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About half of seaweed biomass is composed of polysaccharides. Most of these complex polymers have a marked polyanionic character. For instance, the red algal cell wall is mainly composed of sulfated galactans, agars and carrageenans, while brown algae contain alginate and fucose-containing sulfated polysaccharides (FCSP) as cell wall polysaccharides. Some marine heterotrophic bacteria have developed abilities to grow on such macroalgal polysaccharides. This is the case of Pseudoalteromonas carrageenovora 9T (ATCC 43555T), a marine gammaproteobacterium isolated in 1955 and which was an early model organism for studying carrageenan catabolism. We present here the genomic analysis of P. carrageenovora. Its genome is composed of two chromosomes and of a large plasmid encompassing 109 protein-coding genes. P. carrageenovora possesses a diverse repertoire of carbohydrate-active enzymes (CAZymes), notably specific for the degradation of macroalgal polysaccharides (laminarin, alginate, FCSP, carrageenans). We confirm these predicted capacities by screening the growth of P. carrageenovora with a large collection of carbohydrates. Most of these CAZyme genes constitute clusters located either in the large chromosome or in the small one. Unexpectedly, all the carrageenan catabolism-related genes are found in the plasmid, suggesting that P. carrageenovora acquired its hallmark capacity for carrageenan degradation by horizontal gene transfer (HGT). Whereas P. carrageenovora is able to use lambda-carrageenan as a sole carbon source, genomic and physiological analyses demonstrate that its catabolic pathway for kappa- and iota-carrageenan is incomplete. This is due to the absence of the recently discovered 3,6-anhydro-D-galactosidase genes (GH127 and GH129 families). A genomic comparison with 52 Pseudoalteromonas strains confirms that carrageenan catabolism has been recently acquired only in a few species. Even though the loci for cellulose biosynthesis and alginate utilization are located on the chromosomes, they were also horizontally acquired. However, these HGTs occurred earlier in the evolution of the Pseudoalteromonas genus, the cellulose- and alginate-related loci being essentially present in one large, late-diverging clade (LDC). Altogether, the capacities to degrade cell wall polysaccharides from macroalgae are not ancestral in the Pseudoalteromonas genus. Such catabolism in P. carrageenovora resulted from a succession of HGTs, likely allowing an adaptation to the life on the macroalgal surface.

Flavobacteriia are recognized as key players in the marine carbon cycle, due to their ability to efficiently degrade algal polysaccharides both in the open ocean and in coastal regions. The chemical complexity of algal polysaccharides, their differences between algal groups and variations through time and space, imply that marine flavobacteria have evolved dedicated degradation mechanisms and regulation of their metabolism during interactions with algae. In the present study, we report the first transcriptome-wide gene expression analysis for an alga-associated flavobacterium during polysaccharide degradation. Zobellia galactanivorans DsijT, originally isolated from a red alga, was grown in minimal medium with either glucose (used as a reference monosaccharide) or one selected algal polysaccharide from brown (alginate, laminarin) or red algae (agar, porphyran, ι- or κ-carrageenan) as sole carbon source. Expression profiles were determined using whole-genome microarrays. Integration of genomic knowledge with the automatic building of a co-expression network allowed the experimental validation of operon-like transcription units. Differential expression analysis revealed large transcriptomic shifts depending on the carbon source. Unexpectedly, transcriptomes shared common signatures when growing on chemically divergent polysaccharides from the same algal phylum. Together with the induction of numerous transcription factors, this hints at complex regulation events that fine-tune the cell behavior during interactions with algal biomass in the marine environment. The results further highlight genes and loci that may participate in polysaccharide utilization, notably encoding Carbohydrate Active enZymes (CAZymes) and glycan binding proteins together with a number of proteins of unknown function. This constitutes a set of candidate genes potentially representing new substrate specificities. By providing an unprecedented view of global transcriptomic responses during polysaccharide utilization in an alga-associated model flavobacterium, this study expands the current knowledge on the functional role of flavobacteria in the marine carbon cycle and on their interactions with algae.

Tenacibaculum maritimum is a devastating bacterial pathogen of wild and farmed marine fish with a broad host range and a worldwide distribution. We report here the complete genome sequence of the T. maritimum type strain NCIMB 2154T. The genome consists of a 3,435,971-base pair circular chromosome with 2,866 predicted protein-coding genes. Genes encoding the biosynthesis of exopolysaccharides, the type IX secretion system, iron uptake systems, adhesins, hemolysins, proteases, and glycoside hydrolases were identified. They are likely involved in the virulence process including immune escape, invasion, colonization, destruction of host tissues, and nutrient scavenging. Among the predicted virulence factors, type IX secretion-mediated and cell-surface exposed proteins were identified including an atypical sialidase, a sphingomyelinase and a chondroitin AC lyase which activities were demonstrated in vitro.