Abstract
In bacteria from the phylum Bacteroidetes, the genes coding for enzymes involved in polysaccharide degradation are often colocalized and coregulated in so-called “polysaccharide utilization loci” (PULs). PULs dedicated to the degradation of marine polysaccharides (e.g. laminaran, ulvan, alginate and porphyran) have been characterized in marine bacteria. Interestingly, the gut microbiome of Japanese individuals acquired, by lateral transfer from marine bacteria, the genes involved in the breakdown of porphyran, the cell wall polysaccharide of the red seaweed used in maki. Sequence similarity analyses predict that the human gut microbiome also encodes enzymes for the degradation of alginate, the main cell wall polysaccharide of brown algae. We undertook the functional characterization of diverse polysaccharide lyases from family PL17, frequently found in marine bacteria as well as those of human gut bacteria. We demonstrate here that this family is polyspecific. Our phylogenetic analysis of family PL17 reveals that all alginate lyases, which have all the same specificity and mode of action, cluster together in a very distinct subfamily. The alginate lyases found in human gut bacteria group together in a single clade which is rooted deeply in the PL17 tree. These enzymes were found in PULs containing PL6 enzymes, which also clustered together in the phylogenetic tree of PL6. Together, biochemical and bioinformatics analyses suggest that acquisition of this system appears ancient and, because only traces of two successful transfers were detected upon inspection of PL6 and PL17 families, the pace of acquisition of marine polysaccharide degradation system is probably very slow.
Highlights
The high complexity of polysaccharides arises from the stereochemical diversity of their constitutive monosaccharide residues and from the many ways to assemble these residues through glycosidic bonds
The phylogenetic tree computed from the alignment of the catalytic modules of 272 PL17 sequences shows a clear division into two main clades (Fig. 1)
The phylogenetic analysis of family PL17 suggests the ancient acquisition of alginate lyase genes by the human gut microbiome
Summary
The high complexity of polysaccharides arises from the stereochemical diversity of their constitutive monosaccharide residues and from the many ways to assemble these residues through glycosidic bonds. In bacteria belonging to phylum Bacteroidetes, genes involved in the degradation of a given polysaccharide are often clustered on the genome and coregulated These gene clusters have been termed “polysaccharide utilization loci” (PULs)[12,13]. Porphyranases are glycoside hydrolases that belong to the polyspecific GH16 family, which contains agarases and carrageenases and other enzymes for the degradation of red algal polysaccharides. Phylogenetic analyses of family GH16 show that the porphyranase clade groups with both marine and gut Bacteroidetes and shares a common ancestor with agarases and carrageenases[23]. These results highlight the plasticity of the gut microbiome and its ability to adapt to diet. The frequency of acquisition of a novel gene introduced by diet and the mechanisms of adaptation to diet remain obscure
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