Abstract
Over the last decade, our appreciation for the contribution of resident gut microorganisms—the gut microbiota—to human health has surged. However, progress is limited by the sheer diversity and complexity of these microbial communities. Compounding the challenge, the majority of our commensal microorganisms are not close relatives of Escherichia coli or other model organisms and have eluded culturing and manipulation in the laboratory. In this Review, we discuss how over a century of study of the readily cultured, genetically tractable human gut Bacteroides has revealed important insights into the biochemistry, genomics and ecology that make a gut bacterium a gut bacterium. While genome and metagenome sequences are being produced at breakneck speed, the Bacteroides provide a significant ‘jump-start’ on uncovering the guiding principles that govern microbiota–host and inter-bacterial associations in the gut that will probably extend to many other members of this ecosystem.
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References
Sender, R., Fuchs, S. & Milo, R. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164, 337–340 (2016).
Savage, D. C. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31, 107–133 (1977).
Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 (2006).
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I. & Jansson, J. K. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).
Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A. & Gordon, J. I. Host-bacterial mutualism in the human intestine. Science 307, 1915–1920 (2005).
Koenig, J. E. et al. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl Acad. Sci. USA 108, 4578–4585 (2011).
Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A. & Brown, P. O. Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 (2007).
Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013).
Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).
The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).
David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).
Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).
Browne, H. P. et al. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature 533, 543–546 (2016).
Rettedal, E. A., Gumpert, H. & Sommer, M. O. Cultivation-based multiplex phenotyping of human gut microbiota allows targeted recovery of previously uncultured bacteria. Nat. Commun. 5, 4714 (2014).
Sommer, M. O. Advancing gut microbiome research using cultivation. Curr. Opin. Microbiol. 27, 127–132 (2015).
Goodman, A. L. et al. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc. Natl Acad. Sci. USA 108, 6252–6257 (2011).
Lagier, J.-C. C. et al. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat. Microbiol. 1, 16203 (2016).
Distaso, A. Contribution à l’étude sur l’intoxication intestinale. Centralb. f. Bakteriol. 62, 433 (1912).
Eggerth, A. H. & Gagnon, B. H. The Bacteroides of human feces. J. Bacteriol. 25 389–413 (1933).
Veillon, M. H. & Zuber, H. Recherches sur quelques microbes strictement anaérobies et leur rôle en pathologie. Arch. Med. Exp. Anat. Pathol. 10, 517–545 (1898).
Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).
Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6, 776–788 (2008).
Kraus, D. Concepts of Modern Biology (Globe Book Company, 1993).
Helander, H. F. & Fändriks, L. Surface area of the digestive tract – revisited. Scand. J. Gastroenterol. 49, 681–689 (2014).
Donaldson, G. P., Lee, S. M. & Mazmanian, S. K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14, 20–32 (2015).
Evans, D. F., Pye, G., Bramley, R., Clark, A. G. & Dyson, T. J. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 29, 1035–1041 (1988).
Albenberg, L., Esipova, T. V., Judge, C. P. & Bittinger, K. Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. Gastroenterology 147, 1055–1063 (2014).
Stecher, B., Maier, L. & Hardt, W.-D. D. ‘Blooming’ in the gut: how dysbiosis might contribute to pathogen evolution. Nat. Rev. Microbiol. 11, 277–284 (2013).
Belkaid, Y. & Hand, T. W. Role of the microbiota in immunity and inflammation. Cell 157, 121–141 (2014).
Kurokawa, K., Itoh, T., Kuwahara, T. & Oshima, K. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res. 14, 169–181 (2007).
Baughn, A. D. & Malamy, M. H. The strict anaerobe Bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature 427, 441–444 (2004).
Meehan, B. M., Baughn, A. D., Gallegos, R. & Malamy, M. H. Inactivation of a single gene enables microaerobic growth of the obligate anaerobe Bacteroides fragilis. Proc. Natl Acad. Sci. USA 109, 12153–12158 (2012).
Rocha, E. R. & Smith, C. J. Ferritin-like family proteins in the anaerobe Bacteroides fragilis: when an oxygen storm is coming, take your iron to the shelter. Biometals 26, 577–591 (2013).
Smalley, D., Rocha, E. R. & Smith, C. J. Aerobic-type ribonucleotide reductase in the anaerobe Bacteroides fragilis. J. Bacteriol. 184, 895–903 (2002).
