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

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...

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Main Authors: Xiangchao Zhang, Xiaogang Xun, Deting Meng, Moli Li, Lirong Chang, Jiaoxia Shi, Wei Ding, Yue Sun, Huizhen Wang, Zhenmin Bao, Xiaoli Hu
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/12/6/1150
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author Xiangchao Zhang
Xiaogang Xun
Deting Meng
Moli Li
Lirong Chang
Jiaoxia Shi
Wei Ding
Yue Sun
Huizhen Wang
Zhenmin Bao
Xiaoli Hu
author_facet Xiangchao Zhang
Xiaogang Xun
Deting Meng
Moli Li
Lirong Chang
Jiaoxia Shi
Wei Ding
Yue Sun
Huizhen Wang
Zhenmin Bao
Xiaoli Hu
author_sort Xiangchao Zhang
collection DOAJ
description 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, <i>Patinopecten yessoensis</i>, with the PST-producing dinoflagellate <i>Alexandrium catenella</i>. 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 (<i>CYP</i>s), type I iodothyronine deiodinase (<i>IOD1</i>s), peroxidasin (<i>PXDN</i>), and acyl-Coenzyme A oxidase 1 (<i>ACOX1</i>) at day 1 and a superoxide dismutase (<i>SOD</i>) 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 <i>PyC1QL4-1</i>, the gene encoding Complement C1Q-like protein 4, C1QL4. In addition, the correlation between <i>PyC1QL4-1</i> expression and PST toxicity was also the highest. Further analysis in another aquaculture scallop (<i>Chlamys farreri</i>) indicated that the expression of <i>CfC1QL4-1</i>, the homolog of <i>PyC1QL4-1</i>, 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 <i>C1QL4-1</i> 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.
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spelling doaj.art-2eb1dd978a3243b695f286d6c29954d42023-11-18T09:02:08ZengMDPI AGAntioxidants2076-39212023-05-01126115010.3390/antiox12061150Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST MonitoringXiangchao Zhang0Xiaogang Xun1Deting Meng2Moli Li3Lirong Chang4Jiaoxia Shi5Wei Ding6Yue Sun7Huizhen Wang8Zhenmin Bao9Xiaoli Hu10MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaParalytic 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, <i>Patinopecten yessoensis</i>, with the PST-producing dinoflagellate <i>Alexandrium catenella</i>. 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 (<i>CYP</i>s), type I iodothyronine deiodinase (<i>IOD1</i>s), peroxidasin (<i>PXDN</i>), and acyl-Coenzyme A oxidase 1 (<i>ACOX1</i>) at day 1 and a superoxide dismutase (<i>SOD</i>) 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 <i>PyC1QL4-1</i>, the gene encoding Complement C1Q-like protein 4, C1QL4. In addition, the correlation between <i>PyC1QL4-1</i> expression and PST toxicity was also the highest. Further analysis in another aquaculture scallop (<i>Chlamys farreri</i>) indicated that the expression of <i>CfC1QL4-1</i>, the homolog of <i>PyC1QL4-1</i>, 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 <i>C1QL4-1</i> 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.https://www.mdpi.com/2076-3921/12/6/1150paralytic shellfish toxinsscallopdigestive glandsoxidative stress<i>C1QL4</i>biomarker
spellingShingle Xiangchao Zhang
Xiaogang Xun
Deting Meng
Moli Li
Lirong Chang
Jiaoxia Shi
Wei Ding
Yue Sun
Huizhen Wang
Zhenmin Bao
Xiaoli Hu
Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring
Antioxidants
paralytic shellfish toxins
scallop
digestive glands
oxidative stress
<i>C1QL4</i>
biomarker
title Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring
title_full Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring
title_fullStr Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring
title_full_unstemmed Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring
title_short Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring
title_sort transcriptome analysis reveals the genes involved in oxidative stress responses of scallop to pst producing algae and a candidate biomarker for pst monitoring
topic paralytic shellfish toxins
scallop
digestive glands
oxidative stress
<i>C1QL4</i>
biomarker
url https://www.mdpi.com/2076-3921/12/6/1150
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