Taxonomically different symbiotic communities of sympatric Arctic sponge species show functional similarity with specialization at species level

Abstract

Marine sponges harbor diverse communities of associated organisms, including eukaryotes, viruses, and bacteria. Sponge associated microbiomes contribute to the health of the host organisms by defending them against invading bacteria and providing them with essential metabolites. Here we describe microbiomes of three sympatric species of cold-water marine sponges - Halichondria panicea, Halichondria sitiens, and Isodictya palmata - sampled over a period of six years at the White Sea. We identified the sponges as low microbial abundance species and detected stably associated bacteria that represent new taxa of sponge symbionts within Alpha- and Gammaproteobacteria. The sponges carried unique sets of unrelated species of symbiotic bacteria illustrating varying complexity of microbiomes. On a community level, sponge associated microbiomes shared common symbiotic features; they encoded multiple eukaryotic-like proteins, biosynthetic pathways, and transporters of amino acids and vitamins essential for sponges. On a species level, however, different classes of eukaryotic-like proteins and pathways were distributed between dominant and minor symbionts indicating specialization within microbiomes. Particularly, taurine and sulfoacetate metabolism pathways were associated exclusively with dominant symbionts in all three sponge species. Our study demonstrates strong functional convergence and co-evolution of microbiomes of sympatric cold-water sponge species with a distribution of functions between community members. Additionally, we observed dramatic shifts in compositions of sponge microbiomes coinciding with abnormally high water temperatures during the 2018 season, highlighting the vulnerability of cold-water ecosystems to global warming.