Rocha, E. R., Selby, T., Coleman, J. P. & Smith, J. C. Oxidative stress response in an anaerobe, Bacteroides fragilis: a role for catalase in protection against hydrogen peroxide. J. Bacteriol. 178, 6895–6903 (1996).
Bry, L., Falk, P. G., Midtvedt, T. & Gordon, J. I. A model of host–microbial interactions in an open mammalian ecosystem. Science 273, 1380–1383 (1996).
Ng, K. M. et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502, 96–99 (2013).
Wright, E. M., Martín, M. G. & Turk, E. Intestinal absorption in health and disease—sugars. Best. Pract. Res. Clin. Gastroenterol. 17, 943–956 (2003).
Salyers, A. A., Vercellotti, J. R. & West, S. E. Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl. Environ. Microbiol. 33, 319–322 (1977).
McNeil, N. I. The contribution of the large intestine to energy supplies in man. Am. J. Clin. Nutr. 39, 338–342 (1984).
Lee, S. M. et al. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501, 426–429 (2013).
Anderson, K. L. & Salyers, A. A. Biochemical evidence that starch breakdown by Bacteroides thetaiotaomicron involves outer membrane starch-binding sites and periplasmic starch-degrading enzymes. J. Bacteriol. 171, 3192–3198 (1989).
Anderson, K. L. & Salyers, A. A. Genetic evidence that outer membrane binding of starch is required for starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 171, 3199–3204 (1989).
Martens, E. C., Chiang, H. C. & Gordon, J. I. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4, 447–457 (2008).
Koropatkin, N. M., Cameron, E. A. & Martens, E. C. How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10, 323–335 (2012).
Motherway, M. et al. Characterization of ApuB, an extracellular type II amylopullulanase from Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 74, 6271–6279 (2008).
Xu, J. et al. A genomic view of the human–Bacteroides thetaiotaomicron symbiosis. Science 299, 2074–2076 (2003).
Xu, J. et al. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 5, e156 (2007).
Cameron, E. A. et al. Multifunctional nutrient-binding proteins adapt human symbiotic bacteria for glycan competition in the gut by separately promoting enhanced sensing and catalysis. mBio 5, e01441–14 (2014).
Martens, E. C., Roth, R., Heuser, J. E. & Gordon, J. I. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J. Biol. Chem. 284, 18445–18457 (2009).
Lynch, J. B. & Sonnenburg, J. L. Prioritization of a plant polysaccharide over a mucus carbohydrate is enforced by a Bacteroides hybrid two-component system. Mol. Microbiol. 85, 478–491 (2012).
Sonnenburg, E. D. et al. A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism. Proc. Natl Acad. Sci. USA 103, 8834–8839 (2006).
Townsend, G. E., Raghavan, V., Zwir, I. & Groisman, E. A. Intramolecular arrangement of sensor and regulator overcomes relaxed specificity in hybrid two-component systems. Proc. Natl Acad. Sci. USA 110, 161–169 (2013).
Raghavan, V., Lowe, E. C., Townsend, G. E., Bolam, D. N. & Groisman, E. A. Tuning transcription of nutrient utilization genes to catabolic rate promotes growth in a gut bacterium. Mol. Microbiol. 93, 1010–1025 (2014).
Schwalm, N. D., Townsend, G. E. & Groisman, E. A. Multiple signals govern utilization of a polysaccharide in the gut bacterium Bacteroides thetaiotaomicron. mBio 7, e01342–16 (2016).
Cann, I., Bernardi, R. C. & Mackie, R. I. Cellulose degradation in the human gut: Ruminococcus champanellensis expands the cellulosome paradigm. Environ. Microbiol. 18, 307–310 (2016).
Artzi, L., Bayer, E. A. & Moraïs, S. Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides. Nat. Rev. Microbiol. 15, 83–95 (2016).
Sonnenburg, J. L. et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955–1959 (2005).
Sonnenburg, E. D. et al. Diet-induced extinctions in the gut microbiota compound over generations. Nature 529, 212–215 (2016).
Pumbwe, L., Skilbeck, C. A. & Wexler, H. M. The Bacteroides fragilis cell envelope: quarterback, linebacker, coach-or all three? Anaerobe 12, 211–220 (2006).
Wangdi, T., Lee, C. Y., Spees, A. M., Yu, C. & Kingsbury, D. D. The Vi capsular polysaccharide enables Salmonella enterica serovar typhi to evade microbe-guided neutrophil chemotaxis. PLoS Pathog. 10, e1004306 (2014).
