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Stress and stability: applying the Anna Karenina principle to animal microbiomes

Nature Microbiology volume 2, Article number: 17121 (2017) Cite this article

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Abstract

All animals studied to date are associated with symbiotic communities of microorganisms. These animal microbiotas often play important roles in normal physiological function and susceptibility to disease; predicting their responses to perturbation represents an essential challenge for microbiology. Most studies of microbiome dynamics test for patterns in which perturbation shifts animal microbiomes from a healthy to a dysbiotic stable state. Here, we consider a complementary alternative: that the microbiological changes induced by many perturbations are stochastic, and therefore lead to transitions from stable to unstable community states. The result is an ‘Anna Karenina principle’ for animal microbiomes, in which dysbiotic individuals vary more in microbial community composition than healthy individuals—paralleling Leo Tolstoy's dictum that “all happy families look alike; each unhappy family is unhappy in its own way”. We argue that Anna Karenina effects are a common and important response of animal microbiomes to stressors that reduce the ability of the host or its microbiome to regulate community composition. Patterns consistent with Anna Karenina effects have been found in systems ranging from the surface of threatened corals exposed to above-average temperatures, to the lungs of patients suffering from HIV/AIDs. However, despite their apparent ubiquity, these patterns are easily missed or discarded by some common workflows, and therefore probably underreported. Now that a substantial body of research has established the existence of these patterns in diverse systems, rigorous testing, intensive time-series datasets and improved stochastic modelling will help to explore their importance for topics ranging from personalized medicine to theories of the evolution of host–microorganism symbioses.

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Figure 1: Anna Karenina principle of perturbations inducing microbiome destabilization.
Figure 2: Stochasticity produces contrasting effects of mild and severe perturbations under different models of microbiome dynamics.

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Acknowledgements

The authors would like to thank D. Burkepile, J. Gilbert, D. McDonald, T. Sharpton, C. Armour, J. Jensen, C. Chang and many other colleagues for useful discussions. This work was supported by a National Science Foundation Dimensions of Biodiversity grant (no. 1442306).

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  1. Department of Biological Sciences, School of Science, Technology, Education, and Mathematics, University of Washington, UWBB 249, Bothell, 98011-8246, Washington, USA

    Jesse R. Zaneveld

  2. Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, 97331, Oregon, USA

    Ryan McMinds & Rebecca Vega Thurber

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J.R.Z. wrote the manuscript. All authors conducted research, contributed intellectually, and edited the manuscript.

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Correspondence to Jesse R. Zaneveld or Rebecca Vega Thurber.

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Zaneveld, J., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol 2, 17121 (2017). https://doi.org/10.1038/nmicrobiol.2017.121

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