The evolution of cooperation within the gut microbiota.
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.
Division of Infectious Diseases, Department of Medicine, Boston Children's Hospital and Harvard Medical School, 300 Longwood Avenue, Boston, Massachusetts 02115, USA.|Division of Infectious Diseases, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, Massachusetts 02115, USA.
Seth
S
Rakoff-Nahoum
Department of Zoology and Oxford Centre for Integrative Systems Biology, University of Oxford, Oxford OX1 3PS, UK.
Kevin R
KR
Foster
Division of Infectious Diseases, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, Massachusetts 02115, USA.
Laurie E
LE
Comstock
D000818:Animals; D001439:Bacteroides / Q000201:enzymology / Q000235:genetics / Q000502:physiology*; D005075:Biological Evolution; D004040:Dietary Carbohydrates / Q000378:metabolism; D000069196:Gastrointestinal Microbiome / Q000502:physiology*; D005856:Germ-Free Life; D006026:Glycoside Hydrolases / Q000378:metabolism; D006801:Humans; D066298:In Vitro Techniques; D007422:Intestines / Q000382:microbiology; D007444:Inulin / Q000378:metabolism; D008297:Male; D051379:Mice; D013559:Symbiosis
D004040:Dietary Carbohydrates; D007444:Inulin; D006026:Glycoside Hydrolases