The “Anna Karenina principle” of unhappy microbiomes

Corvallis, Ore.—The bacterial communities that live inside everyone are quite similar and stable when times are good, but when stress enters the equation, those communities can react very differently from person to person.

A microbiological version of the “Anna Karenina principle,” it’s a new paradigm suggested by scientists at Oregon State University—one that has key implications for a more personalized approach to antibiotic therapy, management of chronic diseases and other aspects of medical care. Microbiology Associate Professor Rebecca Vega Thurber and doctoral student Ryan McMinds contributed to the study published today in Nature Microbiology. 

The principle gets its name from the opening line of the novel Anna Karenina by 19th century Russian author Leo Tolstoy: “All happy families are alike; each unhappy family is unhappy in its own way.”

It turns out that this observation also applies to perturbed microbiotas of humans and animals.

“When microbiologists have looked at how microbiomes change when their hosts are stressed from any number of factors – temperature, smoking, diabetes, for example – they’ve tended to assume directional and predictive changes in the community,” said  Vega Thurber, corresponding author on the perspective study funded by the National Science Foundation. “After tracking many datasets of our own we never seemed to find this pattern but rather a distinct one where microbiomes actually change in a stochastic, or random, way.”

Lead author Jesse Zaneveld of the University of Washington-Bothell collaborated with Vega Thurber and her student, McMinds, to survey the literature on microbial changes caused by perturbation. Together they found those stochastic changes to be a common occurrence, but one that researchers have tended to discard as “noise” rather than report.

“Thus we present the Anna Karenina principle for microbiomes,” Vega Thurber said. “When microbiomes are happy they are all similar in their composition but during stress or unhappiness they change in a multitude of distinct ways. This piece draws together diverse microbiome research. We think this is an important emerging paradigm for thinking about microbiome data. We present ways of identifying it and distinguishing it from other patterns.”

In addition to the literary reference, Vega Thurber offers a wintry metaphor to explain what she and her collaborators have discovered.

“When healthy our microbiomes look alike, but when stressed each one of us has our own microbial snowflake,” she said. “You or I could be put under the same stress, and our microbiomes will respond in different ways – that’s a very important facet to consider for managing approaches to personalized medicine. Stressors like antibiotics or diabetes can cause different people’s microbiomes to react in very different ways.”

Humans and animals are filled with symbiotic communities of microorganisms that often fill key roles in normal physiological function and also influence susceptibility to disease. Predicting how these communities of organisms respond to perturbations – anything that alters the systems’ function – is one of microbiologists’ essential challenges.

Header image: Samples were taken of the microbiome of corals as part of a three year experiment.

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