title: Characterization of the first alginolytic operons in a marine bacterium: from their emergence in marine Flavobacteriia to their independent transfers to marine Proteobacteria and human gut Bacteroides.
abstract: Alginate constitutes a significant part of seaweed biomass and thus a crucial nutrient for numerous marine heterotrophic bacteria. However, the mechanisms for alginate assimilation remain largely unknown in marine microorganisms. We show here that the genome of the marine flavobacterium Zobellia galactanivorans contains seven putative alginate lyase genes, five of them localized within two clusters comprising additional carbohydrate-related genes. The transcription of these genes and the alginolytic activity were strongly induced when Z. galactanivorans used alginate as sole carbon source. These clusters were shown to be transcribed as polycistronic mRNAs and thus to constitute operons. Several candidate enzymes were successfully overexpressed in Escherichia coli, purified and their activity tested. Particularly, AlyA1, AlyA4, AlyA5 and AlyA7 are confirmed as active alginate lyases. Zg2622 and Zg2614 are a dehydrogenase and a kinase, respectively, further converting the terminal unsaturated monosaccharides released by alginate lyases into 2-keto-3-deoxy-6-phosphogluconate. In-depth phylogenomic analyses reveal that such alginolytic operons originated from an ancestral marine flavobacterium and were independently transferred to marine proteobacteria and Japanese gut Bacteroides. These bacteria thus gained the capacity to assimilate the main polysaccharide of brown algae, an adaptive advantage in coastal environments but also in the gut microbiota of specific human population.
authors.affiliation: UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France.
authors.forename: François
authors.initials: F
authors.lastname: Thomas
authors.forename: Tristan
authors.initials: T
authors.lastname: Barbeyron
authors.forename: Thierry
authors.initials: T
authors.lastname: Tonon
authors.forename: Sabine
authors.initials: S
authors.lastname: Génicot
authors.forename: Mirjam
authors.initials: M
authors.lastname: Czjzek
authors.forename: Gurvan
authors.initials: G
authors.lastname: Michel
mesh_terms: D000464:Alginates / Q000378:metabolism*; D000595:Amino Acid Sequence; D001419:Bacteria / Q000145:classification / Q000201:enzymology* / Q000235:genetics*; D001439:Bacteroides / Q000201:enzymology / Q000235:genetics; D004783:Environmental Microbiology; D041965:Flavobacteriaceae / Q000201:enzymology / Q000235:genetics; D020723:Glucuronic Acid / Q000378:metabolism; D006603:Hexuronic Acids / Q000378:metabolism; D006801:Humans; D007422:Intestines / Q000382:microbiology; D008969:Molecular Sequence Data; D005810:Multigene Family / Q000235:genetics; D009876:Operon / Q000235:genetics*; D010802:Phylogeny; D011133:Polysaccharide-Lyases / Q000235:genetics*; D020560:Proteobacteria / Q000201:enzymology / Q000235:genetics; D059467:Transcriptome
chemical_list: D000464:Alginates; D006603:Hexuronic Acids; D020723:Glucuronic Acid; D011133:Polysaccharide-Lyases; C016158:poly(beta-D-mannuronate) lyase