Environmental and gut bacteroidetes: the food connection

Abstract

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.

Figure 1

Schematic diagram representing the total number of coded proteins as a function of genome size of Bacteroidetes species. Only complete and published genomes of the Bacteroidetes phylum have been included (see also Table 2).

Figure 2

Schematic representation of a PUL region, present in the genome of Bacteroides plebeius and first identified as interesting because of the presence of a porphyranase gene (Bp1689; Hehemann et al., 2010). Besides the conserved Sus-like genes, the locus also contains carbohydrate-related genes which share highest identity with proteins used for red algal galactan degradation in two marine Bacteroides. Shown are the sequence identities between B. plebeius and one Microscilla sp. PRE1 protein, as well as with several Zobellia galactanivorans proteins. Six of these genes (Bp1670, Bp1671, Bp1689, Bp1693, Bp1694, and Bp1696) are conserved only with marine bacteria, and are absent in genomes of other gut Bacteroides. The crystal structures of marine homologous enzymes, coded by three of these genes (namely Bp1670, Bp1671, and Bp1689) have recently been determined and are illustrated as ribbon representations (PDB codes: AgaB – 1O4Z; AghA – 3P2N; and PorA – 3ILF). The 3D structures help determine the crucial residues for activity and substrate specificity that are all verified and present in the sequences of the B. plebeius proteins.