Repeated selective enrichment process of sediment microbiota occurred in sea cucumber guts

Abstract

Deposit-feeding sea cucumbers repeat ingestion of sediments and excretion of faeces daily and consequently increase bacterial abundance in sediments and promote organic matter mineralization. Such ecological roles are expected to be collaborative activities of sea cucumbers and the gut microbiota. Here, we performed a spatiotemporally broad 16S rRNA gene analysis using 109 samples from sea cucumber faeces and habitat sediments to explore potential contribution of their gut microbiota to the ecological roles. Most operational taxonomic units (OTUs) observed in the faecal samples were shared with the sediment samples, nevertheless faecal and sediment microbiota differed from each other in UniFrac analysis. Lower bacterial diversity and increased relative abundance of specific OTUs in the faecal microbiota strongly suggest selective enrichment of ingested sediment microbiota in their guts. Interestingly, representative faecal OTUs were more abundant in sea cucumber-populated sediments than in un-inhabited sediments, indicating bacteria selectively enriched in the guts were spread on ambient sediments via faeces. Moreover, the predicted microbial community metabolic potential showed a higher abundance of genes related to carbohydrate and xenobiotics metabolisms in faeces than in sediments. Our study suggests the repeated selective enrichment transforms ambient sediment microbial communities and maintains the host's ecological roles by promoting organic matter mineralization.

Tracking the dynamics of individual gut microbiome of sea cucumber Apostichopus japonicus during gut regeneration

“…Aquatic animals are more likely to live in water environments involving multiple perturbation factors compared to those of humans, however, resilience of gut microbiota at individual level on a fine temporal scale has not been fully tested yet due to a lack of methodology. Using individual microbiome methodology (Yamazaki et al, 2016(Yamazaki et al, , 2019(Yamazaki et al, , 2020) and a gut-regenerating animal model of sea cucumber A. japonicus, which is located on a deep branch of Deuterostomia, we succeeded in tracking the individuality of the gut microbiome in marine invertebrate animals during the organ regeneration process under both open water and laboratory conditions. Firstly, we tested whether resilience of gut microbiomes of sea cucumber can be observed tracking individual gut microbiome dynamics during gut regeneration using caged wild animals.…”

“…1B), which indicates that feeding behaviors of sea cucumbers became active at that time. Such short-time reconstruction of the gut microbiomes might suggest immediate recovery of holobiont functions which benefit the host via microbial metabolisms such as degradation and mineralization of ingested algae and organic matter (Gao et al, 2014;Yamazaki et al, 2019;2020). Unfortunately, we could not perform fine temporal scale sampling using wild animals at that time in 2016 due to the severe winter ocean conditions around this area.…”

“…Secondly, we tested individuality under a laboratory set up using an isolator. As the gut microbiome of A. japonicus is shaped by ingested sedimentary materials (Yamazaki et al, 2019), to avoid cross-contamination of the other individual microbiomes, we set up a laboratory isolator to feed individual animals and monitor daily gut microbiome dynamics. Before starting the experiments, we expected the individual fecal microbiota at the same regeneration stage would be grouped to each other as reported by Zhang et al (2019), but our study using isolators did not show such trends during the 28 day regeneration experiments (Fig.…”

“…(1) Rhodobacterales bacteria were also enriched in sea cucumber guts (Yamazaki et al, 2019); (2) they were more abundant in larger size individuals than in smaller size ones (Yamazaki et al, 2016); (3) potential probiotics, Paracoccus marcusii, have been reported based on their effects on host growth and immune stimulation after treatment with diets (Yan et al, 2014;Yang et al, 2015). Interestingly, two key features affiliated to Rhodobacteraceae responding to gut regeneration were extracted; one was related to an uncultured clone, of which the roles are currently difficult to be estimated (Sunagawa et al, 2009), but the other was likely to be affiliated to S. pontiacus.…”

“…Tracking the individuality and resilience of human gut microbiomes and/or those of other terrestrial animals after external pertubations (e.g., antibiotics) have been established in monitoring feces microbiomes, but there have been few studies analyzing those of aquatic animals including sea cucumber due to the difficulties of taking fresh feces samples under-water and to purify the DNA of small animals including juveniles. A recently developed approach designed "individual microbiome analysis" taking feces sample of cultured sea cucumbers on-site without sacrificing animals reveals (1) significant abundance of specific taxa belonging to Rhodobacterales possessing PHB metabolism in larger individuals of A. japonicus (Yamazaki et al, 2016), and (2) continuous selective enrichments of ingested microbes from environmental sediments as a driving force in shaping the gut microbiomes of wild sea cucumbers in Japan (Yamazaki et al, 2019). Using the individual microbiome approach, new insights into the structure and functional dynamics of sea cucumber gut microbiomes have quickly come to light.…”