The Cultivable Surface Microbiota of the Brown Alga Ascophyllum nodosum is Enriched in Macroalgal-Polysaccharide-Degrading Bacteria

Abstract

Bacteria degrading algal polysaccharides are key players in the global carbon cycle and in algal biomass recycling. Yet the water column, which has been studied largely by metagenomic approaches, is poor in such bacteria and their algal-polysaccharide-degrading enzymes. Even more surprisingly, the few published studies on seaweed-associated microbiomes have revealed low abundances of such bacteria and their specific enzymes. However, as macroalgal cell-wall polysaccharides do not accumulate in nature, these bacteria and their unique polysaccharidases must not be that uncommon. We, therefore, looked at the polysaccharide-degrading activity of the cultivable bacterial subpopulation associated with Ascophyllum nodosum. From A. nodosum triplicates, 324 bacteria were isolated and taxonomically identified. Out of these isolates, 78 (~25%) were found to act on at least one tested algal polysaccharide (agar, ι- or κ-carrageenan, or alginate). The isolates “active” on algal-polysaccharides belong to 11 genera: Cellulophaga, Maribacter, Algibacter, and Zobellia in the class Flavobacteriia (41) and Pseudoalteromonas, Vibrio, Cobetia, Shewanella, Colwellia, Marinomonas, and Paraglaceciola in the class Gammaproteobacteria (37). A major part represents likely novel species. Different proportions of bacterial phyla and classes were observed between the isolated cultivable subpopulation and the total microbial community previously identified on other brown algae. Here, Bacteroidetes and Gammaproteobacteria were found to be the most abundant and some phyla (as Planctomycetes and Cyanobacteria) frequently encountered on brown algae weren't identified. At a lower taxonomic level, twelve genera, well-known to be associated with algae (with the exception for Colwellia), were consistently found on all three A. nosodum samples. Even more interesting, 9 of the 11 above mentioned genera containing polysaccharolytic isolates were predominant in this common core. The cultivable fraction of the bacterial community associated with A. nodosum is, thus, significantly enriched in macroalgal-polysaccharide-degrading bacteria and these bacteria seem important for the seaweed holobiont even though they are under-represented in alga-associated microbiome studies.

Deterministic influences exceed dispersal effects on hydrologically‐connected microbiomes

“…Microbiomes with a diverse community of Proteobacteria may therefore be well‐adapted to fluctuations in organic C availability, facilitating their persistence across all zones. Moreover, Bacteriodetes has been shown to be prevalent in both waterborne and biofilm microbiomes in other systems – preferentially degrading recalcitrant C compounds and recycling biomass (Cottrell and Kirchman, ; Martin et al ., ; Bennke et al ., ). The presence of Bacteroidetes in addition to Proteobacteria within nearshore and river microbiomes may therefore indicate niche complementarity within these higher‐C environments, possibly coincident with spatial organization that is not captured in our measurements.…”

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

“…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).…”

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

“…Most strains were isolated from algae where interactions might range from symbiosis with green seaweeds (Matsuo et al, 2005) to algicidal behaviour towards dinoflagellates (Skerratt et al, 2002). Recent studies indicate that Zobellia strains are an integral part of the core microbiota of healthy seaweeds (Hahnke and Harder, 2013;Hollants et al, 2013;Martin et al, 2015;Marzinelli et al, 2015).…”