Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring
Abstract
:1. Introduction
2. Materials and Methods
2.1. Culturing of PST-Producing Alexandrium catenella
2.2. Exposure of P. yessoensis to PST-Producing A. catenella
2.3. Measurement of the PST Concentration and Toxicity
2.4. Transcriptome Analysis of the Digestive Gland in P. yessoensis Exposed to PST-Producing A. catenella
2.5. Screening and Characterization of the Candidate Biomarker Gene in P. yessoensis for PST Monitoring
2.6. Verification of the Candidate Biomarker Gene in C. farreri
3. Results
3.1. PST Composition and DEGs in the Digestive Gland of P. yessoensis after A. catenella Exposure
3.2. Screening and Characterization of the Biomarker Gene for PST Monitoring in P. yessoensis
3.3. Correlation of PyC1QL4-1 Homologs Expression and PST Accumulation in C. farreri
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Whittle, K.; Gallacher, S. Marine toxins. Br. Med. Bull. 2000, 56, 236–253. [Google Scholar] [CrossRef] [PubMed]
- Kleinteich, J.; Wood, S.A.; Puddick, J.; Schleheck, D.; Küpper, F.C.; Dietrich, D. Potent toxins in Arctic environments--presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems. Chem. Biol. Interact. 2013, 206, 423–431. [Google Scholar] [CrossRef] [PubMed]
- McLeroy, S. Paralytic shellfish poisoning: Seafood safety and human health perspectives. Toxicon 2010, 56, 108–122. [Google Scholar] [CrossRef]
- Hodgson, E. Toxins and venoms. Prog. Mol. Biol. Transl. Sci. 2012, 112, 373–415. [Google Scholar] [CrossRef] [PubMed]
- Raposo, M.I.C.; Gomes, M.; Botelho, M.J.; Rudnitskaya, A. Paralytic shellfish toxins (PST)-transforming enzymes: A review. Toxins 2020, 12, 334. [Google Scholar] [CrossRef]
- Berdalet, E.; Fleming, L.E.; Gowen, R.; Davidson, K.; Hess, P.; Backer, L.C.; Moore, S.K.; Hoagland, P.; Enevoldsen, H. Marine harmful algal blooms, human health and wellbeing: Challenges and opportunities in the 21st century. J. Mar. Biol. Assoc. UK 2015, 2015, 61–91. [Google Scholar] [CrossRef]
- Dorner, B.; Zeleny, R.; Harju, K.; Hennekinne, J.-A.; Vanninen, P.; Schimmel, H.; Rummel, A. Biological toxins of potential bioterrorism risk: Current status of detection and identification technology. TrAC Trends Anal. Chem. 2016, 85, 89–102. [Google Scholar] [CrossRef]
- Toyofuku, H. Joint FAO/WHO/IOC activities to provide scientific advice on marine biotoxins (research report). Mar. Pollut. Bull. 2006, 52, 1735–1745. [Google Scholar] [CrossRef]
- Andres, J.K.; Yñiguez, A.; Maister, J.; Turner, A.; Olano, D.; Mendoza, J.; Salvador-Reyes, L.; Azanza, R. Paralytic shellfish toxin uptake, assimilation, depuration, and transformation in the Southeast Asian Green-Lipped Mussel (Perna viridis). Toxins 2019, 11, 468. [Google Scholar] [CrossRef]
- Wright, J. Dealing with seafood toxins: Present approaches and future options. Food Res. Int. 1995, 28, 347–358. [Google Scholar] [CrossRef]
