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Host-Microbial Symbiosis in the Vertebrate Gastrointestinal Tract and the Lactobacillus Reuteri Paradigm

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Host-Microbial Symbiosis in the Vertebrate Gastrointestinal Tract and the Lactobacillus Reuteri Paradigm Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm Jens Waltera,1, Robert A. Brittonb, and Stefan Roosc aDepartment of Food Science and Technology, University of Nebraska, Lincoln, NE 68583-0919; bDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824; and cDepartment of Microbiology, Swedish University of Agricultural Sciences, S-750 07 Uppsala, Sweden Edited by Todd R. Klaenhammer, North Carolina State University, Raleigh, NC, and approved June 1, 2010 (received for review February 6, 2010) Vertebrates engage in symbiotic associations with vast and com- Greek sym “with” and biosis “living”), a term that describes close plex microbial communities that colonize their gastrointestinal and long-term interactions between unlike organisms (10). Once tracts. Recent advances have provided mechanistic insight into the considered a rare phenomenon, microbial symbiosis is gaining important contributions of the gut microbiome to vertebrate recognition as a ubiquitous feature in animal life (11). According biology, but questions remain about the evolutionary processes to the fitness effects on the host, symbiotic relationships can be that have shaped symbiotic interactions in the gut and the con- everything from beneficial to detrimental. This broad definition sequences that arise for both the microbes and the host. Here we of symbiosis is not universally agreed on, and some researchers discuss the biological principles that underlie microbial symbiosis prefer to reserve the term solely for mutualistic interactions. in the vertebrate gut and the potential of the development of However, when Anton de Bary introduced the term in the mid- mutualism. We then review phylogenetic and experimental stud- nineteenth century, he characterized symbiosis as “specific cases ies on the vertebrate symbiont Lactobacillus reuteri that have pro- of parasitism and mutualism” (10). vided novel insight into the ecological and evolutionary strategy In this article we will follow de Bary’soriginaldefinition and refer of a gut microbe and its relationship with the host. We argue that to symbiosis as an umbrella term for mutualistic, commensal, or a mechanistic understanding of the microbial symbiosis in the ver- parasitic relationships, including all of the interactions for which the tebrate gut and its evolution will be important to determine how full spectrum of effects on the host is simply not known. Using the this relationship can go awry, and it may reveal possibilities by term in this context is appropriate when referring to individual which the gut microbiome can be manipulated to support health. members of the gut microbiota because there is currently no sci- entific consensus on which microbial taxa constitute the mutualistic vertebrate symbiont | microbiota | mutualism and pathogenic components within this community. Although many scientists have attempted to make such categorizations, they rokaryotic microorganisms arose more than 3 billion y ago remain hypothetical (and indeed difficult to prove). One has also to Pand have diversified to occupy virtually all environments that consider that symbiotic relationships in the vertebrate gut exist on became available. Multicellular eukaryotes appeared later, and a continuum between mutualism and parasitism dependent on the their bodies provided new habitats for microbial exploitation. host’s genetic background and environmental factors. The net ef- The microbial communities that inhabit the digestive tracts of fect of the gut microbiota, however, is beneficial, and of critical vertebrates are especially impressive both in sheer number and importance for vertebrate biology. complexity. The largest populations are found in the digestive Gut microbes were pivotal in the emergence of herbivorous tracts of mammals, which can contain 1010 to 1012 cells/mL (e.g., lifestyles in mammals and birds (12). Vertebrate genomes harbor a in the rumen and large intestines), the highest cell numbers very limited repertoire of glycosylhydrolases, and it is the microbes recorded for any known microbial ecosystem (1). These com- that confer metabolic traits to extract energy from the fibrous munities are comprised of thousands of species, and their di- portion of plants, such as leaves, petioles, and stems (13). The versity and metabolic capacity is specific for a particular host energy contributions through microbial metabolism, which are to animal and gut segment. Technical advances in the molecular a large degree through the provision of short chain fatty acids characterization of the gut microbiota and work with