Doorduijn, D. J., Rooijakkers, S. H., van Schaik, W. & Bardoel, B. W. Complement resistance mechanisms of Klebsiella pneumoniae. Immunobiology 221, 1102–1109 (2016).
Krinos, C. M. et al. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414, 555–558 (2001).
Chatzidaki-Livanis, M., Weinacht, K. G. & Comstock, L. E. Trans locus inhibitors limit concomitant polysaccharide synthesis in the human gut symbiont Bacteroides fragilis. Proc. Natl Acad. Sci. USA 107, 11976–11980 (2010).
Comstock, L. E. & Kasper, D. L. Bacterial glycans: key mediators of diverse host immune responses. Cell 126, 847–850 (2006).
Coyne, M. J. & Comstock, L. E. Niche-specific features of the intestinal Bacteroidales. J. Bacteriol. 190, 736–742 (2008).
Fletcher, C. M., Coyne, M. J., Bentley, D. L., Villa, O. F. & Comstock, L. E. Phase-variable expression of a family of glycoproteins imparts a dynamic surface to a symbiont in its human intestinal ecosystem. Proc. Natl Acad. Sci. USA 104, 2413–2418 (2007).
Coyne, M. J., Chatzidaki-Livanis, M., Paoletti, L. C. & Comstock, L. E. Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis. Proc. Natl Acad. Sci. USA 105, 13099–13104 (2008).
Peterson, D. A., McNulty, N. P., Guruge, J. L. & Gordon, J. I. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2, 328–339 (2007).
Mazmanian, S. K., Round, J. L. & Kasper, D. L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620–625 (2008).
Shen, Y. et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12, 509–520 (2012).
Chu, H. et al. Gene–microbiota interactions contribute to the pathogenesis of inflammatory bowel disease. Science 352, 1116–1120 (2016).
Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006).
Fischbach, M. A. & Sonnenburg, J. L. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe 10, 336–347 (2011).
Sonnenburg, E. D. & Sonnenburg, J. L. Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 20, 779–786 (2014).
Harmsen, H. J. et al. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30, 61–67 (2000).
Marcobal, A. et al. Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food. Chem. 58, 5334–5340 (2010).
Marcobal, A. et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10, 507–514 (2011).
Kunz, C., Rudloff, S., Baier, W., Klein, N. & Strobel, S. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu. Rev. Nutr. 20, 699–722 (2000).
Ninonuevo, M. R., Park, Y., Yin, H. & Zhang, J. A strategy for annotating the human milk glycome. J. Agric. Food Chem. 54 7471–7480 (2006).
Charbonneau, M. R. et al. Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell 164, 859–871 (2016).
Fukuda, S. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543–547 (2011).
Saez-Lara, M. J. & Gomez-Llorente, C. The role of probiotic lactic acid bacteria and bifidobacteria in the prevention and treatment of inflammatory bowel disease and other related diseases: a systematic review of randomized human clinical trials. Biomed. Res. Int. 2015, 505878 (2015).
Mahowald, M. A. et al. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc. Natl Acad. Sci. USA 106, 5859–5864 (2009).
Sonnenburg, J. L., Chen, C. T. L. & Gordon, J. I. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol. 4, e413 (2006).
Allen, R. H. & Stabler, S. P. Identification and quantitation of cobalamin and cobalamin analogues in human feces. Am. J. Clin. Nutr. 87, 1324–1335 (2008).
Degnan, P. H., Taga, M. E. & Goodman, A. L. Vitamin B12 as a modulator of gut microbial ecology. Cell Metab. 20, 769–778 (2014).
Degnan, P. H., Barry, N. A., Mok, K. C., Taga, M. E. & Goodman, A. L. Human gut microbes use multiple transporters to distinguish vitamin B12 analogs and compete in the gut. Cell Host Microbe 15, 47–57 (2014).
Goodman, A. L. et al. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6, 279–289 (2009).
Rakoff-Nahoum, S., Coyne, M. J. & Comstock, L. E. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24, 40–49 (2014).
Rakoff-Nahoum, S., Foster, K. R. & Comstock, L. E. The evolution of cooperation within the gut microbiota. Nature 533, 255–259 (2016).
Elhenawy, W., Debelyy, M. O. & Feldman, M. F. Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. mBio 5, e00909–14 (2014).