- Gonzalez, J.C.; Leira, F.; Fontal, O.; Vieytes, M.; Arévalo, F.; Vieites, J.; Bermúdez-Puente, M.; Muñiz, S.; Salgado, C.; Yasumoto, T.; et al. Inter-laboratory validation of the fluorescent protein phosphatase inhibition assay to determine diarrhetic shellfish toxins: Intercomparison with liquid chromatography and mouse bioassay. Anal. Chim. Acta 2002, 466, 233–246. [Google Scholar] [CrossRef]
- Usleber, E.; Donald, M.; Straka, M.; Märtlbauer, E. Comparison of enzyme immunoassay and mouse bioassay for determining paralytic shellfish poisoning toxins in shellfish. Food Addit. Contam. 1997, 14, 193–198. [Google Scholar] [CrossRef]
- Cusick, K.D.; Sayler, G.S. An overview on the marine neurotoxin, saxitoxin: Genetics, molecular targets, methods of detection and ecological functions. Mar. Drugs 2013, 11, 991–1018. [Google Scholar] [CrossRef] [PubMed]
- Bodero, M.; Gerssen, A.; Portier, L.; Klijnstra, M.D.; Hoogenboom, R.; Guzmán, L.; Hendriksen, P.J.M.; Bovee, T.F.H. A Strategy to replace the mouse bioassay for detecting and identifying lipophilic marine biotoxins by combining the neuro-2a bioassay and LC-MS/MS analysis. Mar. Drugs 2018, 16, 501. [Google Scholar] [CrossRef]
- Sullivan, J.; Wekell, M.; Kentala, L. Application of HPLC for the determination of PSP toxins in shellfish. J. Food Sci. 2006, 50, 26–29. [Google Scholar] [CrossRef]
- Watanabe, R.; Matsushima, R.; Harada, T.; Oikawa, H.; Murata, M.; Suzuki, T. Quantitative determination of paralytic shellfish toxins in cultured toxic algae by LC-MS/MS. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2013, 30, 1351–1357. [Google Scholar] [CrossRef]
- Paix, B.; Othmani, A.; Debroas, D.; Culioli, G.; Briand, J.F. Temporal covariation of epibacterial community and surface metabolome in the Mediterranean seaweed holobiont Taonia atomaria. Environ. Microbiol. 2019, 21, 3346–3363. [Google Scholar] [CrossRef]
- KarSoon, T.; Liu, H.; Ye, T.; Ma, H.; Li, S.; Zheng, H. Growth, survival and lipid composition of Crassostrea gigas, C. angulata and their reciprocal hybrids cultured in southern China. Aquaculture 2019, 516, 734524. [Google Scholar] [CrossRef]
- KarSoon, T.; Zhang, H.; Liu, H.; Cheng, D.; Ye, T.; Ma, H.; Li, S.; Zheng, H. Enhancing lipid nutritional quality of oysters by hybridization between Crassostrea gigas and C. angulata. Aquac. Res. 2019, 50, 3776–3782. [Google Scholar] [CrossRef]
- Zhao, W.; Shen, H. A statistical analysis of China’s fisheries in the 12th five-year period. Aquac. Fish. 2016, 1, 41–49. [Google Scholar] [CrossRef]
- Meng, D.; Shi, J.; Li, M.; Wei, Z.; Wang, Y.; Xu, Y.; Li, Y.; Bao, Z.; Hu, X. Identification of monitoring organ in bivalves for early warning of paralytic shellfish toxins accumulation. J. Ocean Univ. China 2023, 22, 251–257. [Google Scholar] [CrossRef]
- Li, Y.; Xiaoqing, S.; Hu, X.; Xun, X.; Zhang, J.; Guo, X.; Jiao, W.; Zhang, L.; Liu, W.; Wang, J.; et al. Scallop genome reveals molecular adaptations to semi-sessile life and neurotoxins. Nat. Commun. 2017, 8, 1721. [Google Scholar] [CrossRef] [PubMed]
- Fabioux, C.; Sulistiyani, Y.; Haberkorn, H.; Hégaret, H.; Amzil, Z.; Soudant, P. Exposure to toxic Alexandrium minutum activates the detoxifying and antioxidant systems in gills of the oyster Crassostrea gigas. Harmful Algae 2015, 48, 55–62. [Google Scholar] [CrossRef]
