Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria

Elizabeth Ficko-Blean, Aurélie Préchoux, François Thomas, Tatiana Rochat, Robert Larocque, Yongtao Zhu, Mark Stam, Sabine Génicot, Murielle Jam, Alexandra Calteau, Benjamin Viart, David Ropartz, David Pérez-Pascual, Gaëlle Correc, Maria Matard-Mann, Keith A. Stubbs, Hélène Rogniaux, Alexandra Jeudy, Tristan Barbeyron, Claudine Médigue, Mirjam Czjzek, David Vallenet, Mark J. McBride, Eric Duchaud and Gurvan Michel ()
Additional contact information
Elizabeth Ficko-Blean: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Aurélie Préchoux: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
François Thomas: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Tatiana Rochat: Université Paris-Saclay
Robert Larocque: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Yongtao Zhu: University of Wisconsin-Milwaukee
Mark Stam: Université Évry-Val-d’Essonne, CEA, Institut de Génomique - Genoscope, Laboratoire d’Analyses Bioinformatiques pour la Génomique et le Métabolisme
Sabine Génicot: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Murielle Jam: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Alexandra Calteau: Université Évry-Val-d’Essonne, CEA, Institut de Génomique - Genoscope, Laboratoire d’Analyses Bioinformatiques pour la Génomique et le Métabolisme
Benjamin Viart: Université Évry-Val-d’Essonne, CEA, Institut de Génomique - Genoscope, Laboratoire d’Analyses Bioinformatiques pour la Génomique et le Métabolisme
David Ropartz: UR1268 Biopolymers Interactions Assemblies
David Pérez-Pascual: Université Paris-Saclay
Gaëlle Correc: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Maria Matard-Mann: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Keith A. Stubbs: The University of Western Australia
Hélène Rogniaux: UR1268 Biopolymers Interactions Assemblies
Alexandra Jeudy: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Tristan Barbeyron: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
Claudine Médigue: Université Évry-Val-d’Essonne, CEA, Institut de Génomique - Genoscope, Laboratoire d’Analyses Bioinformatiques pour la Génomique et le Métabolisme
Mirjam Czjzek: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff
David Vallenet: Université Évry-Val-d’Essonne, CEA, Institut de Génomique - Genoscope, Laboratoire d’Analyses Bioinformatiques pour la Génomique et le Métabolisme
Mark J. McBride: University of Wisconsin-Milwaukee
Eric Duchaud: Université Paris-Saclay
Gurvan Michel: UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff

Nature Communications, 2017, vol. 8, issue 1, 1-17

Abstract: Abstract Macroalgae contribute substantially to primary production in coastal ecosystems. Their biomass, mainly consisting of polysaccharides, is cycled into the environment by marine heterotrophic bacteria using largely uncharacterized mechanisms. Here we describe the complete catabolic pathway for carrageenans, major cell wall polysaccharides of red macroalgae, in the marine heterotrophic bacterium Zobellia galactanivorans. Carrageenan catabolism relies on a multifaceted carrageenan-induced regulon, including a non-canonical polysaccharide utilization locus (PUL) and genes distal to the PUL, including a susCD-like pair. The carrageenan utilization system is well conserved in marine Bacteroidetes but modified in other phyla of marine heterotrophic bacteria. The core system is completed by additional functions that might be assumed by non-orthologous genes in different species. This complex genetic structure may be the result of multiple evolutionary events including gene duplications and horizontal gene transfers. These results allow for an extension on the definition of bacterial PUL-mediated polysaccharide digestion.

Date: 2017
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DOI: 10.1038/s41467-017-01832-6

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