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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

Authors

  • François Thomas,

    1. UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
    2. CNRS, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
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    • Present address: Biology Department, Woods Hole Oceanographic Institution, Wods Hole, MA, USA.

  • Tristan Barbeyron,

    1. UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
    2. CNRS, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
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  • Thierry Tonon,

    1. UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
    2. CNRS, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
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  • Sabine Génicot,

    1. UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
    2. CNRS, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
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  • Mirjam Czjzek,

    1. UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
    2. CNRS, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
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  • Gurvan Michel

    Corresponding author
    1. UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
    2. CNRS, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Brittany, France
      E-mail gurvan@sb-roscoff.fr; Tel. (+33) 298 29 23 30; Fax (+33) 298 29 23 24.
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E-mail gurvan@sb-roscoff.fr; Tel. (+33) 298 29 23 30; Fax (+33) 298 29 23 24.

Summary

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.

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