- Qiu, J.; Ma, F.; Fan, H.; Aifeng, L. Effects of feeding Alexandrium tamarense, a paralytic shellfish toxin producer, on antioxidant enzymes in scallops (Patinopecten yessoensis) and mussels (Mytilus galloprovincialis). Aquaculture 2013, 396, 76–81. [Google Scholar] [CrossRef]
- Cao, R.; Wang, D.; Wei, Q.; Wang, Q.; Yang, D.; Liu, H.; Dong, Z.; Zhang, X.; Zhang, Q.; Zhao, J. Integrative biomarker assessment of the influence of saxitoxin on marine bivalves: A comparative study of the two bivalve species oysters, Crassostrea gigas, and scallops, Chlamys farreri. Front. Physiol. 2018, 9, 1173. [Google Scholar] [CrossRef] [PubMed]
- Lian, S.; Zhao, L.; Xun, X.; Lou, J.; Li, M.; Li, X.; Wang, S.; Zhang, L.; Hu, X.; Bao, Z. Genome-wide identification and characterization of SODs in Zhikong scallop reveals gene expansion and regulation divergence after toxic dinoflagellate exposure. Mar. Drugs 2019, 17, 700. [Google Scholar] [CrossRef]
- Li, M.; Wang, Y.; Tang, Z.; Wang, H.; Hu, J.; Bao, Z.; Hu, X. Expression plasticity of Peroxisomal acyl-coenzyme A oxidase genes implies their involvement in redox regulation in scallops exposed to PST-producing Alexandrium. Mar. Drugs 2022, 20, 472. [Google Scholar] [CrossRef]
- Lou, J.; Cheng, J.; Xun, X.; Li, X.; Li, M.; Zhang, X.; Li, T.; Bao, Z.; Hu, X. Glutathione S-transferase genes in scallops and their diverse expression patterns after exposure to PST-producing dinoflagellates. Mar. Life Sci. Technol. 2020, 2, 252–261. [Google Scholar] [CrossRef]
- Hu, X.; Bao, Z.; Hu, J.; Shao, M.; Zhang, L.; Bi, K.; Zhan, A.; Huang, X. Cloning and characterization of tryptophan 2,3- dioxygenase gene of Zhikong scallop Chlamys farreri (Jones and Preston 1904). Aquac. Res. 2006, 37, 1187–1194. [Google Scholar] [CrossRef]
- Wang, S.; Zhang, J.; Jiao, W.; Li, J.; Xun, X.; Sun, Y.; Guo, X.; Huan, P.; Dong, B.; Zhang, L.; et al. Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat. Ecol. Evol. 2017, 1, 120. [Google Scholar] [CrossRef]
- Anders, S.; Pyl, P.T.; Huber, W. HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 2015, 31, 166–169. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Yang, P.; Jiang, F.; Wei, Y.; Ma, Z.; Kang, L. De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS ONE 2010, 5, e15633. [Google Scholar] [CrossRef] [PubMed]
- Ning, X.; Li, X.; Wang, J.; Zhang, X.; Bao, Z.J.A. Genome-wide association study reveals E2F3 as a candidate gene for scallop growth. Aquaculture 2019, 511, 734216. [Google Scholar] [CrossRef]
- Schultz, J.; Milpetz, F.; Bork, P.; Ponting, C.P. SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl. Acad. Sci. USA 1998, 95, 5857–5864. [Google Scholar] [CrossRef]
- Liu, W.; Xie, Y.; Ma, J.; Luo, X.; Nie, P.; Zuo, Z.; Lahrmann, U.; Zhao, Q.; Zheng, Y.; Zhao, Y.; et al. IBS: An illustrator for the presentation and visualization of biological sequences. Bioinformatics 2015, 31, 3359–3361. [Google Scholar] [CrossRef]
- Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28, 1647–1649. [Google Scholar] [CrossRef]
