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Marine sponges are early-branching, filter-feeding metazoans that usually host complex microbiomes comprised of several, currently uncultivatable symbiotic lineages. Here, we use a low-carbon based strategy to cultivate low-abundance bacteria from  Spongia officinalis . This approach favoured the growth of  Alphaproteobacteria  strains in the genera  Anderseniella ,  Erythrobacter ,  Labrenzia ,  Loktanella ,  Ruegeria ,  Sphingorhabdus ,  Tateyamaria  and  Pseudovibrio , besides two likely new genera in the  Rhodobacteraceae  family. Mapping of complete genomes against the metagenomes of  S .  officinalis , seawater, and sediments confirmed the rare status of all the above-mentioned lineages in the marine realm. Remarkably, this community of low-abundance  Alphaproteobacteria  possesses several genomic attributes common to dominant, presently uncultivatable sponge symbionts, potentially contributing to host fitness through detoxification mechanisms (e.g. heavy metal and metabolic waste removal, degradation of aromatic compounds), provision of essential vitamins (e.g. B6 and B12 biosynthesis), nutritional exchange (especially regarding the processing of organic sulphur and nitrogen) and chemical defence (e.g. polyketide and terpenoid biosynthesis). None of the studied taxa displayed signs of genome reduction, indicative of obligate mutualism. Instead, versatile nutrient metabolisms along with motility, chemotaxis, and tight-adherence capacities - also known to confer environmental hardiness – were inferred, underlying dual host-associated and free-living life strategies adopted by these diverse sponge-associated  Alphaproteobacteria .

Genomic blueprints of sponge-prokaryote symbiosis are shared by low abundant and cultivatable Alphaproteobacteria