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

Abstract

Comprehension of the degradation of macroalgal polysaccharides suffers from the lack of genetic tools for model marine bacteria, despite their importance for coastal ecosystem functions. We developed such tools for Zobellia galactanivorans, an algae-associated flavobacterium that digests many polysaccharides, including alginate. These tools were used to investigate the biological role of AlyA1, the only Z. galactanivorans alginate lyase known to be secreted in soluble form and to have a recognizable carbohydrate-binding domain. A deletion mutant, ΔalyA1, grew as well as the wild type on soluble alginate but was deficient in soluble secreted alginate lyase activity and in digestion of and growth on alginate gels and algal tissues. Thus, AlyA1 appears to be essential for optimal attack of alginate in intact cell walls. alyA1 appears to have been recently acquired via horizontal transfer from marine Actinobacteria, conferring an adaptive advantage that might benefit other algae-associated bacteria by exposing new substrate niches. The genetic tools described here function in diverse members of the phylum Bacteroidetes and should facilitate analyses of polysaccharide degradation systems and many other processes in these common but understudied bacteria.