- Sharifi, J.; St Germain, D.L. The cDNA for the type I iodothyronine 5′-deiodinase encodes an enzyme manifesting both high Km and low Km activity. Evidence that rat liver and kidney contain a single enzyme which converts thyroxine to 3,5,3′-triiodothyronine. J. Biol. Chem. 1992, 267, 12539–12544. [Google Scholar] [CrossRef]
- Rosen, D.R.; Siddique, T.; Patterson, D.; Figlewicz, D.A.; Sapp, P.; Hentati, A.; Donaldson, D.; Goto, J.; O’Regan, J.P.; Deng, H.X.; et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362, 59–62. [Google Scholar] [CrossRef]
- Kishore, U.; Reid, K.B. C1q: Structure, function, and receptors. Immunopharmacology 2000, 49, 159–170. [Google Scholar] [CrossRef]
- Leite, R.B.; Milan, M.; Coppe, A.; Bortoluzzi, S.; dos Anjos, A.; Reinhardt, R.; Saavedra, C.; Patarnello, T.; Cancela, M.L.; Bargelloni, L. mRNA-seq and microarray development for the grooved carpet shell clam, Ruditapes decussatus: A functional approach to unravel host-parasite interaction. BMC Genom. 2013, 14, 741. [Google Scholar] [CrossRef]
- He, L.; He, T.; Farrar, S.; Ji, L.; Liu, T.; Ma, X. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol. Biochem. 2017, 44, 532–553. [Google Scholar] [CrossRef] [PubMed]
- Papageorgiou, A.P.; Heymans, S. Peroxidasin-like protein: Expanding the horizons of matrix biology. Cardiovasc. Res. 2014, 101, 342–343. [Google Scholar] [CrossRef] [PubMed]
- Reddy, J.K.; Hashimoto, T. Peroxisomal beta-oxidation and peroxisome proliferator-activated receptor alpha: An adaptive metabolic system. Annu. Rev. Nutr. 2001, 21, 193–230. [Google Scholar] [CrossRef] [PubMed]
- Cheon, Y.H.; Lee, C.H.; Jeong, D.H.; Kwak, S.C.; Kim, S.; Lee, M.S.; Kim, J.Y. Dual oxidase maturation factor 1 positively regulates RANKL-Induced osteoclastogenesis via activating reactive oxygen species and TRAF6-mediated signaling. Int. J. Mol. Sci. 2020, 21, 6416. [Google Scholar] [CrossRef] [PubMed]
- Salminen, A. Role of indoleamine 2,3-dioxygenase 1 (IDO1) and kynurenine pathway in the regulation of the aging process. Ageing Res. Rev. 2022, 75, 101573. [Google Scholar] [CrossRef]
- Bianco, A.C.; Dumitrescu, A.; Gereben, B.; Ribeiro, M.O.; Fonseca, T.L.; Fernandes, G.W.; Bocco, B. Paradigms of dynamic control of thyroid hormone signaling. Endocr. Rev. 2019, 40, 1000–1047. [Google Scholar] [CrossRef]
- Mullur, R.; Liu, Y.Y.; Brent, G.A. Thyroid hormone regulation of metabolism. Physiol. Rev. 2014, 94, 355–382. [Google Scholar] [CrossRef]
- Hong, M. Biochemical studies on the structure-function relationship of major drug transporters in the ATP-binding cassette family and solute carrier family. Adv. Drug Deliv. Rev. 2017, 116, 3–20. [Google Scholar] [CrossRef]
- Canada, A.T.; Calabrese, E.J. Superoxide dismutase: Its role in xenobiotic detoxification. Pharmacol. Ther. 1989, 44, 285–295. [Google Scholar] [CrossRef]
- Long, R.; Liu, Z.; Li, J.; Yu, H. COL6A6 interacted with P4HA3 to suppress the growth and metastasis of pituitary adenoma via blocking PI3K-Akt pathway. Aging 2019, 11, 8845–8859. [Google Scholar] [CrossRef]
