Whole Genome Sequencing of the SymbiontPseudovibriosp. from the Intertidal Marine SpongePolymastia penicillusRevealed a Gene Repertoire for Host-Switching Permissive Lifestyle

Abstract

Sponges harbor a complex consortium of microbial communities living in symbiotic relationship benefiting each other through the integration of metabolites. The mechanisms influencing a successful microbial association with a sponge partner are yet to be fully understood. Here, we sequenced the genome of Pseudovibrio sp. POLY-S9 strain isolated from the intertidal marine sponge Polymastia penicillus sampled from the Atlantic coast of Portugal to identify the genomic features favoring the symbiotic relationship. The draft genome revealed an exceptionally large genome size of 6.6 Mbp compared with the previously reported genomes of the genus Pseudovibrio isolated from a coral and a sponge larva. Our genomic study detected the presence of several biosynthetic gene clusters—polyketide synthase, nonribosomal peptide synthetase and siderophore—affirming the potential ability of the genus Pseudovibrio to produce a wide variety of metabolic compounds. Moreover, we identified a repertoire of genes encoding adaptive symbioses factors (eukaryotic-like proteins), such as the ankyrin repeats, tetratrico peptide repeats, and Sel1 repeats that improve the attachment to the eukaryotic hosts and the avoidance of the host’s immune response. The genome also harbored a large number of mobile elements (∼5%) and gene transfer agents, which explains the massive genome expansion and suggests a possible mechanism of horizontal gene transfer. In conclusion, the genome of POLY-S9 exhibited an increase in size, number of mobile DNA, multiple metabolite gene clusters, and secretion systems, likely to influence the genome diversification and the evolvability.

Ecology and Biotechnological Potential of Bacteria Belonging to the Genus Pseudovibrio

“…Recent data suggest that symbionts may adopt specific mechanisms to manipulate host behavior and avoid digestion (7). In line with this view, all Pseudovibrio genomes analyzed so far encode a great diversity of systems potentially used to interact with the sponge cells, evade defense systems and digestion, and colonize both the host cells and the extracellular space (46)(47)(48)75). From these genomic analyses, three types of systems detected in the majority of Pseudovibrio genomes stood out for their role in the interaction with the hosts: type III and type VI secretion systems (T3SS and T6SS, respectively), toxin-like proteins, and proteins containing eukaryotic-like domains (ELD).…”

Detecting signatures of a sponge‐associated lifestyle in bacterial genomes

“…they are not obligate/strict symbionts of sponges. In support of this notion is the recent comparative genomics work for Pseudovibrio that postulated that the genus possesses features that make it metabolically flexible to adapt to a free‐living lifestyle and symbiotic interactions, probably not only with sponges, but also in range of other hosts and habitats (Bondarev et al ., ; Alex and Antunes, ). If true, then any of the Pseudovibrio strains isolated from sponges (Webster and Hill, ; Enticknap et al ., ; O'Halloran et al ., ) might have been in the sponge just by chance and hence are genomically not different to isolates found in the seawater (or elsewhere).…”

“…Similarly, reconstructed genomes from the phylum Poribacteria, a group found in high abundance so far only in sponges, were enriched in gene functions for organic phosphate uptake systems and eukaryotic‐like domains, when compared with 98 free‐living bacterial genomes (Kamke et al ., ). A recent genome analysis of a cultivated sponge‐associated Pseudovibrio strain has also highlighted the presence of eukaryotic‐like proteins, adhesion factors and transposons (Alex and Antunes, ) as potential adaptation to the sponge environment. These findings indicate that genomic adaptation to sponge symbiosis might occur in a wide range of cultured and uncultured bacterial taxa.…”

“…One of the limitations of some of these comparative genome analyses is, however, that they often rely on only a single genome (Gao et al ., ; Alex and Antunes, ), which precludes conclusion about the general relevance of any feature identified for the given phylogenetic or taxonomic group studied. Furthermore, the identification of genes relevant to a symbiotic lifestyle might be biased by the lack of suitable references, as any genomic differences might be caused by evolutionary divergence that is not due to the adaptation to a particular lifestyle (e.g., symbiosis with sponges).…”

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

“…Horizontal gene transfer plays an important role in adaptation and evolution of both prokaryotes and eukaryotes (Keeling and Palmer, ; Wiedenbeck and Cohan, ). In sponge‐associated microbes, adaptation to either specific niches or to changes in environmental conditions can be facilitated by mobile genetic elements such as transposons, plasmids and prophages (Fan et al ., ; Alex and Antunes, ). SAUL bins encoded for transposable insertion elements such as transposases (COG1943, COG3415, and COG3328), retroid elements containing reverse transcriptase (COG3344, PF00078) and integrases (PF00665).…”