Phylogeny and genomics of SAUL, an enigmatic bacterial lineage frequently associated with marine sponges

Abstract

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.

Marine sponges as Chloroflexi hot-spots: Genomic insights and high resolution visualization of an abundant and diverse symbiotic clade

“…Many LRR proteins are involved in protein-ligand interactions; these include plant immune response and the mammalian innate immune response (for review see (75), such as the detection of pathogen-associated molecular patterns by recognition receptors (76). Our findings are in good agreement with general patterns previously found in metagenomes of sponge symbionts (50, 61), in enriched (mini)-metagenomes of cyanobacterial sponge symbionts (69) and single amplified genomes from members of SAUL (20) and Ca . Poribacteria (68).…”

“…These appear to be xyloglucan-hydrolyzing enzymes, that act on β-1,4 linkages and might help degrade various oligo- and polysaccharides. The previously reported glycosylhydrolases GH33 and GH32 (19, 20) were third most abundant, but were restricted to Caldilineae bin C174. This enzyme family is annotated as sialidase (EC: 3.2.1.18), capable of hydrolysing glycosidic linkages of terminal sialic acid residues, which are present in sponge mesohyl (59).…”

“…The numbers of carbohydrate-active enzymes on Chloroflexi symbiont genomes reflect their extensive potential to degrade complex carbohydrates as was reported previously for Ca . Poribacteria and the sponge associated unidentified lineage SAUL (19, 20).…”

“…Eukaryotic-like proteins (ELPs) seem to be a general genomic feature of sponge symbionts (20, 50, 60, 61, 68–70). Particularly ankyrin (ANK), tetratricopeptide (TPR), and leucine-rich (LRR) repeat proteins are postulated to be involved in mediating host-microbe interactions (71, 72).…”

“…Another example of sponge-symbiont enriched features are the clustered, regularly interspaced, short, palindromic repeats (CRISPRs) and their associated proteins (Cas) that have recently been reported from the genomes of sponge symbionts (20, 50, 60, 61, 69). Here, the investigated Caldilineae genomes and the two SAR202 genomes showed an enrichment of CRISPR (Table 2).…”