Host Filtering Overrides Environmental Heterogeneity in Shaping Sea Cucumber Gut Microbiomes

Gut microbiomes play critical roles in host physiology and ecological contributions of sea cucumbers in tropical coral reefs. However, the relative importance of host filtering versus environmental factors in gut microbiome assembly remains poorly quantified in natural populations. Using 16S rRNA gene amplicon sequencing and sediment physicochemical analyses, this study characterized gut microbiomes of three co-occurring sea cucumber species (Holothuria atra, Holothuria edulis and Stichopus chloronotus) across heterogeneous habitats. Despite significant spatial variation in sediment properties and microbial communities, all three sea cucumber species maintained species-specific and stable gut microbiomes across sites. Although source tracking identified sediment as the primary microbial reservoir, variation partitioning revealed that host filtering far overrode environmental heterogeneity, with sediment physicochemical properties explaining a negligible fraction (< 1%) of community variation. Each host harboured distinct functional taxa, and most dominant genera showed no significant correlations with sediment properties. These results support a 'host as filter and sediment as source' pattern, indicating that host-mediated selection can filter microbes from distinct source pools to establish a conserved gut microbiome largely independent of environmental variation. By retaining microbial taxa with functional potentials, sea cucumbers may ensure consistent contributions to organic matter degradation and nutrient cycling regardless of environmental fluctuations.