Abstract

Sponges are among the oldest metazoans and their success is partly due to their abundant and diverse microbial symbionts. They are one of the few animals that have Thaumarchaeota symbionts. Here we compare genomes of 11 Thaumarchaeota sponge symbionts, including three new genomes, to free-living ones. Like their free-living counterparts, sponge-associated Thaumarchaeota can oxidize ammonia, fix carbon, and produce several vitamins. Adaptions to life inside the sponge host include enrichment in transposases, toxin-antitoxin systems and restriction modifications systems, enrichments previously reported also from bacterial sponge symbionts. Most thaumarchaeal sponge symbionts lost the ability to synthesize rhamnose, which likely alters their cell surface and allows them to evade digestion by the host. All but one archaeal sponge symbiont encoded a high-affinity, branched-chain amino acid transporter system that was absent from the analyzed free-living thaumarchaeota suggesting a mixotrophic lifestyle for the sponge symbionts. Most of the other unique features found in sponge-associated Thaumarchaeota, were limited to only a few specific symbionts. These features included the presence of exopolyphosphatases and a glycine cleavage system found in the novel genomes. Thaumarchaeota have thus likely highly specific interactions with their sponge host, which is supported by the limited number of host sponge species to which each of these symbionts is restricted.

Highlights

  • Sponges are sessile, soft-bodied invertebrates that inhabit marine and freshwater environments around the globe (Van Soest et al, 2012)

  • One of the few previously identified general patterns for sponge-associated archaeal genomes is a higher GC content compared to free-living Thaumarchaeota (Moeller et al, 2019; Zhang et al, 2019)

  • The inclusion of the here generated genome of the thaumarchaeal symbiont from the deep-sea sponge Hymedesmia (Stylopus) methanophila suggests that low GC content is a general feature among deep-sea sponge-associated Thaumarchaeota

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Summary

Introduction

Sponges (phylum Porifera) are sessile, soft-bodied invertebrates that inhabit marine and freshwater environments around the globe (Van Soest et al, 2012). As highly efficient filter feeders, they are a crucial link between the pelagic and benthic environments (Yahel et al, 2003; de Goeij et al, 2013) Their success has been attributed to their microbial symbionts (Taylor et al, 2007) that can make up to 38% of their tissue volume (Vacelet and Donadey, 1977). Sponge symbionts, including bacteria and archaea, can be transmitted both horizontally and vertically (Steger et al, 2008; Björk et al, 2019). The symbionts support their host in various ways. Given that sponges are one of the earliestbranching multi-cellular animals (Metazoa) (Feuda et al, 2017), these symbiotic interactions are considered ancient

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