- Campbell, K.; Vilarino, N.; Botana, L.; Elliott, C. A European perspective on progress in moving away from the mouse bioassay for marine-toxin analysis. TrAC Trends Anal. Chem. 2011, 30, 239–253. [Google Scholar] [CrossRef]
- Kahl, K.; Seither, J.; Reidy, L. LC-MS-MS vs ELISA: Validation of a comprehensive urine toxicology screen by LC-MS-MS and a comparison of 100 forensic specimens. J. Anal. Toxicol. 2019, 43, 734–745. [Google Scholar] [CrossRef] [PubMed]
- Puszkiel, A.; Noé, G.; Boudou-Rouquette, P.; Cossec, C.; Jennifer, A.; Giraud, J.-S.; Thomas-Schoemann, A.; Alexandre, J.; Vidal, M.; Goldwasser, F.; et al. Development and validation of an ELISA method for the quantification of nivolumab in plasma from non-small-cell lung cancer patients. J. Pharm. Biomed. Anal. 2017, 139, 30–36. [Google Scholar] [CrossRef]
- Botana, L. A perspective on the toxicology of marine toxins. Chem. Res. Toxicol. 2012, 25, 1800–1804. [Google Scholar] [CrossRef] [PubMed]
- Khatib, L.A.; Tsai, Y.L.; Olson, B. A biomarker for the identification of cattle fecal pollution in water using the LTIIa toxin gene from enterotoxigenic Escherichia coli. Appl. Microbiol. Biotechnol. 2002, 59, 97–104. [Google Scholar] [CrossRef] [PubMed]
- Xu, K.; Wang, Y.; Lian, S.; Hu, N.; Chen, X.; Dai, X.; Zhang, L.; Wang, S.; Hu, X.; Hu, X.; et al. Expansion of C1Q Genes in Zhikong scallop and their expression profiling after exposure to the toxic dinoflagellates. Front. Mar. Sci. 2021, 8, 640425. [Google Scholar] [CrossRef]
- Wu, H.Y.; Zhang, F.; Dong, C.F.; Zheng, G.C.; Zhang, Z.H.; Zhang, Y.Y.; Tan, Z.J. Variations in the toxicity and condition index of five bivalve species throughout a red tide event caused by Alexandrium catenella: A field study. Environ. Res. 2022, 215, 114327. [Google Scholar] [CrossRef]
Toxins | Relative Toxicity |
---|---|
STX | 1 |
GTX1 | 0.994 |
neoSTX | 0.9243 |
GTX4 | 0.7261 |
GTX3 | 0.6379 |
GTX2 | 0.3592 |
C2 | 0.0963 |
GTX6 | 0.06 |
C1 | 0.006 |
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Zhang, X.; Xun, X.; Meng, D.; Li, M.; Chang, L.; Shi, J.; Ding, W.; Sun, Y.; Wang, H.; Bao, Z.; et al. Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring. Antioxidants 2023, 12, 1150. https://doi.org/10.3390/antiox12061150
Zhang X, Xun X, Meng D, Li M, Chang L, Shi J, Ding W, Sun Y, Wang H, Bao Z, et al. Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring. Antioxidants. 2023; 12(6):1150. https://doi.org/10.3390/antiox12061150
Chicago/Turabian StyleZhang, Xiangchao, Xiaogang Xun, Deting Meng, Moli Li, Lirong Chang, Jiaoxia Shi, Wei Ding, Yue Sun, Huizhen Wang, Zhenmin Bao, and et al. 2023. "Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring" Antioxidants 12, no. 6: 1150. https://doi.org/10.3390/antiox12061150
APA StyleZhang, X., Xun, X., Meng, D., Li, M., Chang, L., Shi, J., Ding, W., Sun, Y., Wang, H., Bao, Z., & Hu, X. (2023). Transcriptome Analysis Reveals the Genes Involved in Oxidative Stress Responses of Scallop to PST-Producing Algae and a Candidate Biomarker for PST Monitoring. Antioxidants, 12(6), 1150. https://doi.org/10.3390/antiox12061150