Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring

Abstract

Paralytic shellfish toxins (PST) could be accumulated in bivalves and cause safety problems. To protect public health, bivalves are examined for PST contamination before entering the market, usually by high-performance liquid chromatography (HPLC) or LC-tandem mass spectrometry (LC-MS/MS) in the lab, which needs PST standards not all available and is time-consuming for large sample sizes. To detect PST toxicity in bivalves rapidly and sensitively, a biomarker gene is highly demanded, but the related study is very limited. In this study, we fed a commercially important bivalve, Patinopecten yessoensis, with the PST-producing dinoflagellate Alexandrium catenella. After 1, 3, and 5 days of exposure, both PST concentrations and toxicity levels in the digestive gland continuously increased. Transcriptome analysis revealed that the differentially expressed genes were significantly enriched in oxidation-reduction process, which included the cytochrome P450 genes (CYPs), type I iodothyronine deiodinase (IOD1s), peroxidasin (PXDN), and acyl-Coenzyme A oxidase 1 (ACOX1) at day 1 and a superoxide dismutase (SOD) at day 5, highlighting the crucial roles of these genes in response to oxidative stress induced by PST. Among the 33 continuously upregulated genes, five showed a significant correlation between gene expression and PST concentration, with the highest correlation present in PyC1QL4-1, the gene encoding Complement C1Q-like protein 4, C1QL4. In addition, the correlation between PyC1QL4-1 expression and PST toxicity was also the highest. Further analysis in another aquaculture scallop (Chlamys farreri) indicated that the expression of CfC1QL4-1, the homolog of PyC1QL4-1, also exhibited significant correlations with both PST toxicity and concentration. Our results reveal the gene expression responses of scallop digestive glands to PST-producing algae and indicate that the C1QL4-1 gene might be a potential biomarker for PST monitoring in scallops, which may provide a convenient way for the early warning and sensitive detection of PST contamination in the bivalves.