Host species and body site equally impact microbiome structure between sympatric Atlantic sea cucumber species

Abstract

Sea cucumbers are key members in the marine ecosystem, food webs, and support valuable commercial fisheries, yet their microbiomes, which likely influence host health and function, are relatively understudied. There is specifically a paucity of microbiome studies of echinoderm coelomic fluid (CF), which is centrally involved in circulation, digestion, and immunity. This study analyzed the microbiomes of two sympatric holothurians (sea cucumbers), Leptosynapta tenuis, and Sclerodactyla briareus, found in coastal, temperate waters of the Northeast Atlantic. First, we found unexpectedly high levels (approaching 107 cells/ml) of prokaryotic-sized cells in the coelomic fluid of the sympatric sea star Asterias forbesi. Amplicon sequencing of the 16S rRNA gene revealed significant differences in alpha and beta diversity of sea cucumber microbiomes. This included differences in CF communities between the two sea cucumber species and among body sites--CF, epidermis, and gut--of S. briareus. Host and body sites explained roughly equal amounts of microbial community variation (22% and 27%, respectively). We identified particular taxa associated with differences in community composition, including enrichment of anaerobic taxa (e.g., Desulftobacterota) in gut samples and Proteobacteria (including Burkholderiales and Pseudomonadales) in epidermis samples. We also uncovered higher levels of Synechococcales cyanobacteria in CF relative to the gut, epidermis, and background seawater samples. CF is thought to exchange with surrounding seawater, so these results highlight an apparent selective retention of CF microbial communities. This work adds to our growing knowledge of echinoderm microbiomes and highlights the need for additional surveys of their microbiomes. ImportanceMicrobiomes influence the function and health of animal hosts, but basic characterization of sea cucumber microbiomes is lacking. Furthermore, there are few studies on the microbiomes of echinoderm coelomic fluid that interacts with the respiratory, digestion, locomotion, and reproduction systems of these animals. To fill these gaps in knowledge, we analyzed the microbiomes of two sea cucumber and one sea star species from the North Atlantic. We found unexpectedly high abundances of bacteria-sized cells in the coelomic fluid of all three species. Using DNA sequencing, we uncovered differences in bacterial communities across the two sea cucumber species and across body sites (the epidermis, gut, and coelomic fluid) within one host species. This is consistent with patterns of host and body-site specificity seen in animal other microbiome studies. These results build important information for sea cucumbers that play important roles in natural marine ecosystems and support globally important fisheries.