Compartment-Specific Differentiation of Bacterial Communities in the Sea Cucumber Holothuria leucospilota from the South China Sea

While the gut bacterial communities of sea cucumbers have been extensively studied, the extent to which environmental filtering may shape bacterial assembly across different host compartments remains poorly understood. This study employed Illumina MiSeq high-throughput sequencing technology to investigate the bacterial communities in environmental sediments (E), body epidermis (B), foregut (F) and hindgut (H) samples of Holothuria leucospilota (n = 4 per group) from the South China Sea. A total of 749,222 high-quality 16S rRNA sequences were dereplicated into 911 amplicon sequence variants (ASVs). Alpha diversity revealed that environmental sediments exhibited the highest diversity among the four samples (Shannon index: 7.33 ± 0.11). Beta-diversity analysis revealed pronounced differentiation in bacterial community structure among sample types. Proteobacteria, Bacteroidetes, and Firmicutes were the dominant bacterial phyla. The bacterial taxonomic composition across compartments of H. leucospilota varied considerably. Woeseia was not detected from host niches but was present only in environmental sediments. The genus Vibrio dominated in environmental sediments and foregut samples. The epidermal bacterial communities were characterized by the prevalence of the NS11-12 marine group, Rhodobacteraceae, and Rhizobiaceae. The distinct successional gradient observed in Woeseia, Vibrio, and Pseudomonas suggested that bacterial colonization of the gut is consistent with selective environmental filtering. Functional annotation (KEGG) indicated dominance in core metabolic pathways, particularly carbohydrate and amino acid degradation, revealing complementary metabolic functions among dominant taxa with the potential for metabolic niche partitioning to support host energy harvest. Our findings provide a baseline framework that may assist in future screening of probiotic candidates and disease management strategies, pending experimental validation of the functional roles of the identified taxa.