Kulp, A. & Kuehn, M. J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64, 163 (2010).
Mazmanian, S. K., Liu, C. H., Tzianabos, A. O. & Kasper, D. L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107–118 (2005).
Cotter, P. D., Hill, C. & Ross, R. P. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol. 3, 777–788 (2005).
Kommineni, S. et al. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526, 719–722 (2015).
Chatzidaki-Livanis, M., Coyne, M. J. & Comstock, L. E. An antimicrobial protein of the gut symbiont Bacteroides fragilis with a MACPF domain of host immune proteins. Mol. Microbiol. 94, 1361–1374 (2014).
Roelofs, K. G., Coyne, M. J., Gentyala, R. R., Chatzidaki-Livanis, M. & Comstock, L. E. Bacteroidales secreted antimicrobial proteins target surface molecules necessary for gut colonization and mediate competition in vivo. mBio 7, e01055–16 (2016).
Tomita, H., Fujimoto, S., Tanimoto, K. & Ike, Y. Cloning and genetic and sequence analyses of the bacteriocin 21 determinant encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pPD1. J. Bacteriol. 179, 7843–7855 (1997).
Russell, A. B. et al. A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 16, 227–236 (2014).
Coyne, M. J., Zitomersky, N. L., McGuire, A. M., Earl, A. M. & Comstock, L. E. Evidence of extensive DNA transfer between Bacteroidales species within the human gut. mBio 5, 14 (2014).
Russell, A. B., Peterson, S. B. & Mougous, J. D. Type VI secretion system effectors: poisons with a purpose. Nat. Rev. Microbiol. 12, 137–148 (2014).
Coyne, M. J., Roelofs, K. G. & Comstock, L. E. Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. BMC Genomics 17, 58 (2016).
Wexler, A. G. et al. Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc. Natl Acad. Sci. USA 113, 3639–3644 (2016).
Chatzidaki-Livanis, M., Geva-Zatorsky, N. & Comstock, L. E. Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc. Natl Acad. Sci. USA 113, 3627–3632 (2016).
Whitney, J. C. et al. An interbacterial NAD(P)+ glycohydrolase toxin requires elongation factor Tu for delivery to target cells. Cell 163, 607–619 (2015).
Hecht, A. L. et al. Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep. 17, 1281–1291 (2016).
Moreau, M. C., Ducluzeau, R. & Guy-Grand, D. Increase in the population of duodenal immunoglobulin A plasmocytes in axenic mice associated with different living or dead bacterial strains of intestinal origin. Infect. Immun. 21, 532–539 (1978).
Macpherson, A. J. & Harris, N. L. Opinion: interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4, 478–485 (2004).
Sprinz, H. et al. The response of the germfree guinea pig to oral bacterial challenge with Escherichia coli and Shigella flexneri. Am. J. Pathol. 39, 681–695 (1961).
Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323 (2009).
Ivanov, I. I. et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337–349 (2008).
Round, J. L. & Mazmanian, S. K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl Acad. Sci. USA 107, 12204–12209 (2010).
Neff, C. P. et al. Diverse intestinal bacteria contain putative zwitterionic capsular polysaccharides with anti-inflammatory properties. Cell Host Microbe 20, 535–547 (2016).
Vatanen, T. et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 165, 842–853 (2016).
Atarashi, K. et al. Induction of colonic regulatory T Cells by indigenous Clostridium species. Science 331, 337–341 (2011).
Rosenshine, I., Ruschkowski, S. & Stein, M. A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J. 15, 2613–2624 (1996).
Kaper, J. B., Nataro, J. P. & Mobley, H. L. T. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2, 123–140 (2004).
Curtis, M. M. et al. The gut commensal Bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape. Cell Host Microbe 16, 759–769 (2014).
Pacheco, A. R. et al. Fucose sensing regulates bacterial intestinal colonization. Nature 492, 113–117 (2012).
Huang, Y.-L. L., Chassard, C., Hausmann, M., von Itzstein, M. & Hennet, T. Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice. Nat. Commun. 6, 8141 (2015).
Rivera-Chávez, F. et al. Depletion of butyrate-producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host Microbe 19, 443–454 (2016).
McClean, K. L., Sheehan, G. J. & Harding, G. K. Intraabdominal infection: a review. Clin. Infect. Dis. 19, 100–116 (1994).
