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 host organisms by defending them against invading bacteria and providing them with essential metabolites. Here, we describe the microbiomes of three sympatric species of cold-water marine sponges-Halichondria panicea, Halichondria sitiens, and Isodictya palmata-sampled at three time points over a period of 6 years in 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 the varying complexity of their microbiomes. At the 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. At the species level, however, different classes of eukaryotic-like proteins and pathways were distributed between dominant and minor symbionts, indicating specialization within microbiomes. Particularly, the taurine and sulfoacetate import and degradation pathways were associated exclusively with dominant symbionts in all three sponge species, suggesting that these pathways may represent symbiotic features. Our study indicates convergent evolution in the microbiomes of sympatric cold-water sponge species, as reflected by strong functional similarity despite the presence of distinct, taxonomically unrelated symbiotic communities.

Importance: Sponges are regarded among the earliest multicellular organisms and the most ancient examples of animal-bacterial symbiosis. The study of host-microbe interactions in sponges has advanced rapidly due to the application of next-generation sequencing (NGS) technologies that help overcome the challenges of investigating their communities. However, many sponge species, particularly those from polar ecosystems, remain poorly characterized. Here, we demonstrate that three sympatric cold-water sponge species, including two analyzed for the first time, harbor distinct sets of bacterial symbionts, stably associated over 6 years. Using CORe contigs ITerative Expansion and Scaffolding, an algorithm developed in this study, we reconstructed high-quality symbiont genomes and revealed shared features indicative of convergent evolution toward symbiosis. Notably, we identified a potentially novel symbiotic feature-a gene cluster likely involved in sulfoacetate uptake and dissimilation. We also observed shifts in microbiome composition, associated with increasing water temperatures, raising concerns about the impact of global warming on cold-water ecosystems.

Keywords: 16S RNA; bacteria symbionts; global warming; holobiont; metagenomes; sponges; symbiosis; symbiotic features.