Metagenomic binning reveals versatile nutrient cycling and distinct adaptive features in alphaproteobacterial symbionts of marine sponges

Abstract

Marine sponges are early-branched metazoans known to harbor dense and diverse microbial communities. Yet the role of the so far uncultivable alphaproteobacterial lineages that populate these sessile invertebrates remains unclear. We applied a sequence composition-dependent binning approach to assemble one Rhodospirillaceae genome from the Spongia officinalis microbial metagenome and contrast its functional features with those of closely related sponge-associated and free-living genomes. Both symbiotic and free-living Rhodospirillaceae shared a suite of common features, possessing versatile carbon, nitrogen, sulfur and phosphorus metabolisms. Symbiotic genomes could be distinguished from their free-living counterparts by the lack of chemotaxis and motility traits, enrichment of genes required for the uptake and utilization of organic sulfur compounds-particularly taurine-, higher diversity and abundance of ABC transporters, and a distinct repertoire of genes involved in natural product biosynthesis, plasmid stability, cell detoxification and oxidative stress remediation. These sessile symbionts may more effectively contribute to host fitness via nutrient exchange, and also host detoxification and chemical defense. Considering the worldwide occurrence and high diversity of sponge-associated Rhodospirillaceae verified here using a tailored in silico approach, we suggest that these organisms are not only relevant to holobiont homeostasis but also to nutrient cycling in benthic ecosystems.

Comparative genomics reveals complex natural product biosynthesis capacities and carbon metabolism across host‐associated and free‐living Aquimarina (Bacteroidetes, Flavobacteriaceae) species

“…Consistent with genome‐wide variability above the species level, the core/pan genome ratio observed here for Aquimarina spp. (0.058) was below the abovementioned intraspecies values and above ratios calculated for more diversified genome groups such as uncultivated marine sponge symbionts of the Rhodospirillalles order, found to span different genera and to present a core/pan genome ratio of 0.026 (Karimi et al ., ). Phylogenomics metrics were further used in this study to attempt the identification of Aquimarina strains to the species level, revealing cases where the emergence of novel species could either be proposed or become matter of debate.…”

Microbiota of the alien species Paraleucilla magna (Porifera, Calcarea) from the Southwestern Atlantic, and a comparison with that of other calcareous sponges

“…Karimi et al [44] published a study reporting the main genomic features of alphaproteobacterial sponge symbionts. Corroborating our data, their study showed a prevalence of ABC transporters, fundamental for nutrient obtention, and versatile nutrients metabolism, pointing to a great importance in nutrient cycling.…”

Host genetics and geography influence microbiome composition in the sponge Ircinia campana

“…Sponges (phylum Porifera) are considered valuable model systems in host-microbiome research due to the abundance and diversity within their associated microbial communities (Pita, Fraune, & Hentschel, 2016), with a total of 52 bacterial phyla and candidate phyla discovered among sponge hosts (Thomas et al, 2016). Spongemicrobiome interactions are numerous and complex, and microbial symbionts may confer a number of benefits to their host including nutrition and waste metabolism (Freeman, Thacker, Baker, & Fogel, 2013;Karimi et al, 2018;Moitinho-Silva et al, 2017;Thomas, Rusch, et al, 2010), acclimation to ocean acidification (Ribes et al, 2016), reduction in host surface fouling (On, Lau, & Qian, 2006) and production of compounds that deter predation of the sponge host (Garate, Blanquer, & Uriz, 2015). Sponge-associated microbes are also of significant biotechnological interest due to their potential for production of novel, pharmaceutically active secondary metabolites .…”