The deep‐sea glass sponge Lophophysema eversa harbours potential symbionts responsible for the nutrient conversions of carbon, nitrogen and sulfur

Abstract

Glass sponge (Hexactinellida, Porifera) is a special lineage because of its unique tissue organization and skeleton material. Structure and physiology of glass sponge have been extensively studied. However, our knowledge of the glass sponge-associated microbial community and of the interaction with the host is rather limited. Here, we performed genomic studies on the microbial community in the glass sponge Lophophysema eversa in seamount. The microbial community was dominated by an ammonia-oxidizing archaeum (AOA), a nitrite-oxidizing bacterium (NOB) and a sulfur-oxidizing bacterium (SOB), all of which were autotrophs. Genomic analysis on the AOA, NOB and SOB in the sponge revealed specific functional features of sponge-associated microorganisms in comparison with the closely related free-living relatives, including chemotaxis, phage defence, vitamin biosynthesis and nutrient uptake among others, which are related to ecological functions. The three autotrophs play essential roles in the cycles of carbon, nitrogen and sulfur in the microenvironment inside the sponge body, and they are considered to play symbiotic roles in the host as scavengers of toxic ammonia, nitrite and sulfide. Our study extends knowledge regarding the metabolism and the evolution of chemolithotrophs inside the invertebrate body.

Genome Reduction and Microbe-Host Interactions Drive Adaptation of a Sulfur-Oxidizing Bacterium Associated with a Cold Seep Sponge

“…To gain better understanding of the functional profile of Gsub, we compared its genome to two of its nearest neighbor genomes: two endosymbiont SOB (“ Candidatus Ruthia magnifica” strain Cm [Rmag] and “ Candidatus Vesicomyosocius okutanii” strain HA [Voku]) from vent clams (24, 25); the comparison also included two potential sponge symbiont SOB (the SOB in the deep-sea glass sponge Lophophysema [Glop] and in the shallow water sponge Haliclona [Ghal]) (30, 44) and two free-living SOB ( Thioalkalivibrio sulfidophilus HL-EbGr7 [Tsul] and Thiomicrospira crunogena XCL-2 [Tcru]) from shallow and deep water environments (Table 1). The overall genomic picture of Gsub was highly similar to that of the Rmag and Voku, which possess a much lower number of unique Kyoto Encyclopedia of Genes and Genomes (KEGG) genes (4 to 39) than the free-living bacteria (183 to 383) (Table 1 and Fig.…”

“…In addition, the hosts acquire food from the bacterial symbionts and provide them with shelter. Genomic studies have investigated several sulfur-oxidizing symbionts from deep-sea invertebrates, including “ Candidatus Ruthia magnifica” strain Cm in the clam Calyptogena magnifica (25), “ Candidatus Vesicomyosocius okutanii” strain HA in the clam Calyptogena okutanii (26), a symbiont of the oligochaete Olavius algarvensis (29), a gammaproteobacterium in the snail Crysomallon squamiferum (27), and a gammaproteobacterium in the deep-sea glass sponge Lophophysema eversa (30). In Lophophysema eversa , the microbial community was dominated by an ammonia-oxidizing archaeon (AOA), a nitrite-oxidizing bacterium (NOB), and a SOB, all of which were autotrophs.…”

The Cyanobacteria-Dominated Sponge Dactylospongia elegans in the South China Sea: Prokaryotic Community and Metagenomic Insights

“…Proteobacteria has been reported to be one of the most diverse phyla of sponge-associated microbial communities (Schmitt et al, 2012), and an Gammaproteobacteria symbiont from the deep-sea glass sponge Lophophysema eversa has been confirmed to play important roles in sulfur oxidation pathway (Tian et al, 2016). It is reasonable to think that the predominant Proteobacteria play important symbiotic roles in the sponge D. elegans .…”

“…The ammonia oxidizer Ceratodictyon spongiosum has been demonstrated to remove the ammonia excreted by the sponge host in the sponge Haliclona cymaeformis (Davy et al, 2002). Furthermore, Nitrosopumilus -like archaea were predominant in the deep-sea glass sponge L. eversa and cold-seep sponge Suberites sp., both of which have been proposed to play important roles in ammonia oxidization (Tian et al, 2016, 2017). Similar roles should also be suggested for the Thaumarchaeota in the sponge D. elegans .…”

“…A recent work investigating the deep-see glass sponge Lophophysema eversa serves as an ideal example of the interactive network of chemoautotrophic sponge symbionts with respect to nutrient conversions (Tian et al, 2016). For sponges predominantly inhabited by cyanobacteria, other microbes also maintain interactions with the sponge host and play important symbiotic roles.…”