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Summary: Many marine sponges contain dense and diverse communities of associated microorganisms. Members of the ‘sponge‐associated unclassified lineage’ (SAUL) are frequently recorded from sponges, yet little is known about these bacteria. Here we investigated the distribution and phylogenetic status of SAUL. A meta‐analysis of the available literature revealed the widespread distribution of this clade and its association with taxonomically varied sponge hosts. Phylogenetic analyses, conducted using both 16S rRNA gene‐based phylogeny and concatenated marker protein sequences, revealed that SAUL is a sister clade of the candidate phylum ‘Latescibacteria’. Furthermore, we conducted a comprehensive analysis of two draft genomes assembled from sponge metagenomes, revealing novel insights into the physiology of this symbiont. Metabolic reconstruction suggested that SAUL members are aerobic bacteria with facultative anaerobic metabolism, with the capacity to degrade multiple sponge‐ and algae‐derived carbohydrates. We described for the first time in a sponge symbiont the putative genomic capacity to transport phosphate into the cell and to produce and store polyphosphate granules, presumably constituting a phosphate reservoir for the sponge host in deprivation periods. Our findings suggest that the lifestyle of SAUL is symbiotic with the host sponge, and identify symbiont factors which may facilitate the establishment and maintenance of this relationship. [ABSTRACT FROM AUTHOR]