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The Human Gut Microbiome: Ecology and Recent Evolutionary Changes University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in Food Science and Technology Food Science and Technology Department 6-2011 The Human Gut Microbiome: Ecology and Recent Evolutionary Changes Jens Walter Ruth Ley Follow this and additional works at: https://digitalcommons.unl.edu/foodsciefacpub Part of the Food Science Commons, Genetics and Genomics Commons, and the Microbiology Commons This Article is brought to you for free and open access by the Food Science and Technology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in Food Science and Technology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. MI65CH21-Ley ARI 27 July 2011 8:58 The Human Gut Microbiome: Ecology and Recent Evolutionary Changes Jens Walter1 and Ruth Ley2 1Department of Food Science, University of Nebraska, Lincoln, Nebraska 68583-0919 2Department of Microbiology, Cornell University, Ithaca, New York 14853; email: [email protected] Annu. Rev. Microbiol. 2011. 65:411–29 Keywords First published online as a Review in Advance on host-microbe interactions, ecological theory, niche, microbial June 16, 2011 diversity, human genetics, amylase The Annual Review of Microbiology is online at micro.annualreviews.org Abstract This article’s doi: The human gastrointestinal tract is divided into sections, allowing di- 10.1146/annurev-micro-090110-102830 gestion and nutrient absorption in the proximal region to be separate Copyright c 2011 by Annual Reviews. from the vast microbial populations in the large intestine, thereby re- All rights reserved ducing conflict between host and microbes. In the distinct habitats of 0066-4227/11/1013-0411$20.00 the gut, environmental filtering and competitive exclusion between mi- crobes are the driving factors shaping microbial diversity, and stochas- tic factors during colonization history and in situ evolution are likely to introduce intersubject variability. Adaptive strategies of microbes with different niches are genomically encoded: Specialists have smaller genomes than generalists, and microbes with environmental reservoirs have large accessory genomes. A shift toward a Neolithic diet increased loads of simple carbohydrates and selected for their increased break- down and absorption in the small intestine. Humans who outcompeted microbes for the new substrates obtained more energy from their diets and prospered, an evolutionary process reflected in modern population genetics. The three-way interactions between human genetics, diet, and the microbiota fundamentally shaped modern populations and continue to affect health globally. 411 MI65CH21-Ley ARI 27 July 2011 8:58 brates because vertebrate hosts generally har- Contents bor more diverse and dense microbial commu- nities in their intestines (45, 58). The human INTRODUCTION.................. 412 gut microbiota as a whole encode 150 times GUT HABITATS AND THEIR more genes in their collective metagenome than INHABITANTS.................. 412 are present in the human host genome (70). Stomach and Small Intestine. 414 Traits humans have gained from the acqui- LargeIntestine.................... 414 sition of microbial symbionts include biosyn- MICROBIAL ECOLOGY thetic capacities to break down a greater range OFTHEGUT.................... 415 of plant polysaccharides; microbial fermenta- Determinants of a Highly Individual tion provides roughly 10% of daily energy from Microbiome Composition . 416 a Western diet (8). But human gut microbes ap- GutNiches........................ 419 pear to have retained many genes also present RECENT EVOLUTION OF THE in the host genome (70). Host enzymes that are HUMAN-MICROBIOTA active in food degradation have equivalents in SYMBIOSIS....................... 420 most if not all gut bacterial genomes (51). This Changes to the Microbiome over stands in contrast to the mutualisms of insects, Human Evolution. 422 in which either bacteria or host loses redun- CONCLUDINGREMARKS......... 423 dant functions and as a result they become irre- versibly dependent on each other for nutrition (60). In this review, we focus on the ecology and INTRODUCTION evolution of the human gut microbiota over A fast and powerful way for an organism to the long term and in very recent human evo- take on new faculties is to acquire the necessary lution. We discuss the current understanding genes from another organism. In microbes, the of microbial biomass and diversity in the small Niche: the ecological expansion into new niches is often and large intestines, the functions of microbes complement of facilitated by the uptake of gene sequences in these habitats, and the ecological forces that activities that support from other microbes via horizontal