Comparative genomics provides insight into the function of broad-host range sponge symbionts

Abstract

Sponges have evolved complex associations with conserved bacteria symbionts that contribute to the fitness of the host. Sponges of the family, Latrunculiidae, produce a diverse array of cytotoxic pyrroloiminoquinone alkaloids and their microbiomes are dominated by a conserved spirochete and betaproteobacterium. We investigated the microbiome of Tsitsikamma favus, a latrunculid species that produces predominantly tsitsikammamines. A total of 50 Metagenome-Assembled-Genomes (MAGs) were recovered from the four metagenomes, including representatives of the conserved spirochete and betaproteobacterium symbionts. We predict that the Sp02-3, one of two spirochetes unique to latrunculid species, is likely an anaerobic symbiont that produces vitamin B6. Dysbiosis of the spirochete population correlates with the chemistry associated with distinct sponge chemotypes, implying a role in pyrroloiminoquinone production. The betaproteobacteria symbiont belongs to the newly defined Tethybacterales order and likely aids in the removal of nitrate. There is also evidence to suggest that the two symbionts may work in tandem to remove sulfate from the sponge. Additionally, we analyzed seventeen Tethybacterales genomes and identified a third family within the order. The phylogeny of Tethybacterales is incongruent with that of the sponge hosts suggesting that the association of Tethybacterales and their sponge hosts likely occurred multiple times over their evolutionary history.

Testing cophylogeny between coral reef invertebrates and their bacterial and archaeal symbionts

“…In non-marine hosts such as termites, Spirochaetes of the genus Treponema (family: Spirochaetaceae) have been implicated in nitrogen fixation (Lilburn et al, 2001), while in the marine environ- lucinid clams (Lim et al, 2019). Further, Spirochaeta were identified as a key member of the holobiont in Tsitsikamma and Cyclacanthia sponges where cophylogenetic patterns were observed (Matcher et al, 2017) and metagenomic analysis of the sponge-associated Spirochaete suggested roles in vitamin B6 and pyrroloiminoquinone production (Waterworth et al, 2020). The Thaumarcheota genus Nitrosopumilus (family: Nitrosopumiliaceae) is characterised by its ability to convert ammonia to nitrite, providing an essential step in nitrogen cycling (Könneke et al, 2005).…”

Zooming into the sponge microbiome in the omics era

“…On the other hand, several sponge symbionts displayed a limited carbohydrate metabolism(Bayer et al, 2020;Knobloch et al, 2020). This metabolic specialization of microbes that represent certain lineages inhabiting a similar environmental niche and encoding equivalent genes for carbohydrate utilization indicates the possible presence of functional guilds within the sponge microbiome(Fan et al, 2012) Waterworth et al, 2021),. supporting the notion that synthesis of these essential molecules represents a microbially-mediated function common within the sponge microbiome(Hentschel et al, 2012;Pita et al, 2018).…”