Trends in Ecology & Evolution
Review
Microbial ecologyAssembly of the human intestinal microbiota
Microbial ecology
Introduction
Like other mammals, humans have been associated with complex microbial communities throughout our evolution, with every birth renewing this intimate web of relationships. The specialized microbes inhabiting the surfaces and alimentary tract of a human adult (Box 1) outnumber the human cells by a factor of ten [1]. The hundreds of microbial species native to the colon, where microbial richness and abundance are maximal, contain 100-fold more genes than does the human genome [1]. This large and diverse microbiota (see Glossary) has long been recognized as contributing to gut maturation, host nutrition and pathogen resistance [2]; more recently, microbes have been shown to regulate intestinal epithelial proliferation [3], host energy metabolism [4] and inflammatory immune responses [5]. Intestinal communities are implicated in diseases ranging from allergies [6] to late-onset autism [7], inflammatory bowel disease [8] and cancer [9]. Hence, our understanding of intestinal microbial ecology has a direct bearing on our ability to manage and maintain human health (Box 2).
The prevailing ecological paradigm for the adult human gut microbiota, now decades old, is that each region of the intestine (Box 1) harbors a stable climax community comprising the superior competitors for a fixed set of niches 2, 10. This perspective has fostered fruitful research into the factors that define microbial niches in the intestine, such as the diet and genotype of the host. However, we argue here that the diverse and personalized gut communities of humans are also shaped by less predictable influences, such as historical contingencies during community assembly and temporal dynamics arising from interactions within the microbiota.
Section snippets
History: new evidence and old perspectives
During the 1970s, epidemiological links between diet and cancer stimulated intensive cultivation-based research in gastrointestinal microbiology. The diversity of human fecal bacteria was unexpectedly high, with only a minority of individuals harboring most species, even among those individuals with similar diets, ethnicity and geographical origin 11, 12. By contrast, the identity and relative abundance of most genera was similar within such social groups and, to some extent, between groups [12]
Factors generating a diverse, personalized human microbiota
Although many factors are known to influence intestinal microbiota, we focus here on diet, host genotype and microbial interactions, three categories that seem most able to explain the diversity and the individuality of these communities.
Colonization history
The effects of diet, genotype and microbial interactions on the composition of the intestinal microbiota are productive areas of research, but ‘accidents’ also influence the microbiota of every individual. The thousands of microbial strains capable of inhabiting the gut are distributed unevenly between hosts and differ in transmissibility [12]; thus, the colonization history of a particular human can only be described in probabilistic terms, rather than being predicted in detail 29, 56. The
Conclusions and future directions
Recent culture-independent investigations have greatly expanded our knowledge of the human gastrointestinal microbiota, emphasizing its diversity and uniqueness in every individual. Several external factors have predictable effects on the composition of colonic communities, but interactions within the microbiota determine the existence and extent of many microbial niches. The uneven distribution, overlapping resource-use profiles and strong interactions that are characteristic of
Acknowledgements
We thank B. Bohannan and members of the Relman laboratory for stimulating discussions, and apologize to colleagues whose work we could not cite owing to space limitations. Work in the authors’ laboratory is supported by the National Institutes of Health (DE13541 and AI51259), the Horn Foundation, and the Ellison Medical Foundation.
Glossary
- Archaea
- a domain (the highest taxonomic rank) containing prokaryotic microbes that includes the methanogens. Archaea, Bacteria (another domain of prokaryotic microbes), and Eukarya (all organisms with nucleated cells) comprise the three-domain taxonomy of life.
- Bacteriocin
- a protein released by a microbe with killing activity against other microbes.
- Climax
- a steady-state community composition attained as the endpoint of succession.
- Fermentation
- an anaerobic energy-generating pathway involving the
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These authors contributed equally to this work.