Unusual Ecofunctional Traits of Endozoicomonas: A Pan-Genomic Perspective

Abstract

BackgroundEndozoicomonas is a widely distributed genus of marine bacteria, associated with various marine organisms, and recognized for its ecological importance in host health, nutrient cycling, and disease dynamics. Despite its significance, genomic features of Endozoicomonas remain poorly characterized due to limited availability of high-quality genome assemblies. ResultsIn this study, we sequenced 5 novel Endozoicomonas strains and re-sequenced 1 known strain to improve genomic resolution. By integrating these 6 high-quality genomes with 31 others that were publicly available, we identified a distinct, coral-associated clade not recognized by the previous two-clade classification. Pan-genomic analysis revealed significant variation in genetic trait distribution among clades. Notably, Endozoicomonas lacks quorum sensing capabilities, suggesting resistance to quorum quenching mechanisms. It also lacks the ability to synthesize and transport vitamin B12, indicating that it is not a primary source of this nutrient for holobionts. A remarkable feature of Endozoicomonas is its abundance of giant proteins, ranging from 15 to 65 kbp. We identified 92 such proteins, which clustered into three major groups based on amino acid similarity, each associated with specialized functions, such as antimicrobial synthesis, exotoxin production, and cell adhesion. Additionally, we explored prophages and CRISPR-Cas systems. We found that Endozoicomonas acquired prophages from diverse sources via infection or other types of gene transfer. Notably, CRISPR-Cas sequences suggest independent evolutionary trajectories from both prophage acquisition and phylogenetic lineage, implying a potential influence of geographic or environmental pressures. ConclusionsThis study provides new insights into the genomic diversity of Endozoicomonas and its genetic adaptation to diverse hosts. Identification of novel genomic features, including deficiencies in B12 synthesis and quorum sensing, the presence of giant proteins, prophages, and CRISPR-Cas systems, underscores its ecological roles in various holobionts. These findings open new avenues for research on Endozoicomonas and its ecological interactions.