Widespread occurrence of chitinase-encoding genes suggests the Endozoicomonadaceae family as a key player in chitin processing in the marine benthos.

ABSTRACT

Chitin is the most abundant natural polymer in the oceans, where it is primarily recycled by chitin-degrading microorganisms. Endozoicomonadaceae (Oceanospirillales) bacteria are prominent symbionts of sessile marine animals, particularly corals, and presumably contribute to nutrient cycling in their hosts. To reveal the chitinolytic potential of this iconic, animal-dwelling bacterial family, we examined 42 publicly available genomes of cultured and uncultured Endozoicomonadaceae strains for the presence of chitinase-encoding genes. Thirty-two of 42 Endozoicomonadaceae genomes harbored endo-chitinase- (EC 3.2.1.14), 25 had exo-chitinase- (EC 3.2.1.52) and 23 polysaccharide deacetylase-encoding genes. Chitinases were present in cultured and uncultured Endozoicomonadaceae lineages associated with diverse marine animals, including the three formally described genera Endozoicomonas, Paraendozoicomonas and Kistimonas, the new genus Candidatus Gorgonimonas, and other, yet unclassified, groups of the family. Most endo-chitinases belonged to the glycoside hydrolase family GH18 but five GH19 endo-chitinases were also present. Many endo-chitinases harbored an active site and a signal peptide domain, indicating the enzymes are likely functional and exported to the extracellular environment where endo-chitinases usually act. Phylogenetic analysis revealed clade-specific diversification of endo-chitinases across the family. The presence of multiple, distinct endo-chitinases on the genomes of several Endozoicomonadaceae species hints at functional variation to secure effective chitin processing in diverse micro-niches and changing environmental conditions. We demonstrate that endo-chitinases and other genes involved in chitin degradation are widespread in the Endozoicomonadaceae family and posit that these symbionts play important roles in chitin turnover in filter- and suspension-feeding animals and in benthic, marine ecosystems at large.