Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota

Abstract

Gut microbes supply the human body with energy from dietary polysaccharides through carbohydrate active enzymes, or CAZymes, which are absent in the human genome. These enzymes target polysaccharides from terrestrial plants that dominated diet throughout human evolution. The array of CAZymes in gut microbes is highly diverse, exemplified by the human gut symbiont Bacteroides thetaiotaomicron, which contains 261 glycoside hydrolases and polysaccharide lyases, as well as 208 homologues of susC and susD-genes coding for two outer membrane proteins involved in starch utilization. A fundamental question that, to our knowledge, has yet to be addressed is how this diversity evolved by acquiring new genes from microbes living outside the gut. Here we characterize the first porphyranases from a member of the marine Bacteroidetes, Zobellia galactanivorans, active on the sulphated polysaccharide porphyran from marine red algae of the genus Porphyra. Furthermore, we show that genes coding for these porphyranases, agarases and associated proteins have been transferred to the gut bacterium Bacteroides plebeius isolated from Japanese individuals. Our comparative gut metagenome analyses show that porphyranases and agarases are frequent in the Japanese population and that they are absent in metagenome data from North American individuals. Seaweeds make an important contribution to the daily diet in Japan (14.2 g per person per day), and Porphyra spp. (nori) is the most important nutritional seaweed, traditionally used to prepare sushi. This indicates that seaweeds with associated marine bacteria may have been the route by which these novel CAZymes were acquired in human gut bacteria, and that contact with non-sterile food may be a general factor in CAZyme diversity in human gut microbes.

Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing

“…In the intestinal tract, Bacteroides spp. are versatile in hydrolyzing a broad array of polysaccharides (Shah and Gharbia, 1993), and a recent study has demonstrated that B. plebieus contains beta-agarases and beta-porphyranases capable of breaking down algal polysaccharides such as agar, carrageenan, laminarin and porphyrans (Hehemann et al, 2010). Given that MI consume seaweed as its only diet since speciation 10-20 M years ago, the higher abundance of Bacteroides spp.…”

Extensive Horizontal Gene Transfer in Cheese-Associated Bacteria

“…Advances in genome sequencing have begun to provide a glimpse into HGT within environmentally, medically and economically important microbiomes (McDaniel et al, 2010;Andam et al, 2015). For example, extensive gene sharing has been observed throughout the commensal human microbiome, including sharing of genes that enable nutrient acquisition from novel food sources (Hehemann et al, 2010;Smillie et al, 2011), and pathogenicity islands and antibiotic resistance genes in pathogenic microbes Hiramatsu et al, 2001;Forsberg et al, 2012). There is evidence of extensive HGT in other natural habitats, such as soil (Coombs and Barkay, 2004;Heuer and Smalla, 2012) and aquatic environments (McDaniel et al, 2010;Frischer et al, 1994).…”

Les Japonais et nous

“…Car la surface des algues est colonisée par des bactéries marines hétérotrophes qui entretiennent avec les algues des relations trophiques (commensalisme, saprophytisme) et dégradent, par exemple, divers polysaccharides sulfatés grâce à des CAZymes (enzymes carbohydrate actives). [2]. Grâce à une recherche dans des banques de données, de nombreuses  porphyranases ont été trouvées, provenant toutes de bactéries marines, ce qui est parfaitement logique puisque les porphyrases n'existent pas dans les plantes terrestres (➜).…”

“…Outre l'intérêt croissant des variations de flores intestinales selon l'alimentation, en particulier dans les études sur l'obésité [6], et l'exemplarité de l'alimentation nippone qui n'est sans doute pas pour rien dans la longévité des Japonais, ce travail laisse entrevoir l'incroyable réseau que les êtres vivants sont capables de tisser entre eux à travers le temps et l'espace. ‡ The Japanese and us 2 Ce n'est que vers l'époque de la restauration de Meiji, à la fin du XIX e siècle, que la consommation de viande fut permise, voire encouragée. …”