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

Elizabeth Ficko-Blean (1) , Aurelie Prechoux (1) , François Thomas (1) , Tatiana Rochat (2) , Robert Larocque (1) , Yongtao Zhu (3) , Mark Stam (4) , Sabine Génicot (1) , Murielle Jam (1) , Alexandra Calteau (4) , Benjamin Viart (4) , David Ropartz (5) , David Pérez-Pascual (2) , Gaëlle Correc (1) , Maria Matard-Mann (1) , Keith A Stubbs (6) , Hélène Rogniaux (5) , Alexandra Jeudy (7, 8) , Tristan Barbeyron (1) , Claudine Médigue (4) , Mirjam Czjzek (1) , David Vallenet (4) , Mark J Mcbride (3) , Éric Duchaud (2) , Gurvan Michel (1)

1 LBI2M - Laboratoire de Biologie Intégrative des Modèles Marins
2 VIM (UR 0892) - Unité de recherche Virologie et Immunologie Moléculaires
3 University of Wisconsin - Milwaukee
4 UMR 8030 - Génomique métabolique
5 BIA - Unité de recherche sur les Biopolymères, Interactions Assemblages
6 School of Molecular and Microbial Sciences
7 FR2424 - Fédération de recherche de Roscoff
8 SBR - Station biologique de Roscoff = Roscoff Marine Station

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.

Domains: Bacteriology; Biochemistry, Molecular Biology

Elizabeth Ficko-Blean, Aurelie Prechoux, François Thomas, Tatiana Rochat, Robert Larocque, et al.. Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria. Nature Communications, 2017, 8, pp.1685. ⟨10.1038/s41467-017-01832-6⟩. ⟨hal-01899178⟩