“Transfer of Carbohydrate-Active Enzymes from Marine Bacteria to Japanese Gut Microbiota”, 2010-04-08 ():
Gut microbes supply the human body with energy from dietary polysaccharides through carbohydrate active enzymes, or CAZymes1, which are absent in the human genome. These enzymes target polysaccharides from terrestrial plants that dominated diet throughout human evolution2. The array of CAZymes in gut microbes is highly diverse, exemplified by the human gut symbiont Bacteroides thetaiotaomicron3, 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 usage1,4.
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 individuals5. Our comparative gut metagenome analyses show that porphyranases and agarases are frequent in the Japanese population6 and that they are absent in metagenome data7 from North American individuals. Seaweeds make an important contribution to the daily diet in Japan (14.2g per person per day)8, and Porphyra spp. (nori) is the most important nutritional seaweed, traditionally used to prepare sushi9,10.
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.
The sushi factor: One of the useful roles performed by the human gut microbiota is to supply digestive enzymes missing from the human genome. For instance, polysaccharides from the terrestrial plants that have been part of the human diet throughout evolution are broken down in the gut by carbohydrate active enzymes, or CAZymes, many of them highly specific enzymes from Bacteroides spp. bacteria. Little is known about the gut enzymes acting on edible marine algae such as nori, sea lettuce and wakame, common in Japanese cuisine. Now CAZymes able to digest sulphated polysaccharides from Porphyra sp. marine red algae have been identified in marine Bacteroides isolates. And surprisingly, genome data mining reveals that this enzyme is present in gut bacteria from Japanese—but not American—individuals. This demonstrates that the gene transfer has taken place—recently in evolutionary terms—from a marine environmental bacterium to the Japanese gut bacterium Bacteroides plebeius. Porphyra are otherwise known as nori and used traditionally in sushi, so it seems probable that contact with non-sterile food may be a general factor in stocking gut microbes with a varied arsenal of CAZymes.