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

Nature volume 464, pages 908–912 (2010)Cite this article

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Abstract

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 utilization1,4. 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 (14.2 g 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.

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Figure 1: Activity screening on natural algal polysaccharides reveals porphyranase activity.
Figure 2: Structural determinants of porphyran active enzymes.
Figure 3: Phylogenetic analysis of GH16 galactanases reveals porphyranases in many marine bacteria and in the Japanese gut bacterium B. plebeius.
Figure 4: Upstream and downstream of the porphyranase gene ( Bp1689 ), the genome of B. plebeius contains carbohydrate-related genes that share highest identity with proteins used for red-algal galactan degradation in two marine Bacteroidetes.

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Primary accessions

Protein Data Bank

Data deposits

Atomic coordinates and structure factors have been deposited at the Protein Data Bank under accession codes 3ILF (PorA_E139S) and 3JUU (PorB).

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Acknowledgements

We thank B. Kloareg and C. de Vargas for critical discussions and reading of the manuscript and M. Jam, A. Jeudy and D. Freudenreich for technical assistance. The ‘Marine Plants and Biomolecules’ laboratory is funded by the French national research centre (Centre National de la Recherche Scientifique) and the University Marie Curie; J.-H.H. was supported by a European Marie Curie PhD grant; this work was also funded by the ‘Region Bretagne’ through the program Marine 3D. G.M. was supported by the GIS ‘Genomique Marine’ and the French Research Ministry (ACI Young Researcher). We thank the beamline scientists and staff at the European Synchrotron Radiation Facilities for technical support during data collections, the NMR Service, University Bretagne Occidentale, for access to the Bruker NMR spectrometer and Genoscope for sequencing the Z. galactanivorans genome.

Author Contributions J.-H.H. cloned, purified and crystallized the enzymes and extracted polysaccharides; J.-H.H. and M.C. collected data and solved the crystal structures; G.C. and J.-H.H. purified and characterized oligosaccharides; G.C. and W.H. performed the NMR analysis; G.M., T.B. and J.-H.H. performed the bioinformatic analysis; M.C., T.B., G.M. and J.-H.H. designed the study; J.-H.H., M.C. and G.M. analysed the data and wrote the paper. All authors discussed the results and commented on the manuscript.

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  1. Jan-Hendrik Hehemann

    Present address: Present address: Biochemistry and Microbiology, University of Victoria, PO Box 3055 STN CSC, Victoria, British Columbia V8W 3PG, Canada.,

Authors and Affiliations

  1. Université Pierre et Marie Curie, Paris 6,,

    Jan-Hendrik Hehemann, Gaëlle Correc, Tristan Barbeyron, William Helbert, Mirjam Czjzek & Gurvan Michel

  2. Centre National de la Recherche Scientifique, Végétaux marins et Biomolécules UMR 7139, Station Biologique de Roscoff, Roscoff F 29682, France ,

    Jan-Hendrik Hehemann, Gaëlle Correc, Tristan Barbeyron, William Helbert, Mirjam Czjzek & Gurvan Michel

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Correspondence to Mirjam Czjzek or Gurvan Michel.

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Hehemann, JH., Correc, G., Barbeyron, T. et al. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908–912 (2010). https://doi.org/10.1038/nature08937

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