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

• Published in: Nature (London) 2010-04, Vol.464 (7290), p.908-912
• Main Authors: Hehemann, Jan-Hendrik, Correc, Gaëlle, Barbeyron, Tristan, Helbert, William, Czjzek, Mirjam, Michel, Gurvan
• Format: Article
• Language: English
• Subjects: 631/326/41/2535; 631/45/173; 631/45/72/1205; 692/698/2741/2135; Adaptation, Physiological - physiology; Anaerobic bacteria; Animal, plant and microbial ecology; Bacteria; Bacteroides - enzymology; Bacteroides - genetics; Biological and medical sciences; Biological Evolution; Carrageenin; Crystallography, X-Ray; Cultural Diversity; Diet; E coli; Enzymes; Eukaryota - chemistry; Eukaryota - metabolism; Feces - enzymology; Feces - microbiology; Food Microbiology; Fundamental and applied biological sciences. Psychology; Gene Transfer, Horizontal; Genome, Bacterial - genetics; Glycoside Hydrolases - chemistry; Glycoside Hydrolases - isolation & purification; Glycoside Hydrolases - metabolism; Human genome; Humanities and Social Sciences; Humans; Interpretation and construction; Intestines - microbiology; Japan; letter; Marine Biology; Membrane proteins; Metagenome; Microbial ecology; Microbiology; Microbiota (Symbiotic organisms); Models, Molecular; multidisciplinary; Natural history; Normal microflora of man and animals. Rumen; North America; Phylogeny; Porphyra - chemistry; Porphyra - metabolism; Porphyra - microbiology; Properties; Protein Conformation; Proteins; Science; Sepharose - analogs & derivatives; Sepharose - chemistry; Sepharose - metabolism; Substrate Specificity
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature08937

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. One of the roles of the human gut microbiota is to break down nutrients using bacterial enzymes that are lacking from the human genome. It is now shown that the gut microbiota of Japanese, but not American, individuals contains porphyranases, enzymes that digest sulphated polysaccharides which are present in the marine environment only. These findings indicate that diet can select for gene content of the human microbiota. Gut microbes supply the human body with energy from dietary polysaccharides through carbohydrate active enzymes, or CAZymes 1 , which are absent in the human genome. These enzymes target polysaccharides from terrestrial plants that dominated diet throughout human evolution 2 . The array of CAZymes in gut microbes is highly diverse, exemplified by the human gut symbiont Bacteroides thetaiotaomicron 3 , 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 1 , 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 galactanivora