Gut Biogeography of the Bacterial Microbiota

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Gut Biogeography of the Bacterial Microbiota REVIEWS MICROBIOME Gut biogeography of the bacterial microbiota Gregory P. Donaldson, S. Melanie Lee and Sarkis K. Mazmanian Abstract | Animals assemble and maintain a diverse but host-specific gut microbial community. In addition to characteristic microbial compositions along the longitudinal axis of the intestines, discrete bacterial communities form in microhabitats, such as the gut lumen, colonic mucus layers and colonic crypts. In this Review, we examine how the spatial distribution of symbiotic bacteria among physical niches in the gut affects the development and maintenance of a resilient microbial ecosystem. We consider novel hypotheses for how nutrient selection, immune activation and other mechanisms control the biogeography of bacteria in the gut, and we discuss the relevance of this spatial heterogeneity to health and disease. Microbiota Humans and other mammals harbour a complex gastro- present in the gut microbiota, such as Escherichia coli and 10 The collection of intestinal microbiota that includes all three domains of Clostridium perfringens . Several species of Bacteroides microorganisms (including life (Archaea, Bacteria and Eukarya). This extraordinary can also utilize fucosylated oligosaccharides as carbon bacteria, viruses, fungi and symbiosis, formed by a series of exposures to environ- sources11, suggesting that their colonization of the gut single-celled eukaryotes) that prebiotic inhabit a particular habitat, mental factors, is initiated on contact with the maternal is aided by the properties of milk. Accordingly, 1 such as an animal. vaginal microbiota during birth . Abrupt changes during children of mothers with non‑functional fucosyltrans- the first year of life follow a pattern that corresponds ferase 2 (FUT2), an enzyme required for the fucosylation Syntrophic interactions to gestational age in both mice2 and humans3, which of milk oligosaccharides, display lower levels of faecal Metabolic relationships in suggests that strong deterministic processes shape the Bifidobacterium spp. and Bacteroides spp.12. The impor- which one member provides nutrients to another. composition of the microbiota during development. tance of diet in determining the composition of the These population shifts may be explained by influences microbial community in the gut is also highlighted by Secreted immunoglobulin A from the diet, the developing immune system, chemical the observation that the transition to solid foods coin- (sIgA). By far the most exposures and, potentially, the founder effects of initial cides with the establishment of a microbiota similar to abundant isotype of antibody found in the gut. colonizers. Founder effects are not well understood in that found in adults. the mammalian gut, but the profound changes in host The adult intestinal microbiota consists of hundreds Prebiotic gene expression that occur in response to microorgan- to thousands of species, dominated by the Bacteroidetes A molecule that serves as a isms and also the great potential for syntrophic interactions and Firmicutes phyla13. This ecosystem is distinct from nutrient which stimulates the between bacteria suggest that early colonizers would those of any other microbial habitats that have been sur- growth of commensal or 14 mutualistic gut bacteria. In have long-term effects on the establishment of the veyed and includes many species that exist nowhere else many cases, prebiotics can be microbiota. The immune system imposes selective pres- in nature, indicating that co-evolution of the host with specific for discrete groups of sure on the microbiota through both innate and adaptive its gut microbial symbionts (including commensals and bacteria on the basis of their mechanisms, such as antimicrobial peptides4, secreted mutualists) has generated powerful selective mechanisms. metabolic (that is, nutritional) immunoglobulin A 5 6 requirements. (sIgA) and other contributing factors A recent study of how different microbial communities (see below). However, current research suggests that colonize gnotobiotic animals showed that deterministic diet has the greatest impact on microbiota assembly. mechanisms (presumably host–microorganism inter- Before weaning, breast milk plays a crucial part in actions) led to reproducible shaping of the microbiota shaping the microbial community composition via regardless of the source of the input community15. Division of Biology and transmission of the milk microbiota to the infant gut7, The adult intestinal microbiota is also partially stable, Biological Engineering, protection from harmful species by secreted maternal as a core of ~40 bacterial species (accounting for 75% of California Institute of antibodies8 and selection for certain species