Genome-based investigations of the sponge microbiome have revealed an array of diverse metabolic potential encoded in symbiont genomes, including the processing of organic carbon, nitrogen, and sulfur compounds, autotrophic sulfur oxidation, and vitamin synthesis.
Whilst the specificity, biogeography, and environmental sensitivity of the relationship between sponges and their microbiome has been intensively studied, our understanding of the physiological interactions between sponges and their symbiotic microorganisms is still very limited. Furthermore, isotope labeling experiments have proven that symbiont-derived carbon and nitrogen can be found in sponge cells, with more recent studies revealing an emerging view that not only microbial symbionts can incorporate DOM, but that sponge cells do as well, and can even translocate DOM-derived carbon and nitrogen to their symbionts. These microbial symbionts have been shown to photosynthetically fix carbon, fix N 2, nitrify, as well as carry out anammox, denitrification, and sulfate respiration. Marine sponges often harbor dense, diverse, and stable communities of microorganisms that are thought to play a role in DOM processing, as well as a broad suite of other nutrient transformations. Sponges play a crucial role in maintaining biomass in reef ecosystems by filtering dissolved organic matter (DOM) from large quantities of water and capturing it as biomass, which is then shed as particulate organic matter (POM) and passed to higher trophic levels. Marine sponges are important components of coral reefs with a range of critical ecological functions. These results highlight the important role of biogenic sulfur compounds in the interplay between Ianthella basta and its microbial symbionts. Metaproteogenomic analyses also suggest that ‘ Candidatus Taurinisymbion ianthellae’ imports DMSP and possesses both pathways for DMSP demethylation and cleavage, enabling it to use this compound as a carbon and sulfur source for biomass, as well as for energy conservation.
Furthermore, we found that taurine-derived ammonia is exported by the symbiont for immediate oxidation by the dominant ammonia-oxidizing thaumarchaeal symbiont, ‘ Candidatus Nitrosospongia ianthellae’. ‘ Candidatus Taurinisymbion ianthellae’ incorporates taurine-derived carbon and nitrogen while, at the same time, oxidizing the dissimilated sulfite into sulfate for export. By using a combination of metaproteogenomics and laboratory incubations coupled with isotope-based functional assays, we showed that the dominant gammaproteobacterial symbiont, ‘ Candidatus Taurinisymbion ianthellae’, residing in the marine sponge, Ianthella basta, expresses a pathway for the import and dissimilation of taurine, a ubiquitously occurring sulfonate metabolite in marine sponges. Recent omics-based studies of marine sponge microbiomes have proposed numerous pathways of dissolved metabolite exchange between the host and symbionts within the context of the surrounding environment, but few studies have sought to experimentally interrogate these pathways. As potentially the oldest representation of a metazoan-microbe symbiosis, they also harbor dense, diverse, and species-specific communities of microbes, which are increasingly recognized for their contributions to dissolved organic matter (DOM) processing. Marine sponges are critical components of marine benthic fauna assemblages, where their filter-feeding and reef-building capabilities provide bentho-pelagic coupling and crucial habitat.
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