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

09/22/2022

<jats:title>Abstract </jats:title><jats:sec> <jats:title>Background</jats:title> <jats:p>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.</jats:p> </jats:sec><jats:sec> <jats:title>Results</jats:title> <jats:p>Symbionts of healthy octocorals were affiliated with the taxa <jats:italic>Endozoicomonadaceae</jats:italic>, Candidatus <jats:italic>Thioglobaceae</jats:italic>, <jats:italic>Metamycoplasmataceae</jats:italic>, unclassified <jats:italic>Pseudomonadales</jats:italic>, <jats:italic>Rhodobacteraceae</jats:italic>, unclassified <jats:italic>Alphaproteobacteria</jats:italic> and Ca. <jats:italic>Rhabdochlamydiaceae</jats:italic>. Phylogenomics inference revealed that the <jats:italic>Endozoicomonadaceae</jats:italic> symbionts uncovered here represent two species of a novel genus unique to temperate octocorals, here denoted Ca. <jats:italic>Gorgonimonas</jats:italic><jats:italic>eunicellae</jats:italic> and Ca. <jats:italic>Gorgonimonas</jats:italic><jats:italic>leptogorgiae</jats:italic>. 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 <jats:italic>Endozoicomonadaceae</jats:italic> 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 <jats:italic>Metamycoplasmataceae</jats:italic> and Ca. <jats:italic>Thioglobaceae</jats:italic>, 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 <jats:italic>Proteobacteria </jats:italic>taxa may specialize in chemical defense and guard other symbionts, including <jats:italic>Endozoicomonadaceae</jats:italic>, which lack such capacity.</jats:p> </jats:sec><jats:sec> <jats:title>Conclusion</jats:title> <jats:p>This is the first study to recover MAGs from dominant symbionts of octocorals, including those of so-far unculturable <jats:italic>Endozoicomonadaceae</jats:italic>, Ca. <jats:italic>Thioglobaceae</jats:italic> and <jats:italic>Metamycoplasmataceae</jats:italic> symbionts. We identify a thus-far unanticipated, global role for <jats:italic>Endozoicomonadaceae</jats:italic> 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.</jats:p> </jats:sec>

Authors in the community:

• 

  T

  Tina Keller Costa

  ist427891

  Affiliations and sources

  IST > iBB

  Instituto de Bioengenharia e Biociências

  In: orcid

  ID: 131460618

Microbiome

10

2049-2618

10.1186/s40168-022-01343-7

biological-sciences - Biological sciences

eng - English