Harnessing the catalyst power of host-microbe interactions: a quest for novel chitinases from octocoral symbionts

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Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

Publication . Keller-Costa, Tina; Kozma, Lydia; Silva, Sandra G.; Toscan, Rodolfo; Gonçalves, Jorge Manuel Santos; Lago-Lestón, Asunción; Kyrpides, Nikos C.; Nunes da Rocha, Ulisses; Costa, Rodrigo

The role of bacterial symbionts that populate octocorals (Cnidaria, Octocorallia) is still poorly understood. To shed light on their metabolic capacities, we examined 66 high-quality metagenome-assembled genomes (MAGs) spanning 30 prokaryotic species, retrieved from microbial metagenomes of three octocoral species and seawater. Results Symbionts of healthy octocorals were affiliated with the taxa Endozoicomonadaceae, Candidatus Thioglobaceae, Metamycoplasmataceae, unclassified Pseudomonadales, Rhodobacteraceae, unclassified Alphaproteobacteria and Ca. Rhabdochlamydiaceae. Phylogenomics inference revealed that the Endozoicomonadaceae symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. Gorgonimonas eunicellae and Ca. Gorgonimonas leptogorgiae. Their genomes revealed metabolic capacities to thrive under suboxic conditions and high gene copy numbers of serine-threonine protein kinases, type 3-secretion system, type-4 pili, and ankyrin-repeat proteins, suggesting excellent capabilities to colonize, aggregate, and persist inside their host. Contrarily, MAGs obtained from seawater frequently lacked symbiosis-related genes. All Endozoicomonadaceae symbionts harbored endo-chitinase and chitin-binging protein-encoding genes, indicating that they can hydrolyze the most abundant polysaccharide in the oceans. Other symbionts, including Metamycoplasmataceae and Ca. Thioglobaceae, may assimilate the smaller chitin oligosaccharides resulting from chitin breakdown and engage in chitin deacetylation, respectively, suggesting possibilities for substrate cross-feeding and a role for the coral microbiome in overall chitin turnover. We also observed sharp differences in secondary metabolite production potential between symbiotic lineages. Specific Proteobacteria taxa may specialize in chemical defense and guard other symbionts, including Endozoicomonadaceae, which lack such capacity. Conclusion This is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable Endozoicomonadaceae, Ca. Thioglobaceae and Metamycoplasmataceae symbionts. We identify a thus-far unanticipated, global role for Endozoicomonadaceae symbionts of corals in the processing of chitin, the most abundant natural polysaccharide in the oceans and major component of the natural zoo- and phytoplankton feed of octocorals. We conclude that niche partitioning, metabolic specialization, and adaptation to low oxygen conditions among prokaryotic symbionts likely contribute to the plasticity and adaptability of the octocoral holobiont in changing marine environments. These findings bear implications not only for our understanding of symbiotic relationships in the marine realm but also for the functioning of benthic ecosystems at large.

2022-09-22Journal article

Open access

An artificial selection procedure enriches for known and suspected chitin degraders from the prokaryotic rare biosphere of multiple marine biotopes

Publication . Meunier, Laurence; Keller-Costa, Tina; Cannella, David; Gonçalves, Jorge Manuel Santos; Dechamps, Etienne; Marques, Matilde; Costa, Rodrigo; George, Isabelle F.

Biological of chitin-degrading microbial communities change across marine biotopes, but efforts to isolate chitin degraders within these communities in the laboratory have seldom been attempted. We characterized the prokaryotic communities associated with the marine sponge Sarcotragus spinosulus, the octocoral Eunicella labiata, and their surrounding sediment and seawater and applied an artificial selection procedure to enrich bacterial consortia capable of degrading chitin from the abovementioned biotopes. Throughout the procedure, chitin degradation was monitored, and the taxonomic composition was studied along four successive enrichment cultures from each biotope. Results The naturally occurring prokaryotic communities of the two host species (Sarcotragus spinosulus and Eunicella labiata) were distinct from each other and from those of seawater and sediments, even though they were co-inhabiting the same geographic area. We found that low-abundance bacteria from the rare biosphere were recruited in the enrichment cultures from all biotopes, while dominant bacterial symbionts likely to play a role in chitin degradation within marine sponges and octocorals remained “unculturable” under our experimental conditions. Well-known chitin degraders such as Vibrio, Pseudoalteromonas and Aquimarina, as well as other taxa not known or poorly known for their role(s) in chitin degradation such as Aureivirga, Halodesulfovibrio, Motilimonas, Muricauda, Psychromonas, Poseidonibacter, Reichenbachiella, and Thalassotalea, among others, were enriched using our artificial selection approach. Distinct chitin-degrading consortia were enriched from each marine biotope, highlighting the feasibility of this approach in fostering the discovery of novel microorganisms and enzymes involved in chitin degradation pathways of relevance in applied biotechnology. Conclusion This study unveils distinct bacterial consortia possessing moderate to high efficiency at degrading chitin. They were composed of a mix of known chitin degraders, known chitin utilizers and many taxa poorly or not yet known for their role(s) in chitin degradation such as Aureivirga, Psychromonas, Motilimonas, Reichenbachiella, or Halodesulfovibrio. The latter taxa are potential key players in marine chitin degradation whose study could lead to the discovery of novel enzyme variants able to degrade chitin and its derivatives.

2025-11-25Journal article

Open access