The evolution of cooperation within the gut microbiota

• Published in: Nature (London) 2016-05, Vol.533 (7602), p.255-259
• Main Authors: Rakoff-Nahoum, Seth, Foster, Kevin R., Comstock, Laurie E.
• Format: Article
• Language: English
• Subjects: 13/44; 42/41; 631/181/2469; 631/326/2565/2134; 82/83; Animals; Antibiotic resistance; Bacteria; Bacteroides - enzymology; Bacteroides - genetics; Bacteroides - physiology; Biofilms; Biological Evolution; Dietary Carbohydrates - metabolism; Digestive system; Enzymes; Evolution; Gastrointestinal Microbiome - physiology; Genetic aspects; Germ-Free Life; Glycoside Hydrolases - metabolism; Gram-negative bacteria; Humanities and Social Sciences; Humans; In Vitro Techniques; Intestines - microbiology; Inulin - metabolism; letter; Male; Mice; Microbial activity; Microbiology; Microbiota (Symbiotic organisms); multidisciplinary; Observations; Phenotypes; Quorum sensing; Saccharides; Science; Symbiosis
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature17626

Little is known about cooperative behaviour among the gut microbiota; here, limited cooperation is demonstrated for Bacteroides thetaiotaomicron , but Bacteroides ovatus is found to extracellularly digest a polysaccharide not for its own use, but to cooperatively feed other species such as Bacteroides vulgatus from which it receives return benefits. Cooperation between gut microbes Microbial communities are essentially cooperative networks and here Seth Rakoff-Nahoum et al . examine the mechanisms of cooperative behaviour among gut microbiota. Using a combination of in vitro experiments and a mouse model, the authors show that Bacteroides ovatus uses an enzyme system for the extracellular digestion of the dietary polysaccharide inulin, which is a costly process, but benefits other species such as Bacteroides vulgatus , by supplying a source of food. Potential routes by which B. vulgatus may provide return benefits to B. ovatus include detoxification of inhibitory substances and the secretion of a depleted or growth promoting factor. This is a rare example of naturally evolved cooperation within complex microbial communities that is likely to have an important role in stabilizing the ecosystem. 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 1 , 2 , 3 , 4 , 5 . The human intestine houses a dense and diverse microbial community critical to health 1 , 2 , 4 , 5 , 6 , 7 , 8 , 9 , 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