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Background The bacterial genus Endozoicomonas is a predominant member of the coral microbiome, widely recognised for its ubiquity and ability to form high-density aggregates within coral tissues. Hence, investigating its metabolic interplay with coral hosts offers critical insights into its ecological roles and contributions to coral health and resilience. Results Using long- and short-read whole-genome sequencing of 11 Endozoicomonas strains from Acropora loripes , genome sizes were found to range between 5.8 and 7.1 Mbp. Phylogenomic analysis identified two distinct clades within the family Endozoicomonadaceae. Metabolic reconstruction uncovered clade-specific pathways, including the degradation of holobiont-derived carbon and lipids (e.g., galactose, starch, triacylglycerol, D-glucuronate), the latter of which suggests involvement of Endozoicomonas in host ‘sex-type’ steroid hormone metabolism. A clade-specific type 6 Secretion System (T6SS) and predicted effector molecules were identified, potentially facilitating coral-bacterium symbiosis. Additionally, genomic analyses revealed diverse phosphorus acquisition strategies, implicating Endozoicomonas in holobiont phosphorus cycling and stress responses. Conclusions This study reveals clade-specific genomic signatures of Endozoicomonas supporting its mutualistic lifestyle within corals. Findings suggests possible roles in nutrient cycling, reproductive health, and stress resilience, offering novel insights into coral holobiont functioning.

Bacteria in the genus Endozoicomonas are well-known coral symbionts commonly found as clusters within tissues of several coral species. Mapping the spatial distribution of these microbial communities is critical to gaining a holistic understanding of the potential role they may play within the coral host. This study focuses on characterizing bacterial aggregates associated with the common reef-building coral, Acropora loripes, from the central Great Barrier Reef, Australia. A conventional cultivation-based method was employed to establish a pure culture collection of 11 undescribed Endozoicomonas strains isolated from A. loripes. Subsequent 16S rRNA gene amplicon sequencing revealed their classification into two distinct phylogenetic clades. To resolve their spatial distribution in hospite, clade-specific fluorescence in situ hybridization probes were designed. Aggregates were consistently observed in the gastrodermal tissue layers surrounding the upper and lower gastrovascular cavity and were predominantly formed by cells from the same phylogenetic clade, with a minor proportion of aggregates formed by Endozoicomonas from both targeted clades. Furthermore, a clear distinction in aggregation pattern was observed; one clade exhibited clusters with regular and contained growth patterns, whereas the other formed clusters lacking clear boundaries and having irregular shapes. Scanning electron microscopy revealed the presence of a membrane of unknown origin associated with bacterial aggregates in two instances, suggesting potential structural or functional differences in these aggregates. These morphological differences highlight the importance of further investigations into the mechanisms governing bacterial aggregate formation in corals.

The bacterial genus Endozoicomonas is a predominant member of the coral microbiome, widely recognised for its ubiquity and ability to form high-density aggregates within coral tissues. Hence, investigating its metabolic interplay with coral hosts offers critical insights into its ecological roles and contributions to coral health and resilience. Using long- and short-read whole-genome sequencing of 11 Endozoicomonas strains from Acropora loripes, genome sizes were found to range between 5.8 and 7.1 Mbp. Phylogenomic analysis identified two distinct clades within the family Endozoicomonadaceae. Metabolic reconstruction uncovered clade-specific pathways, including the degradation of holobiont-derived carbon and lipids (e.g., galactose, starch, triacylglycerol, D-glucuronate), latter of suggest involvement of Endozoicomonas in host sex-type steroid hormone metabolism. A clade-specific type 6 Secretion System (T6SS) and predicted effector molecules were identified, potentially facilitating coral-bacterium symbiosis. Additionally, genomic analyses revealed diverse phosphorus acquisition strategies, implicating Endozoicomonas in holobiont phosphorus cycling and stress responses. This study reveals clade-specific genomic signatures of Endozoicomonas supporting its mutualistic lifestyle within corals. Findings suggests possible roles in nutrient cycling, reproductive health, and stress resilience, offering novel insights into coral holobiont functioning and potential strategies for reef restoration.Competing Interest StatementThe authors have declared no competing interest.