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Microbial seed banks: the ecological and evolutionary implications of dormancy

Key Points

  • 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 consists of individuals that are capable of being resuscitated following environmental change. Seed banks can prolong the persistence of genotypes and populations, and also have important consequences for community- and ecosystem-level processes.

  • A review of the literature demonstrates that dormancy is common and phylogenetically widespread. However, microorganisms have evolved diverse genetic and cellular mechanisms for entering and exiting dormancy.

  • Dormancy may help explain various ecological and evolutionary phenomena in microbial systems, including: patterns of biogeography; outbreaks, blooms and successional dynamics; the maintenance of rare taxa; the inability of microbiologists to culture most microorganisms; and the inherent stability of ecosystem services.

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.

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Figure 1: Examples of microbial dormancy.
Figure 2: Dynamics of microbial dormancy.
Figure 3: Predictions of species diversity and species turnover based on the Theory of Island Biogeography 69.
Figure 4: A dynamic rank abundance curve for a microbial community that is influenced by dormancy.
Figure 5: Microbial dormancy fosters stable community function in a simple two-species community via compensatory dynamics.

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Acknowledgements

We acknowledge K. Bird, K. Locey, M. Larsen, J. Palange and three anonymous reviewers for critical feedback on this manuscript. We thank B. Lehmkuhl for technical assistance, and the National Science Foundation (DEB-0842441 and OCE- 0851113) and the US Department of Agriculture National Institute of Food and Agriculture (2008-35107-04481) for financial support. This is Kellogg Biological Station (KBS) contribution number 1559.

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Glossary

Storage effect

An ecological hypothesis stating that environmental fluctuations drive temporal variations in population growth that produce long-lived individual organisms, thus promoting multispecies coexistence.

Metacommunity

A collection of local communities within a heterogeneous landscape that are connected through the dispersal of potentially interacting species.

Histidine kinase sensor

A transmembrane protein that senses external stimuli and conveys signals that lead to changes in cell function.

Stringent response

The microbial stress response to starvation, leading to the reallocation of resources from growth to survival.

Quorum sensing

A process whereby gene expression in and/or growth of microorganisms are coordinated through the production and interpretation of signalling molecules.

Kin selection

Evolutionary selection that occurs when a non-adaptive strategy of an individual improves the fitness of genetically related individuals.

Succession

An ecological phenomenon characterized by predictable changes in community composition over time owing to variation in the colonization potentials and competitive abilities of species and in their responses to disturbances.

Rare biosphere

A concept describing the observation that a very large proportion of the taxa in microbial communities are extremely uncommon.

The Great Plate Count Anomaly

The name given to the underestimation of microbial abundance and diversity, owing to the inability of microorganisms from environmental samples to form colonies on agar media under laboratory conditions.

Stability

In an ecological context: the extent to which populations, communities and ecosystems respond to natural and anthropogenic variability.

Compensatory dynamics

A process whereby a decrease in the abundance of one species results in the increase in the abundance of another species; this balancing can be due to competition or to differences in environmental optima, and can stabilize the functions of ecological communities.

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Lennon, J., Jones, S. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9, 119–130 (2011). https://doi.org/10.1038/nrmicro2504

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