Brook, I. & Frazier, E. H. Aerobic and anaerobic microbiology in intra-abdominal infections associated with diverticulitis. J. Med. Microbiol. 49, 827–830 (2000).
Vaishnava, S. et al. The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255–258 (2011).
Runeberg, B. Studien über die bei peritonealen infektionem appendikularen ursprungs vorkommenden sauerstofftoleranten, mit besonderer berücksichtigung ihrer bedeutung für die pathogenese derartiger peritonitiden. Arb. a. d. Path. Inst. d. Univ. Helsinfors 1, 271 (1908).
Heyde, M. Bakteriologische und experimentalle untersuchungen zur aetiologie der wurmfortsatzentzündung (mit besondere berücksichtigung der anaeroben bakterien). Beitr. z. klin. Chir. 76, 1 (1911).
Castellani, A. & Chalmers, A. J. Manual of Tropical Medicine (Bailliere, Tindall & Cox, 1919).
Shah, H. N. The Genus Bacteroides and Related Taxa (Springer, 1992).
Polk, B. F. & Kasper, D. L. Bacteroides fragilis subspecies in clinical isolates. Annu. Int. Med. 86, 569–571 (1977).
Dürr, U. H. N., Sudheendra, U. S. & Ramamoorthy, A. LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta 1758, 1408–1425 (2006).
Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 415, 389–395 (2002).
Cullen, T. W. et al. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347, 170–175 (2015).
Faith, J. J., McNulty, N. P., Rey, F. E. & Gordon, J. I. Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333, 101–104 (2011).
McNulty, N. P. et al. The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci. Transl. Med. 3, 106ra106 (2011).
Arrieta, M.-C. C., Walter, J. & Finlay, B. B. Human microbiota-associated mice: a model with challenges. Cell Host Microbe 19, 575–578 (2016).
Baxter, N. T., Zackular, J. P., Chen, G. Y. & Schloss, P. D. Structure of the gut microbiome following colonization with human feces determines colonic tumor burden. Microbiome 2, 20 (2014).
Lagier, J.-C. C. et al. The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin. Microbiol. Rev. 28, 237–264 (2015).
Palm, N. W. et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158, 1000–1010 (2014).
Salyers, A. A., Bonheyo, G. & Shoemaker, N. B. Starting a new genetic system: lessons from Bacteroides. Methods 20, 35–46 (2000).
Wu, M. et al. Genetic determinants of in vivo fitness and diet responsiveness in multiple human gut Bacteroides. Science 350, aac5992 (2015).
Mimee, M., Tucker, A. C., Voigt, C. A. & Lu, T. K. Programming a human commensal bacterium, Bacteroides thetaiotaomicron, to sense and respond to stimuli in the murine gut microbiota. Cell Syst. 1, 62–71 (2015).
Kotula, J. W. et al. Programmable bacteria detect and record an environmental signal in the mammalian gut. Proc. Natl Acad. Sci. USA 111, 4838–4843 (2014).
Biteen, J. S. et al. Tools for the Microbiome: Nano and Beyond (ACS Nano, 2015).
Earle, K. A. et al. Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 18, 478–488 (2015).
Geva-Zatorsky, N. et al. In vivo imaging and tracking of host–microbiota interactions via metabolic labeling of gut anaerobic bacteria. Nat. Med. 21, 1091–1100 (2015).
Nishijima, S. et al. The gut microbiome of healthy Japanese and its microbial and functional uniqueness. DNA Res. 23, 125–133 (2016).
Acknowledgements
We thank W. Schofield and B. Lim for careful reading of the manuscript. Support for this work was provided by the National Institutes of Health (GM105456 and GM118159), the Pew Scholars Program, and the Burroughs Wellcome Fund to A.L.G. A.G.W. is supported by a fellowship from the Gruber Foundation.
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A.G.W. drafted the manuscript and prepared figures. A.G.W. and A.L.G. edited the manuscript. All authors read and approved the final manuscript.
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Wexler, A., Goodman, A. An insider's perspective: Bacteroides as a window into the microbiome. Nat Microbiol 2, 17026 (2017). https://doi.org/10.1038/nmicrobiol.2017.26
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DOI: https://doi.org/10.1038/nmicrobiol.2017.26
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The impact of maternal asthma on the preterm infants' gut metabolome and microbiome (MAP study)
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Impact of international travel and diarrhea on gut microbiome and resistome dynamics
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