gene trans- have shaped the gut microbiome. We present the life of an organism, commonly compared fer (91). In contrast, multicellular eukaryotes evidence that the community composition of to profession do not take up exogenous DNA as readily as the gut microbiota and the genetic content of Microbiota: microbes; instead, they form symbiotic asso- bacterial genomes are determined largely by microbial life forms ciations with microbes that carry the necessary adaptations to niches whose characteristics are within a given habitat genes, allowing a rapid adaptive extension shaped by host genotype and microbial inter- or host of their phenotypic capabilities (78). Host- actions within the communities. We then dis- Metagenome: microbe symbiosis is widely distributed within cuss how very recent culturally driven changes community-level the Eukaryota, and the molecular mechanisms in diet are likely to have challenged the com- genome composed of that underlie these relationships and the con- petitive balance of host and gut microbiota and the combined genomes of its constituents tributions made by the microbes toward their to have affected the evolution of this symbiosis. host’s biology are well understood in certain Habitat: the dwelling GUT HABITATS AND THEIR place of an organism invertebrates (e.g., insects and squids) (57, 64). Many of the interactions that have emerged INHABITANTS Microbiome: microbial life forms between symbiotic partners are mutualistic and The human digestive tract is partitioned to seg- inhabiting a living enhance the fitness of the host, and in insects, regate the host digestive processes from most host, their combined those include contribution to nutrition and of the microbial biomass, so that the host has genomes, and their defense. the first shot at dietary substrates. Host di- interactions with the Host-microbe symbiosis in humans and gestive enzymes (e.g., amylase and lipase) are host other mammals differs from that in inverte- secreted from the salivary glands (Figure 1) 412 Walter · Ley MI65CH21-Ley ARI 27 July 2011 8:58 ab pH gradient Microbial biomass Salivary 2–3 gland Oral cavity, 108–9 cells/ml Stomach 1.5–5 10 cells/ml Duodenum 5–7 103–4 cells/ml Esophagus Jejunum 7–9 104–5 cells/ml Ileum 7–8 108 cells/ml Liver Stomach Ileocecal valve Duodenum Pancreas Colon 11 Ileocecal Colon 5–7 10 cells/ml valve Jejunum Cecum Ileum Rectum c Bacterial population present Oral cavity: Small intestine: Gemella (e.g., G. haemolysans), Granulicatella, Escherichia coli, Klebsiella, Enterococcus, Bacteroides, Streptococcus (e.g., S. mitis), Veillonella, Prevotella, Ruminococcus, Dorea, Clostridium, Coprococcus, Porphyromonas, Rothia, Neisseria, Fusobacterium, Weissella, Lactobacillus (some species) Lactobacillus Allochthonous: Granulicatella, Streptococcus Allochthonous microbes are generally outnumbered (e.g., S. mitis), Veillonella, Lactobacillus by autochthonous microbes. Stomach: Large intestine: Helicobacter pylori Five major phyla: Firmicutes, Bacteroidetes, Actionobacteria, Verrucomicrobia, and Proteobacteria. Allochthonous: Gemella (e.g., G. haemolysans), Hundreds of species. Granulicatella, Streptococcus (e.g., S. mitis), Veillonella, Prevotella, Porphyromonas, Rothia, Neisseria, Allochthonous microbes are generally outnumbered Fusobacterium, Lactobacillus by autochthonous microbes. Figure 1 Characteristics of the major habitats of the human gastrointestinal tract and their inhabitants. (a) The major sections of the gastrointestinal tract. (b) Bars in the center indicate pH levels moving from the stomach to the distal gut (left) and biomass levels (right). (c) Boxes indicate the dominant types of microbes either allochthonous or autochthonous to those habitats. www.annualreviews.org • The Human Gut Microbiome 413 MI65CH21-Ley ARI 27 July 2011 8:58 during mastication, and the stomach retains the growth (40). In addition, bile salts, which are food and provides the acidic pH for the host’s secreted into the duodenum via the bile, are proteases to be active. Additional enzymes (e.g., strongly bactericidal. Another tool in the host proteases, lipases, and amylase) are added from arsenal for controlling bacteria is immunoglob- the pancreas and liver via the biliary ducts in the ulin (Ig). IgA recognizes the dominant microbes small intestine (SI). Food components that are present (32). The majority of IgA is thought to degradable by the digestive enzymes are broken be relatively unselective because it binds with down to simple sugars, amino acids, and fatty epitopes that are widely shared among gut bac- acids, which are absorbed in the SI. Food com- teria (89). IgA is generally thought to limit mi- ponents that escape digestion (fiber, resistant crobial penetration
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