animal (SCFA), is significant in many vertebrate species, ranging from models have begun to provide insight into the diversity of these ≈70% in ruminants, 20–30% for several omnivorous animals, and communities and their interactions with the host (2–6). Although 10% for humans (14). Another important attribute conferred by most gut microbes are not pathogenic, it is now widely appreci- the gut microbiota is the capacity to prevent enteric disease by ated that they are of significant importance for the health and pathogenic microorganisms, a trait referred to as colonization re- performance of their vertebrate host (7, 8). To gain a deeper understanding of the microbial populations in the vertebrate digestive tract and their interactions with the host, This paper results from the Arthur M. Sackler Colloquium of the National Academy of it is instructive to consider the biological principles that underlie Sciences, "Microbes and Health," held November 2–3, 2009, at the Arnold and Mabel these partnerships in an evolutionary context. In this review, we Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. fi The complete program and audio files of most presentations are available on the NAS will attempt such an approach by rst discussing the basic char- Web site at http://www.nasonline.org/SACKLER_Microbes_and_Health. acteristics of microbial symbiosis in the vertebrate gut before we Author contributions: S.R. designed research; S.R. performed research; S.R. analyzed data; use findings obtained with the Gram-positive bacterium Lacto- and J.W., R.A.B., and S.R. wrote the paper. bacillus reuteri as a paradigm to gain insight into the ecology, The authors declare no conflict of interest. evolution, and biological role of vertebrate gut microbes. This article is a PNAS Direct Submission. Symbiosis with Trillions of Partners Data deposition: The sequences reported in this paper have been deposited in the Gen- Bank database (accession nos. GU563996, GU563997, GU563998, GU563999, GU564000, At birth, the vertebrate digestive tract is sterile but becomes GU564001, GU564002, GU564003, and GU564004). rapidly colonized by a microbial population that, after a period of 1To whom correspondence should be addressed. E-mail: [email protected]. fl initial uctuations, remains remarkably stable and resilient over This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. time (9). This relationship can be referred to as symbiosis (from 1073/pnas.1000099107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1000099107 PNAS | March 15, 2011 | vol. 108 | suppl. 1 | 4645–4652 Downloaded by guest on September 24, 2021 sistance or microbial interference (9, 15). Vertebrate gut microbes ing. This process could be highly relevant in the evolution of further contribute to epithelial barrier function, the provision mutualism, because the majority of evolutionary changes within an of vitamins, detoxification of xenobiotic compounds, angiogenesis, organism are selectively neutral (32). The host could then further and the development and maturation of the immune system (7). select actively, through its adaptive immune functions or the The significant benefits provided by the gut microbiota demon- evolution of specific attachment sites, for beneficial microbes (21). strate that it is conceptually questionable to dismiss this symbiosis The evolutionary process described herein would result in as mere commensalism. a win-win situation in which the host provides the habitat for gut microbes (which are often extremely rare in the environment) To Live and Let Live: The Evolution of Mutualism while the microbes provide benefits such as access to fibrous diets In symbiotic relationships, selection pressure on the host has the and prevention of enteric infections (13, 15). Unfortunately, we potential to lead to the improvement of beneficial traits in both have no empirical data on the evolutionary outcomes of verte- partners (11). Such mutualistic relationships are extremely well brate symbiosis in terms of measurable fitness benefits for the understood in vertically transmitted symbionts of insects, such as host. Research with gnotobiotic animals has provided clear evi- Buchnera aphidicola in aphids (16). These symbionts have been dence for the significant contributions of the microbiota to colo- stably associated with their host species over evolutionary time, nization resistance and nutrient utilization (2, 15), but we do not as indicated by concurrent phylogenetic trees (17–20). In most know to what degree these attributes are adaptive or coincidental. cases, the microbes produce essential nutrients for the insects, We also lack a general theory about the ecological and evolu- whereas the latter have evolved specialized cells or organs to house tionary factors that favor mutualism in gut ecosystems. In other them and to
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