Webster, Nicole S.

AbstractMany marine sponges host highly diverse microbiomes that contribute to various aspects of host health. Although the putative function of individual groups of sponge symbionts has been increasingly described, the extreme diversity has generally precluded in‐depth characterization of entire microbiomes, including identification of syntrophic partnerships. The Indo‐Pacific sponge Ianthella basta is emerging as a model organism for symbiosis research, hosting only three dominant symbionts: a Thaumarchaeotum, a Gammaproteobacterium, and an Alphaproteobacterium and a range of other low abundance or transitory taxa. Here, we retrieved metagenome assembled genomes (MAGs) representing >90% of I. basta's microbial community, facilitating the metabolic reconstruction of the sponge's near complete microbiome. Through this analysis, we identified metabolic complementarity between microbes, including vitamin sharing, described the importance of low abundance symbionts, and characterized a novel microbe–host attachment mechanism in the Alphaproteobacterium. We further identified putative viral sequences, highlighting the role viruses can play in maintaining symbioses in I. basta through the horizontal transfer of eukaryotic‐like proteins, and complemented this data with metaproteomics to identify active metabolic pathways in bacteria, archaea, and viruses. This data provide the framework to adopt I. basta as a model organism for studying host–microbe interactions and provide a basis for in‐depth physiological experiments.

Summary Marine sponges represent one of the few eukaryotic groups that frequently harbour 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 ianthellae’ 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 harbour 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.