Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes

Abstract

Humans host an intestinal population of microbes—collectively referred to as the gut microbiome—which encode the carbohydrate active enzymes, or CAZymes, that are absent from the human genome. These CAZymes help to extract energy from recalcitrant polysaccharides. The question then arises as to if and how the microbiome adapts to new carbohydrate sources when modern humans change eating habits. Recent metagenome analysis of microbiomes from healthy American, Japanese, and Spanish populations identified putative CAZymes obtained by horizontal gene transfer from marine bacteria, which suggested that human gut bacteria evolved to degrade algal carbohydrates—for example, consumed in form of sushi. We approached this hypothesis by studying such a polysaccharide utilization locus (PUL) obtained by horizontal gene transfer by the gut bacterium Bacteroides plebeius . Transcriptomic and growth experiments revealed that the PUL responds to the polysaccharide porphyran from red algae, enabling growth on this carbohydrate but not related substrates like agarose and carrageenan. The X-ray crystallographic and biochemical analysis of two proteins encoded by this PUL, BACPLE_01689 and BACPLE_01693 , showed that they are β-porphyranases belonging to glycoside hydrolase families 16 and 86, respectively. The product complex of the GH86 at 1.3 Å resolution highlights the molecular details of porphyran hydrolysis by this new porphyranase. Combined, these data establish experimental support for the argument that CAZymes and associated genes obtained from extrinsic microbes add new catabolic functions to the human gut microbiome.

Polysaccharide Utilization Loci: Fueling Microbial Communities

“…The dynamic effects of the human diet on the adaptive evolution of the distal gut microbiota were recently highlighted in the seminal "sushi factor" study, which documented the presence of ␤-porphyranases (i.e., GH16 and GH86), algal polysaccharide-specific CAZymes, in the microbiota of Japanese populations (113). Notably, these CAZymes were found as part of PULs thought to be acquired by the gut bacterium Bacteroides plebeius via lateral gene transfer from porphyranolytic Z. galactanivorans associated with uncooked edible algae (i.e., nori) (114). Further evidence suggests that B. plebeius and other human gut Bacteroides spp.…”

“…Further evidence suggests that B. plebeius and other human gut Bacteroides spp. may have also acquired algal polysaccharide utilization genes from marine bacteria (108,114).…”

Isolation and characterization of an Antarctic Flavobacterium strain with agarase and alginate lyase activities

“…Genomes from this phylum appear to be highly plastic with frequent genetic rearrangements that suggest their adaptation to distinct and specific environmental conditions (Thomas et al 2011). Thus, similar to the acquisition of genes coding for porphyranases and agarases by some human gut bacteria as reported by Hehemann et al (2010Hehemann et al ( , 2012, this could also happen in flavobacteria associated with algal surfaces. Nevertheless, the presence of agar or alginate lyase activity per se cannot be used as a phylogenetic character in this group.…”

“…S20, the agar lyase activity is present only in strain INACH002 and F. faecale, while the alginate lyase is present in all taxa except for F. faecale. It is well known that the phylum Bacteroidetes can obtain the capability to degrade algal carbohydrates by lateral gene transfer (LGT) from other marine bacteria (Thomas et al 2011;Touchon et al 2011;Hehemann et al 2012;Thomas et al 2012). Genomes from this phylum appear to be highly plastic with frequent genetic rearrangements that suggest their adaptation to distinct and specific environmental conditions (Thomas et al 2011).…”

Draft Genome Sequence of the Agarase-Producing Sphingomonas sp. MCT13

“…BSi20429, and 53% identity with an hypothetical agarase from Gilvimarinus agarilyticus (Lee et al, 2015), respectively. Interestingly, ODP38961.1 and ODP36570.1 displayed also 48 and 53% protein identity, respectively, with a previously characterized exo-beta-agarase (Accession number 4BQ2_A) from the marine bacterium Saccharophagus degradans (Pluvinage et al, 2013), while ODP36587.1 displayed also a 31% identity with a beta-porphyranase identified in the gut bacterium Bacteroides plebeius (Hehemann et al, 2012). Further work is currently ongoing to characterize these enzymes.…”