Webster, N. S. | bioRxiv Science

bioRxiv2019

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical sponge Ianthella basta

Marine sponges represent one of the few eukaryotic groups that frequently harbor symbiotic members of the Thaumarchaeota, which are important chemoautotrophic ammonia-oxidizers in many environments. However, in most studies, direct demonstration of ammonia-oxidation by these archaea within sponges is lacking, and little is known about sponge-specific adaptations of ammonia-oxidizing archaea (AOA). Here, we characterized the thaumarchaeal symbiont of the marine sponge Ianthella basta using metaproteogenomics, fluorescence in situ hybridization, qPCR and isotope-based functional assays. "Candidatus Nitrosospongia bastadiensis" is only distantly related to cultured AOA. It is an abundant symbiont that is solely responsible for nitrite formation from ammonia in I. basta that surprisingly does not harbor nitrite-oxidizing microbes. Furthermore, this AOA is equipped with an expanded set of extracellular subtilisin-like proteases, a metalloprotease unique among archaea, as well as a putative branched-chain amino acid ABC transporter. This repertoire is strongly indicative of a mixotrophic lifestyle and is (with slight variations) also found in other sponge-associated, but not in free-living AOA. We predict that this feature as well as an expanded and unique set of secreted serpins (protease inhibitors), a unique array of eukaryotic-like proteins, and a DNA-phosporothioation system, represent important adaptations of AOA to life within these ancient filter-feeding animals. Originality-Significance StatementMany marine sponges harbor symbiotic members of the Thaumarchaeota, but there is generally only indirect evidence available about their functional role within these filter-feeding animals. Furthermore, the specific adaptations of thaumarchaeal symbionts to their sponge hosts are incompletely understood. In this study, we thoroughly characterized a thaumarchaeal symbiont residing in the reef sponge Ianthella basta and demonstrate by using a combination of molecular tools and isotope techniques, that it is the only ammonia-oxidizer in its host. In contrast to other sponges, I. basta does not contain nitrite-oxidizing microbes and thus excretes considerable amounts of nitrite. Furthermore, using metagenomics and metaproteomics we reveal important adaptations of this symbiont, that represents a new genus within the Thaumarchaeota, and conclude that it most likely lives as a mixotroph in its sponge host.

microbiology↗

bioRxiv2019

Microbial predictors of environmental perturbations in coral reef ecosystems

Incorporation of microbial community data into environmental monitoring programs could improve prediction and management of environmental pressures. Coral reefs have experienced dramatic declines due to cumulative impacts of local and global stressors. Here we assess the utility of free-living (i.e. seawater and sediment) and host-associated (i.e. corals, sponges and macroalgae) microbiomes for diagnosing environmental perturbation based on their habitat-specificity, environmental sensitivity and uniformity. We show that the seawater microbiome has the greatest diagnostic value, with environmental parameters explaining 56% of the observed compositional variation and temporal successions being dominated by uniform community assembly patterns. Host-associated microbiomes, in contrast, were five-times less affected by the environment and their community assembly patterns were generally less uniform. Further, seawater microbial community data provided an accurate prediction on the environmental state, highlighting the diagnostic value of microorganisms and illustrating how long-term coral reef monitoring initiatives could be enhanced by incorporating assessments of microbial communities in seawater.\n\nImportanceThe recent success in disease diagnostics based on the human microbiome has highlighted the utility of this approach for model systems. However, despite improved prediction and management of environmental pressures from the inclusion of microbial community data in monitoring programs, this approach has not previously been applied to coral reef ecosystems. Coral reefs are facing unprecedented pressure on a local and global scale, and sensitive and rapid markers for ecosystem stress are urgently needed to underpin effective management and restoration strategies. In this study, we performed the first assessment of the diagnostic value of multiple free-living and host-associated reef microbiomes to infer the environmental state of coral reef ecosystems. Our results reveal that free-living microbial communities have a higher potential to infer environmental parameters than host-associated microbial communities due to their higher determinacy and environmental sensitivity. We therefore recommend timely integration of microbial sampling into current coral reef monitoring initiatives.

microbiology↗