by milk the gut microbiota in terms of abundance) persists for at Technology, Pasadena, 16 California 91125, USA. oligosaccharides, which can be used by microorganisms least 1 year in individuals . A more extensive longitudi- 9 Correspondence to S.K.M. as carbon sources . For example, in in vitro competitive nal study found that 60% of all bacterial strains within an [email protected] growth experiments, Bifidobacterium longum benefits individual persisted for 5 years17. During severe pertur- doi:10.1038/nrmicro3552 from its ability to use the fucosylated oligosaccharides bations such as antibiotic treatment, the faecal commu- Published online 26 Oct 2015 in human milk to outgrow other bacteria that are usually nity is depleted to a low-diversity consortium, but after 20 | JANUARY 2016 | VOLUME 14 www.nature.com/micro © 2016 Macmillan Publishers Limited. All rights reserved REVIEWS Dominant gut phyla: small intestine, caecum and large intestine (colon). Bacteroidetes, Firmicutes, Actinobacteria, Proteobacteria, Verrucomicrobia Physiological variations along the lengths of the small intestine and colon include chemical and nutrient gradi- Predominant families in the: ents, as well as compartmentalized host immune activity, Small intestine Colon all of which are known to influence bacterial community Lactobacillaceae, Bacteroidaceae, Prevotellaceae, composition. For example, the small intestine is more Enterobacteriaceae Rikenellaceae, Lachnospiraceae, Ruminococcaceae Inter-fold regions acidic, and has higher levels of oxygen and antimicro- Lachnospiraceae, bials than the colon (FIG. 1). Therefore, the microbial Bile Transverse Ruminococcaceae community of the small intestine is dominated by fast- duct growing facultative anaerobes that tolerate the combined effects of bile acids and antimicrobials while still effec- tively competing with both the host and other bacteria for the simple carbohydrates that are available in this Ascending Descending region of the gastrointestinal tract. Bile acids, secreted through the bile duct at the proximal end of the small intestine, are bactericidal to certain species owing to their surfactant properties and are known to broadly shape the composition of the microbiota, especially in Appendix Digesta the small intestine. For example, feeding mice excess bile Caecum Bacteroidaceae, acids generally stimulates the growth of Firmicutes and Prevotellaceae, 19 Rectum inhibits the growth of Bacteroidetes . In addition, the Rikenellaceae shorter transit time in the small intestine compared with 1011 cfu g–1 102 cfu g–1 in the colon (an order of magnitude shorter, despite the Bacterial load greater length of the small intestine) is thought to make pH bacterial adherence to tissue or mucus an important Antimicrobials factor for persistent colonization of the small intestine. In ileostomy samples from humans, the small Oxygen intestine was found to exhibit lower bacterial diver- Proximal Distal sity than the colon and was highly enriched in certain Figure 1 | Microbial habitats in the human lower gastrointestinalNature Reviews tract. |The Microbiology dominant Clostridium spp. and certain members of the phylum bacterial phyla in the gut are Bacteroidetes, Firmicutes, Actinobacteria, Proteobacteria Proteobacteria20. Furthermore, a metatranscriptomic and Verrucomicrobia. The dominant bacterial families of the small intestine and colon analysis revealed that, compared with faecal samples, reflect physiological differences along the length of the gut. For example, a gradient of ileal samples showed much higher expression of genes oxygen, antimicrobial peptides (including bile acids, secreted by the bile duct) and pH limits the bacterial density in the small intestinal community, whereas the colon involved in central metabolism and in pathways respon- carries high bacterial loads. In the small intestine, the families Lactobacillaceae and sible for the import of simple sugars by facultative anaer- 20 Enterobacteriaceae dominate, whereas the colon is characterized by the presence obes . In mice, Proteobacteria (especially members of of species from the families Bacteroidaceae, Prevotellaceae, Rikenellaceae, the family Enterobacteriaceae) and members of the fam- Lachnospiraceae and Ruminococcaceae (colours correspond with the relevant phyla). ily Lactobacillaceae are enriched in the small intestine21. A cross-section of the colon shows the digesta, which is dominated by Bacteroidaceae, Although bacteria in the small intestine are potentially Prevotellaceae and Rikenellaceae, and the inter-fold regions of the lumen, which are competing with the host for nutrients, host-derived bile dominated by Lachnospiraceae and Ruminococcaceae. cfu, colony-forming units. acids and antimicrobial peptides limit bacterial growth to low densities in proximal
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