Sponges underpin the productivity of coral reefs, yet few of their microbial symbionts have been functionally characterised. Here we present an analysis of ~1200 metagenome-assembled genomes (MAGs) spanning seven sponge species and 25 microbial phyla. Compared to MAGs derived from reef seawater, sponge-associated MAGs were enriched in glycosyl hydrolases targeting components of sponge tissue, coral mucus and macroalgae, revealing a critical role for sponge symbionts in cycling reef organic matter. Further, visualisation of the distribution of these genes amongst symbiont taxa uncovered functional guilds for reef organic matter degradation. Genes for the utilisation of sialic acids and glycosaminoglycans present in sponge tissue were found in specific microbial lineages that also encoded genes for attachment to sponge-derived fibronectins and cadherins, suggesting these lineages can utilise specific structural elements of sponge tissue. Further, genes encoding CRISPR and restriction-modification systems used in defence against mobile genetic elements were enriched in sponge symbionts, along with eukaryote-like gene motifs thought to be involved in maintaining host association. Finally, we provide evidence that many of these sponge-enriched genes are laterally transferred between microbial taxa, suggesting they confer a selective advantage within the sponge niche and therefore play a critical role in host ecology and evolution.
Microbially mediated processes contribute to coral reef resilience yet, despite extensive characterisation of microbial community variation following environmental perturbation, the effect on microbiome function is poorly understood. We undertook metagenomic sequencing of sponge, macroalgae and seawater microbiomes from a macroalgae-dominated inshore coral reef to define their functional potential and evaluate seasonal shifts in microbially mediated processes. In total, 125 high-quality metagenome-assembled genomes were reconstructed, spanning 15 bacterial and 3 archaeal phyla. Multivariate analysis of the genomes relative abundance revealed changes in the functional potential of reef microbiomes in relation to seasonal environmental fluctuations (e.g. macroalgae biomass, temperature). For example, a shift from Alphaproteobacteria to Bacteroidota-dominated seawater microbiomes occurred during summer, resulting in an increased genomic potential to degrade macroalgal-derived polysaccharides. An 85% reduction of Chloroflexota was observed in the sponge microbiome during summer, with potential consequences for nutrition, waste product removal, and detoxification in the sponge holobiont. A shift in the Firmicutes:Bacteroidota ratio was detected on macroalgae over summer with potential implications for polysaccharide degradation in macroalgal microbiomes. These results highlight that seasonal shifts in the dominant microbial taxa alter the functional repertoire of host-associated and seawater microbiomes, and highlight how environmental perturbation can affect microbially mediated processes in coral reef ecosystems.
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