Habitat and taxon as driving forces of carbohydrate catabolism in marine heterotrophic bacteria: example of the model algae‐associated bacterium Zobellia galactanivorans Dsij^T

Abstract

The marine flavobacterium Zobellia galactanivorans Dsij was isolated from a red alga and by now constitutes a model for studying algal polysaccharide bioconversions. We present an in-depth analysis of its complete genome and link it to physiological traits. Z. galactanivorans exhibited the highest gene numbers for glycoside hydrolases, polysaccharide lyases and carbohydrate esterases and the second highest sulfatase gene number in a comparison to 125 other marine heterotrophic bacteria (MHB) genomes. Its genome contains 50 polysaccharide utilization loci, 22 of which contain sulfatase genes. Catabolic profiling confirmed a pronounced capacity for using algal polysaccharides and degradation of most polysaccharides could be linked to dedicated genes. Physiological and biochemical tests revealed that Z. galactanivorans stores and recycles glycogen, despite loss of several classic glycogen-related genes. Similar gene losses were observed in most Flavobacteriia, suggesting presence of an atypical glycogen metabolism in this class. Z. galactanivorans features numerous adaptive traits for algae-associated life, such as consumption of seaweed exudates, iodine metabolism and methylotrophy, indicating that this bacterium is well equipped to form profitable, stable interactions with macroalgae. Finally, using statistical and clustering analyses of the MHB genomes we show that their carbohydrate catabolism correlates with both taxonomy and habitat.

Genetic analyses unravel the crucial role of a horizontally acquired alginate lyase for brown algal biomass degradation by Zobellia galactanivorans

“…Examination of the genomic context of alyA1, its absence from the vast majority of Flavobacteriaceae possessing alginolytic PULs, and the phylogenies of homologs from distantly related bacteria suggested that alyA1 was recently acquired via HGT from marine Actinobacteria. Although Actinobacteria are not generally considered as major marine macroalgal polysaccharide degraders, a recent census of GHs and PLs in 126 genomes of marine heterotrophic bacteria (Barbeyron et al, 2016) showed that on average, marine actinobacterial genomes encoded 47 such enzymes (4 genomes available), which is comparable to the average 51 found in marine Bacteroidetes (21 genomes available). Therefore, the role of marine Actinobacteria in polysaccharide turnover may previously have been underestimated.…”

“…Zobellia strains are marine Bacteroidetes commonly associated with red, brown and green algae and are considered a normal component of the microbiota of healthy macroalgae (Hollants et al, 2013;Martin et al, 2015;Marzinelli et al, 2015). Zobellia galactanivorans was originally isolated from the red alga Delesseria sanguinea (Barbeyron et al, 2001) and exhibits impressive abilities to digest diverse algal polysaccharides (Barbeyron et al, 2016). Analysis of the Z. galactanivorans genome revealed 141 glycoside hydrolases (GHs), 15 polysaccharide lyases (PLs), 18 carbohydrate esterases and 72 sulfatases.…”

Polysaccharide Utilization Loci: Fueling Microbial Communities

“…The complexity of PULs often scales with that of their cognate substrates ( Fig. 1) (52,53) and may include ancillary enzymes such as proteases (54), sulfatases (55,56), and phosphatases (57). These elegant systems constitute the major nutrient acquisition strategy deployed by Bacteroidetes bacteria and thus are intrinsically linked to the colonization of nutritional niches and the establishment of microbial ecosystems.…”

“…For example, PULs from Zobellia galactanivorans (55), Formosa agariphila (56), and Gramella forsetii (101) contain CAZyme portfolios tuned to the unique monosaccharide residues of algal polysaccharides and, not surprisingly, are also enriched in sulfatases (see also SulfAtlas, a new sulfatase classification database from the Marine Glycobiology and ABiMS teams at the Station Biologique de Roscoff [102; http://abims.sb-roscoff.fr/sulfatlas/]).…”

Asp271 is critical for substrate interaction with the surface binding site in β‐agarase a from Zobellia galactanivorans

“…The marine bacterium Zobellia galactanivorans is a model organism for the increasingly recognized microbial conversion of algal biomass . The genome of Z. galactanivorans encodes four GH16 β‐agarases (EC 3.2.1.81), AgaA, AgaB, AgaC, and AgaD, which cleave internal β‐1,4‐galactosidic linkages in agarose producing agaro‐oligosaccharides (Figure ) .…”