Cited by 616Gut microbiota and healthEvolutionary Game Theory and CooperationBacterial biofilms and quorum sensing

The evolution of cooperation within the gut microbiota

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Rakoff-Nahoum, Seth, Foster, Kevin R., Comstock, Laurie E.·2016·Nature

Abstract

Cooperative phenotypes are considered central to the functioning of microbial communities in many contexts, including communication via quorum sensing, biofilm formation, antibiotic resistance, and pathogenesis. The human intestine houses a dense and diverse microbial community critical to health, yet we know little about cooperation within this important ecosystem. Here we test experimentally for evolved cooperation within the Bacteroidales, the dominant Gram-negative bacteria of the human intestine. We show that during growth on certain dietary polysaccharides, the model member Bacteroides thetaiotaomicron exhibits only limited cooperation. Although this organism digests these polysaccharides extracellularly, mutants lacking this ability are outcompeted. In contrast, we discovered a dedicated cross-feeding enzyme system in the prominent gut symbiont Bacteroides ovatus, which digests polysaccharide at a cost to itself but at a benefit to another species. Using in vitro systems and gnotobiotic mouse colonization models, we find that extracellular digestion of inulin increases the fitness of B. ovatus owing to reciprocal benefits when it feeds other gut species such as Bacteroides vulgatus. This is a rare example of naturally-evolved cooperation between microbial species. Our study reveals both the complexity and importance of cooperative phenotypes within the mammalian intestinal microbiota.

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Authors
Rakoff-Nahoum, S., Foster, K. R., & Comstock, L. E.
Affiliations
  • Brigham and Women's Hospital (US)
  • University of Oxford (GB)
Corresponding author
Rakoff-Nahoum, Seth
Venue
Nature
Published
2016-04-25
Volume
533
Issue
7602
Pages
255-259
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2335934832
Cited by
616
References
33
Citations by year
2026: 51 · 2025: 50 · 2024: 69 · 2023: 58 · 2022: 89 · 2021: 56 · 2020: 69 · 2019: 59 · 2018: 55 · 2017: 42 · 2016: 18
FWCI
30.15
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • National Institute of Allergy and Infectious Diseases (R01AI081843)
  • National Institute of Diabetes and Digestive and Kidney Diseases (P30DK34845, P30DK034854)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12HD052896)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Social Sciences › Sociology and Political Science › Evolutionary Game Theory and Cooperation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
Keywords
gut microbiota, microbial cooperation, cross-feeding, Bacteroides ovatus, Bacteroides vulgatus, Bacteroides thetaiotaomicron, Bacteroidales, dietary polysaccharides, microbial community stability, interspecies interactions
MeSH terms
Gastrointestinal Microbiome, Animals, Bacteroides, Dietary Carbohydrates, Biological Evolution, Germ-Free Life, Glycoside Hydrolases, Humans, Intestines, Inulin, Male, Symbiosis, Mice, In Vitro Techniques

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