Solomons, G. M.*1, Waterworth, S. C.1,2, Kalinski, J-.C. J.1,3, Madonsela, L. S.1, Parker-Nance, S.4,5, Dorrington, R. A.1,4
1 Department of Biochemistry and Microbiology, Rhodes University, Makhanda 6140, South Africa
2 National Cancer Institute, Frederick, Maryland, USA
3 Department of Biochemistry, University of California Riverside, Riverside, USA
4 South African Institute for Aquatic Biodiversity, Makhanda 6140, South Africa
5 South African Environmental Observation Network, Elwandle Coastal Node, Port Elizabeth, South Africa
Symbiotic relationships between sponges and their associated bacteria represent some of the oldest examples of relationships between microbes and animals on Earth. Bacterial symbionts are acquired by their sponge hosts for a number of reasons e.g. uptake of nutrients, acquisition of carbon, nitrogen and phosphorous, recycling of waste and other metabolic byproducts, biosynthesis of amino acids and stabilizing of the host skeletal system. They also facilitate chemical defence against pathogens and predators by producing bioactive secondary metabolites. Marine sponges of the Latrunculiidae family are prolific producers of bioactive secondary metabolites known as pyrroloiminoquinones, a class of alkaloids with a broad spectrum of biological activities with potential as drug leads. The microbiomes associated with sponge species within this family are highly conserved and dominated by two bacterial symbionts: a broad-host range Tethybacterales symbiont shared with other, unrelated sponge taxa and a Spirochete symbiont, found only in latrunculid species. In this study we investigated the nature of the symbiotic relationship between latrunculid sponges and their conserved spirochete symbiont and the production of pyrroloiminoquinones. We analysed shotgun metagenomic libraries of eight sponge specimens representing four latrunculid species and assessed the functional and biosynthetic potential as well as the evolutionary divergence patterns of the spirochete Metagenome-Assembled Genomes (MAGs) associated. We discovered that the spirochetes are likely newly acquired symbionts that are currently undergoing genome reduction, are distinct from other sponge-associated spirochetes and were likely acquired from different free-living spirochete species. Assessment of the functional potential of the latrunculid spirochete symbionts suggests that they were selected by their hosts for their ability to produce terpenoids that may provide antioxidizing protection to the sponge. Despite the absence of putative pyrroloiminoquinone biosynthetic gene clusters on their genomes, dysbiosis between closely related spirochete strains correlated with a change in chemotype observed in T. favus and T. michaeli sponges, this infers that the symbionts play a role in pyrroloiminoquinone production in latrunculid sponges.
Keywords: Latrunculiidae, sponge symbionts, pyrroloiminoquinones, spirochetes, genome erosion