Abstract

The most recently described bacterial members of the genus Endozoicomonas have been found in association with a wide variety of marine invertebrates. Despite their ubiquity in the host holobiont, limited information is available on the molecular genomic signatures of the symbiotic association of Endozoicomonas with marine sponges. Here, we generated a draft genome of Endozoicomonas sp. OPT23 isolated from the intertidal marine sponge Ophlitaspongia papilla and performed comprehensive comparative genomics analyses. Genome-specific analysis and metabolic pathway comparison of the members of the genus Endozoicomonas revealed the presence of gene clusters encoding for unique metabolic features, such as the utilization of carbon sources through lactate, L-rhamnose metabolism, and a phenylacetic acid degradation pathway in Endozoicomonas sp. OPT23. Moreover, the genome harbors genes encoding for eukaryotic-like proteins, such as ankyrin repeats, tetratricopeptide repeats, and Sel1 repeats, which likely facilitate sponge-bacterium attachment. The genome also encodes major secretion systems and homologs of effector molecules that seem to enable the sponge-associated bacterium to interact with the sponge and deliver the virulence factors for successful colonization. In conclusion, the genome analysis of Endozoicomonas sp. OPT23 revealed the presence of adaptive genomic signatures that might favor their symbiotic lifestyle within the sponge host.

Highlights

  • Sponges (Phylum Porifera) interact and co-evolve with microbes belonging to different lineages

  • OPT23 isolated from the intertidal marine sponge Ophlitaspongia papilla and performed a comprehensive comparative genomics analysis with other members (n = 11) of the genus to unravel the genomic signatures of the sponge-associated Endozoicomonas sp

  • Genetic relatedness estimation using average nucleotide identity (ANI) and DNA-DNA hybridization (DDH), and its comparison with previously sequenced genomes suggest that sponge-associated Endozoicomonas sp

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Summary

Introduction

Sponges (Phylum Porifera) interact and co-evolve with microbes belonging to different lineages. Studies using whole-genome sequencing of microbes isolated from sponges and metagenomic binning approaches have shown the genomic and molecular mechanisms involved in the successful association between the sponges and symbiotic microbes. Genome streamlining [2], evolution of bacterial genome through transposable insertion elements [3], presence of adhesion-related genes, the genes encoding eukaryotic-like protein, effector/virulence factors [4,5,6,7] were reported among several sponge-associated bacteria. Since the first description of the genus Endozoicomonas (Gammaproteobacteria; Oceanospirillales) isolated from the sea slug Elysia ornate [8], Endozoicomonas has been widely reported to be found in association with different marine invertebrates. Several studies found the predominance of Endozoicomonas in healthy Mediterranean gorgonians—Paramuricea clavata and coral—Porites astreoides when compared to their diseased counterparts [16,17], suggesting that strains belonging to this genus have been considered to be an integral part of the healthy holobiont

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