Environmental and gut Bacteroidetes: the food connection

Review Article published: 30 May 2011 doi: 10.3389/fmicb.2011.00093 Environmental and gut Bacteroidetes: the food connection François Thomas1,2, Jan-Hendrik Hehemann1,2†, Etienne Rebuffet1,2†, Mirjam Czjzek1,2 and Gurvan Michel 1,2* 1 2 UMR 7139, Marine Plants and Biomolecules, Station Biologique de Roscoff, UPMC University Paris 6, Roscoff, France UMR 7139, CNRS, Marine Plants and Biomolecules, Station Biologique de Roscoff, Roscoff, France Edited by: Peter J. Turnbaugh, Harvard University, USA Reviewed by: Deborah Threadgill, North Carolina State University, USA Alain Stintzi, Ottawa Institute of Systems Biology, Canada *Correspondence: Gurvan Michel, UMR 7139, CNRS/ UPMC, Marine Plants and Biomolecules, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France. e-mail: Current address: Jan-Hendrik Hehemann, Department of Biochemistry and Microbiology, University of Victoria, PO Box 3055 STN CSC, Victoria, BC, Canada V8W 3PG; Etienne Rebuffet, Department of Chemistry, Biochemistry and Biophysics, University of Gothenburg, Box 462, SE-405 30 Göteborg, Sweden. † Members of the diverse bacterial phylum Bacteroidetes have colonized virtually all types of habitats on Earth. They are among the major members of the microbiota of animals, especially in the gastrointestinal tract, can act as pathogens and are frequently found in soils, oceans and freshwater. In these contrasting ecological niches, Bacteroidetes are increasingly regarded as specialists for the degradation of high molecular weight organic matter, i.e., proteins and carbohydrates. This review presents the current knowledge on the role and mechanisms of polysaccharide degradation by Bacteroidetes in their respective habitats. The recent sequencing of Bacteroidetes genomes confirms the presence of numerous carbohydrate-active enzymes covering a large spectrum of substrates from plant, algal, and animal origin. Comparative genomics reveal specific Polysaccharide Utilization Loci shared between distantly related members of the phylum, either in environmental or gut-associated species. Moreover, Bacteroidetes genomes appear to be highly plastic and frequently reorganized through genetic rearrangements, gene duplications and lateral gene transfers (LGT), a feature that could have driven their adaptation to distinct ecological niches. Evidence is accumulating that the nature of the diet shapes the composition of the intestinal microbiota. We address the potential links between gut and environmental bacteria through food consumption. LGT can provide gut bacteria with original sets of utensils to degrade otherwise refractory substrates found in the diet. A more complete understanding of the genetic gateways between food-associated environmental species and intestinal microbial communities sheds new light on the origin and evolution of Bacteroidetes as animals’ symbionts. It also raises the question as to how the consumption of increasingly hygienic and processed food deprives our microbiota from useful environmental genes and possibly affects our health. Keywords: Bacteroidetes, adaptation to environmental niches, microbiota The phylum Bacteroidetes The phylum Bacteroidetes is a very diverse bacterial phylum, the name of which changed several times over the past years. It is also known as the Cytophaga–Flexibacter–Bacteroides (CFB) group, an appellation that reflects the diversity of organisms found in this phylogenetic group (Woese, 1987; Woese et al., 1990). According to the Bergey’s Manual of Systematic Bacteriology (Bergey’s, 2011), the Bacteroidetes phylum comprises four classes: Bacteroidia, Flavobacteria, Sphingobacteria, and Cytophagia, representing around 7000 different species (NCBI, October 2010). The largest class is the Flavobacteria, grouping together around four times more species than the three others (Table 1). These bacteria are all Gram negative, cover a mixture of physiological types, from strictly anaerobic Bacteroides to strictly aerobic Flavobacteria. They are non-motile, flagellated, or move by gliding. Members of the phylum Bacteroidetes have colonized many different ecological niches, including soil, ocean, freshwater, and the gastrointestinal tract (GIT) of animals, where they display various biological functions. In particular, they are well known degraders of polymeric organic matter. This review describes current knowledge on the role and mechanisms of polysaccharide degradation by Bacteroidetes in their respective habitats. We emphasize the features shared by members of the phylum that allow this www.frontiersin.org functional specialization in various environments. We address the links between these different microbial communities through food consumption, which raise the question of the evolution of gut microbes. Bacteroidetes in the normal microbiota of animals Microbes that live in and on humans (known as microbiota) can represent up to 100 trillion cells, 10 times more than the eukaryotic stem and somatic cells (Ley et al., 2006b; Turnbaugh et al., 2007). The large majority of these microbes reside in our GIT, and belong either to the Firmicutes or Bacteroidetes phyla (Marchesi, 2010). In fact, these two bacterial phyla account for >98% of the 16S rRNA sequences detected in the gut microbiota of mammals (Ley et al., 2006b). Bacteroidetes have colonized all the different parts of the GIT, despite the different conditions they have to face in terms of, e.g., pH, nutrients, and oxygen availability. Due to their easier accessibility, the mouth and colon microbiota have been the most studied. The large intestine is the most colonized compartment of the GIT, with bacterial densities reaching 1011–1012 cells/ml (Whitman et al., 1998). Members of the Bacteroidetes phylum are well known colonizers of the colon. They account for about 50% of the 16S rRNA sequences detected from healthy human mucosal tissues (Eckburg et al., 2005). Among this phylum, members of the genus Bacteroides May 2011 | Volume 2 | Article 93 | 1 Thomas et al. Linking environmental and gut Bacteroidetes Table 1 | Census of the phylogenetic divisions inside the Bacteroidetes phylum (NCBI, October 2010). Class No. of families No. of genera No. of species Bacteroidia 5 28 858 Flavobacteria 3 110 3583 Sphingobacteria 3 29 787 Cytophagia 3 47 765 Unclassified strains – – 996 are the most abundantly represented in the fecal microbiota (Moore and Holdeman, 1974; Sghir et al., 2000). Bacteroidetes have also been found in the normal microbiota of the oral cavity, either in the saliva or dental plaque (Keijser et al., 2008; Nasidze et al., 2009a,b). In the throat, Andersson et al. (2008) found that Bacteroidetes account for ∼20% of the reads using barcoding pyrosequencing, and identified Prevotella genus as the second most represented after Streptococcus. The same proportions were found in the distal esophagus (Pei et al., 2004). Due to its low pH, the stomach is a harsh eco (...truncated)