Cited by 333Gut microbiota and healthAnimal Behavior and ReproductionInsect symbiosis and bacterial influences

Why does the microbiome affect behaviour?

Johnson, Katerina V.-A., Foster, Kevin R.·2018·Nature Reviews Microbiology

Abstract

Growing evidence indicates that the mammalian microbiome can affect behaviour, and several symbionts even produce neurotransmitters. One common explanation for these observations is that symbionts have evolved to manipulate host behaviour for their benefit. Here, we evaluate the manipulation hypothesis by applying evolutionary theory to recent work on the gut-brain axis. Although the theory predicts manipulation by symbionts under certain conditions, these appear rarely satisfied by the genetically diverse communities of the mammalian microbiome. Specifically, any symbiont investing its resources to manipulate host behaviour is expected to be outcompeted within the microbiome by strains that do not manipulate and redirect their resources into growth and survival. Moreover, current data provide no clear evidence for manipulation. Instead, we show how behavioural effects can readily arise as a by-product of natural selection on microorganisms to grow within the host and natural selection on hosts to depend upon their symbionts. We argue that understanding why the microbiome influences behaviour requires a focus on microbial ecology and local effects within the host.

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  • Different microbes of the gut microbiota secrete different neurotransmitters: Bacillus species secrete mainly acetylcholine, dopamine, and norepinephrine, while Escherichia secrete serotonin.

    “Johnson and Foster (60) found that the different microbes of the gut microbiota secrete different neurotransmitters: e.g., Bacillus species secrete mainly acetylcholine, dopamine, and norepinephrine, while Escherichia secrete serotonin.”
  • It has been proposed that gut bacteria can influence neurobehavior including host appetite for food.

    “It has been proposed that gut bacteria can influence neurobehavior including host appetite for food (135, 137, 182), so it is not implausible to predict associations between microbiota and all substances passing through the gut.”

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  1. [15]15. receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. USA 108 , 16050-16055 385 (2011). 386 387 388 389
  2. [22]22. gondii . Proc. R. Soc. Lond. B Biol. Sci. 267 433 434 435 436 - , 1591-1594 (2000).
  3. [86]86. Strandwitz, P. et al. GABA modulating bacteria of the human gut microbiome at ASM Microbe Conference (American Society for Microbiology, 2016).
  4. [88]88. Wall, R. et al . in Microbial Endocrinology: The Microbiota-Gut-Brain Axis in Health and Disease (eds Lyte, M. & Cryan, J. F.) 221-239 (Springer, New York, 2014).
  5. [90]90. Roshchina, V. V. in Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health (eds Lyte, M. & Freestone, P. P. E.) 17-52 (Springer, New York, 2010).

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Authors
Johnson, K. V.-A., & Foster, K. R.
Affiliations
University of Oxford (GB)
Corresponding author
  • Johnson, Katerina V.-A.
  • Foster, Kevin R.
Venue
Nature Reviews Microbiology
Published
2018-04-24
Volume
16
Issue
10
Pages
647-655
ISSN
  • 1740-1526 (ISSN-L)
  • 1740-1534
OpenAlex
W2801800085
Cited by
333
References
136
Citations by year
2026: 25 · 2025: 39 · 2024: 39 · 2023: 34 · 2022: 45 · 2021: 55 · 2020: 56 · 2019: 32 · 2018: 7
FWCI
3.66
Type
journal article
Language
en
Open access
closed
Locations
  • Nature Reviews Microbiology (publishedVersion)
  • PubMed (publishedVersion)
Funders
Biotechnology and Biological Sciences Research Council (1467154)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
Keywords
gut microbiota, host behavior, gut-brain axis, microbial evolution, host-microbe coevolution, microbial competition, host dependence, neurotransmitters, microbial ecology, natural selection
MeSH terms
Gastrointestinal Microbiome, Animals, Behavior, Animal, Communicable Diseases, Biological Evolution, Humans, Mammals, Selection, Genetic, Microbiota

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