
  77. Species sorting affects bacterioplankton community composition as determined by 16S rDNA and 16S rRNA fingerprints.
    ISME J. 2010 Jun;4(6):729-38 PMID: 20130658
  78. The role of ecological theory in microbial ecology.
    Nat Rev Microbiol. 2007 May;5(5):384-92 PMID: 17435792
  79. Ultrastructure of coccoid viable but non-culturable Vibrio cholerae.
    Environ Microbiol. 2007 Feb;9(2):393-402 PMID: 17222137
  80. Survival and phospholipid Fatty Acid profiles of surface and subsurface bacteria in natural sediment microcosms.
    Appl Environ Microbiol. 1997 Apr;63(4):1531-42 PMID: 16535578
  81. Mechanisms for the prevention of damage to DNA in spores of Bacillus species.
    Annu Rev Microbiol. 1995;49:29-54 PMID: 8561462
  82. Geologically ancient DNA: fact or artefact?
    Trends Microbiol. 2005 May;13(5):212-20 PMID: 15866038
  83. Ancient bacteria show evidence of DNA repair.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14401-5 PMID: 17728401
  84. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival.
    Proc Natl Acad Sci U S A. 2004 Mar 30;101(13):4631-6 PMID: 15070769
  85. Coevolution and maladaptation.
    Integr Comp Biol. 2002 Apr;42(2):381-7 PMID: 21708731
  86. Synchrony and stability of food webs in metacommunities.
    Am Nat. 2010 Feb;175(2):E16-34 PMID: 20059366
  87. Phenotypic diversity, population growth, and information in fluctuating environments.
    Science. 2005 Sep 23;309(5743):2075-8 PMID: 16123265
  88. Use of the adenylate energy charge ratio to measure growth state of natural microbial communities.
    Proc Natl Acad Sci U S A. 1975 Jun;72(6):2112-5 PMID: 806077
  89. A matter of bacterial life and death.
    EMBO Rep. 2001 Sep;2(9):770-4 PMID: 11559589
  90. A bacterial cytokine.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8916-21 PMID: 9671779
  91. Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities.
    Nat Biotechnol. 2006 Oct;24(10):1263-9 PMID: 16998472
  92. Rates of molecular evolution in bacteria are relatively constant despite spore dormancy.
    Evolution. 2007 Feb;61(2):280-8 PMID: 17348939
  93. Cyclic AMP and acyl homoserine lactones increase the cultivation efficiency of heterotrophic bacteria from the central Baltic Sea.
    Appl Environ Microbiol. 2002 Aug;68(8):3978-87 PMID: 12147499
  94. Large-scale patterns in biodiversity of microbial eukaryotes from the abyssal sea floor.
    Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):115-20 PMID: 20007768
  95. Membrane fatty acid and virulence changes in the viable but nonculturable state of Vibrio vulnificus.
    Appl Environ Microbiol. 1989 Nov;55(11):2837-42 PMID: 2696428
  96. The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment.
    Annu Rev Microbiol. 1987;41:25-49 PMID: 3318670
  97. Dormancy contributes to the maintenance of microbial diversity.
    Proc Natl Acad Sci U S A. 2010 Mar 30;107(13):5881-6 PMID: 20231463
  98. Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity.
    Bioessays. 2010 Jan;32(1):71-81 PMID: 20020499
  99. Here a virus, there a virus, everywhere the same virus?
    Trends Microbiol. 2005 Jun;13(6):278-84 PMID: 15936660
  100. The loss of adaptive plasticity during long periods of environmental stasis.
    Am Nat. 2007 Jan;169(1):38-46 PMID: 17206583
Article Info
Journal
Nature reviews. Microbiology
Abbr.
Nat Rev Microbiol
ISSN
1740-1534
DOI
10.1038/nrmicro2504
Email
[email protected]
Published
2011-00-00
Pages
119-30
Language
English
Region
England
NLM ID
101190261
Subset
IM
External Links
PubMed source DOI: 10.1038/nrmicro2504 View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2