Zhao Z et al. (2022), Sea Cucumber Body Vesicular Syndrome Is Driven ...

ECB-ART-50377

mSystems 2022 Jun 28;73:e0135721. doi: 10.1128/msystems.01357-21.

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Sea Cucumber Body Vesicular Syndrome Is Driven by the Pond Water Microbiome via an Altered Gut Microbiota.

Zhao Z , Jiang J , Pan Y , Dong Y , Wang B , Gao S , Chen Z , Guan X , Wang X , Zhou Z .

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Apostichopus japonicus (sea cucumber) is one of the most valuable aquaculture species in China; however, different diseases can limit its economic development. Recently, a novel disease, body vesicular syndrome (BVS), was observed in A. japonicus aquaculture. Diseased animals displayed no obvious phenotypic characteristics; however, after boiling at the postharvest stage, blisters, lysis, and body ruptures appeared. In this study, a multiomics strategy incorporating analysis of the gut microbiota, the pond microbiome, and A. japonicus genotype was established to investigate BVS. Detailed analyses of differentially expressed proteins (DEPs) and metabolites suggested that changes in cell adhesion structures, caused by disordered fatty acid β-oxidation mediated by vitamin B5 deficiency, could be a putative BVS mechanism. Furthermore, intestinal dysbacteriosis due to microbiome variations in pond water was considered a potential reason for vitamin B5 deficiency. Our BVS index, based on biomarkers identified from the A. japonicus gut microbiota, was a useful tool for BVS diagnosis. Finally, vitamin B5 supplementation was successfully used to treat BVS, suggesting an association with BVS etiology. IMPORTANCE Body vesicular syndrome (BVS) is a novel disease in sea cucumber aquaculture. As no phenotypic features are visible, BVS is difficult to confirm during aquaculture and postharvest activities, until animals are boiled. Therefore, BVS could lead to severe economic losses compared with other diseases in sea cucumber aquaculture. In this study, for the first time, we systematically investigated BVS pathogenesis and proposed an effective treatment for the condition. Moreover, based on the gut microbiota, we established a noninvasive diagnostic method for BVS in sea cucumber.

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	FIG 1. Study information. (a) Morphological differences in healthy and BVS A. japonicus animals after boiling. (b) Multiomics study framework showing the investigation of BVS molecular mechanisms and the identification of biomarkers related to BVS diagnosis. (c) Basic information on A. japonicus culture ponds in this study.
	FIG 2. Proteomic and metabolic response profiles for BVS in A. japonicus. PLS-DA identified changes in proteomic (a) and metabolic (b) profiles in BW and CF samples between healthy and BVS animals. Points with different shapes and colors denote different samples. The numbers of DEPs (c) and DAMs (d) in BW and CF samples between healthy and BVS animals. Red and blue numbers correspond to proteins and metabolites upregulated in BVS and healthy animals. KEGG enrichment analysis based on DEPs (e) and DAMs (f) in BW and CF samples between healthy and BVS animals. The dot size denotes the numbers of genes in each pathway related to DEPs or DAMs in different samples. Only data with adjusted P values of <0.05 are shown.
	FIG 3. Focal adhesion processes are associated with BVS morphological characteristics. (a) Conceptual framework of focal adhesion processes and related proteins. (b to f) Proteins associated with different components of focal adhesion processes downregulated in the CF of BVS animals compared with healthy animals. (g to k) Proteins associated with different components of focal adhesion processes downregulated in the BW of BVS animals compared with healthy animals. **, P < 0.05. (l and m) BW of healthy and BVS animals under high-resolution microscopy (bar = 2 μm). (n and o) BW of healthy and BVS animals under light microscopy after H&E staining (bar = 50 μm).
	FIG 4. The metabolomic identification of disordered fatty acid metabolism in BVS A. japonicus. Different DAM classes identified in CF (a) and BW (b) samples between healthy and BVS A. japonicus. (c to e) Metabolites associated with energy production that were downregulated in the BW of BVS A. japonicus compared with healthy animals. (f to k) Metabolites associated with disordered fatty acid metabolism that were differentially expressed in the CF and BW of BVS A. japonicus compared with healthy animals. (l and m) Variations in vitamin B5 levels in CF and BW samples from healthy and BVS A. japonicus. **, P < 0.05.
	FIG 5. Associations between gut microbiota and host metabolism in A. japonicus with BVS. (a to d) Metabolites associated with disordered sphingolipid metabolism that were differentially expressed in CF and BW of BVS A. japonicus compared with healthy animals. (e and f) Metabolites associated with disordered bile acid metabolism that were differentially expressed in the CF and BW of BVS A. japonicus compared with healthy animals. **, P < 0.05.
	FIG 6. Associations between microbial communities and BVS in A. japonicus. (a) Biomarkers identifying gut microbiota and the disease index for BVS diagnosis. (b) ROC curves evaluating accuracy, susceptibility, and diagnosis thresholds for A. japonicus with BVS. (c) Ratio of gut microbiotas sourced from water and sediments in culture ponds. (d) Ratio differences in water-sourced microbes between the gut microbiotas in BVS and healthy A. japonicus. (e) Ratio differences in sediment-sourced microbes between the gut microbiotas of BVS and healthy A. japonicus. ***, P < 0.01; NS, not significant.
	FIG 7. Putative BVS mechanism in A. japonicus. (a) Conceptual framework of the putative BVS mechanism in A. japonicus. (b) Therapeutic effects of vitamin B5 supplementation on A. japonicus with BVS.

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Ahmed, Proteomics for understanding pathogenesis, immune modulation and host pathogen interactions in aquaculture. 2019, Pubmed