The role of arachidonic acid regulatory network in the metabolism of paralytic shellfish toxins in <i>Mytilus galloprovincialis</i>: based on combined transcriptome and metabolome analysis

Zhang Qianru; Tan Zhijun; Zheng Guanchao; Dong Chenfan; Yang Yuecong; Wu Haiyan

doi:10.12284/hyxb2023142

Volume 45 Issue 11

Nov. 2023

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Zhang Qianru，Tan Zhijun，Zheng Guanchao, et al. The role of arachidonic acid regulatory network in the metabolism of paralytic shellfish toxins in Mytilus galloprovincialis: based on combined transcriptome and metabolome analysis[J]. Haiyang Xuebao，2023, 45(11)：142–152 doi: 10.12284/hyxb2023142

Citation:

Zhang Qianru，Tan Zhijun，Zheng Guanchao, et al. The role of arachidonic acid regulatory network in the metabolism of paralytic shellfish toxins in Mytilus galloprovincialis: based on combined transcriptome and metabolome analysis[J]. Haiyang Xuebao，2023, 45(11)：142–152 doi: 10.12284/hyxb2023142

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The role of arachidonic acid regulatory network in the metabolism of paralytic shellfish toxins in Mytilus galloprovincialis: based on combined transcriptome and metabolome analysis

doi: 10.12284/hyxb2023142

1.
School of Food Science and Engineering, Jiangsu Ocean University, Lianyungang 222005, China
2.
Key Laboratory of Testing and Evaluation for Aquatic Product Safety and Quality, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
3.
State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China

Received Date: 2023-03-29
Rev Recd Date: 2023-07-01

Available Online: 2023-10-26

Publish Date: 2023-11-30

Abstract

Abstract

Mytilus galloprovincialis is the representative bivalve with the great ability to enrich for paralytic shellfish toxins (PSTs), however, it has been shown that exposure of Mytilus galloprovincialis to PSTs can induces an inflammatory response in the organism, while its mechanism and effects on toxin metabolism are not clear. In this study, transcriptomics and metabolomics were used to compare the differences in gene expression and metabolite content of purple mussel (M. galloprovincialis) in different periods of Alexandrium catenella bloom, in order to analyze the inflammatory response mechanism of purple mussel under the stress of PSTs. The results show that there are significantly changes in genes and metabolites expressed after exposure to PSTs, including 17 232 differentially expressed genes and 341 differentially expressed metabolites. Based on the association analysis, differentially expressed genes and metabolites are significantly enriched in the arachidonic acid and glutathione metabolic pathways, and genes PLA2G2F, ALOX5, TBXAS1 and metabolites ARA, PGH₂, TXA₂, LTA₄, 5-HETE play important roles in the pro-inflammatory response of the mussel organism; while genes GPX4, CYP2J2 and metabolites 15-HETE and GSH regulate the regression of inflammation in the organism, constituting a complex network of inflammatory regulatory signals. This study reveals that arachidonic acid-related pathways play an important regulatory role in the inflammatory response of the mussel organism, which provides a basis for further insight into the mechanism of the inflammatory network response of the mussel organism under the stress of PSTs.
- paralytic shellfish toxins,
- Mytilus galloprovincialis,
- metabolism,
- arachidonic acid,
- inflammation

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References

[1]	Xu Houguo, Meng Xiaoxue, Wei Yuliang, et al. Arachidonic acid matters[J]. Reviews in Aquaculture, 2022, 14(4): 1912−1944. doi: 10.1111/raq.12679
[2]	冀倩倩. 花生四烯酸ARA对仿刺参生长及免疫相关功能的影响[D]. 大连: 大连工业大学, 2021. Ji Qianqian. Effects of arachidonic acid on the growth and immune function of Apostichopus japonicus[D]. Dalian: Dalian Polytechnic University, 2021.
[3]	王成强, 王际英, 李宝山, 等. 饲料中花生四烯酸含量对刺参生长性能、抗氧化能力及脂肪酸代谢的影响[J]. 中国水产科学, 2018, 25(3): 555−566. doi: 10.3724/SP.J.1118.2018.17344 Wang Chengqiang, Wang Jiying, Li Baoshan, et al. Effects of dietary arachidonic acid on the growth performance, antioxidant capacity, and fatty acid metabolism of sea cucumber ( Apostichopus japonicus)[J]. Journal of Fishery Sciences of China, 2018, 25(3): 555−566. doi: 10.3724/SP.J.1118.2018.17344
[4]	Tian Jingjing, Lei Caixia, Ji Hong, et al. Dietary arachidonic acid decreases the expression of transcripts related to adipocyte development and chronic inflammation in the adipose tissue of juvenile grass carp, Ctenopharyngodon idella[J]. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 2019, 30: 122−132. doi: 10.1016/j.cbd.2019.02.006
[5]	Furne M, Holen E, Araujo P, et al. Cytokine gene expression and prostaglandin production in head kidney leukocytes isolated from Atlantic cod ( Gadus morhua) added different levels of arachidonic acid and eicosapentaenoic acid[J]. Fish & Shellfish Immunology, 2013, 34(3): 770−777.
[6]	Cho S Y, Kwon Y K, Nam M, et al. Integrated profiling of global metabolomic and transcriptomic responses to viral hemorrhagic septicemia virus infection in olive flounder[J]. Fish & Shellfish Immunology, 2017, 71: 220−229.
[7]	Abshirini M, Coad J, Wolber F M, et al. Green-lipped (greenshell™) mussel ( Perna canaliculus) extract supplementation in treatment of osteoarthritis: a systematic review[J]. Inflammopharmacology, 2021, 29(4): 925−938. doi: 10.1007/s10787-021-00801-2
[8]	赵利斌, 王鑫磊, 黄旭雄, 等. 饲料中花生四烯酸水平对凡纳滨对虾免疫相关基因表达及抗菌能力的影响[J]. 水产学报, 2016, 40(5): 763−775. Zhao Libin, Wang Xinlei, Huang Xuxiong, et al. Effects of dietary arachidonic acid on the immune-related gene expressions and Vibrio-resistant ability in Litopenaeus vannamei[J]. Journal of fisheries of China, 2016, 40(5): 763−775.
[9]	王成强, 王际英, 黄炳山, 等. 饲料花生四烯酸水平对珍珠龙胆石斑鱼幼鱼生长性能、抗氧化能力、血清生化指标以及肝脏和肌肉脂肪酸组成的影响[J]. 动物营养学报, 2018, 30(9): 3567−3580. doi: 10.3969/j.issn.1006-267x.2018.09.027 Wang Chengqiang, Wang Jiying, Huang Bingshan, et al. Effects of dietary arachidonic acid level on growth performance, antioxidant ability, serum biochemical parameters and fatty acid composition in liver and muscle of juvenile hybrid grouper ( Epinephelus fuscoguttatus♀× Epinephelus lanceolatus♂)[J]. Chinese Journal of Animal Nutrition, 2018, 30(9): 3567−3580. doi: 10.3969/j.issn.1006-267x.2018.09.027
[10]	张圆琴, 徐后国, 曹林, 等. 饲料中花生四烯酸对发育前期大菱鲆亲鱼性类固醇激素合成的影响[J]. 水产学报, 2017, 41(4): 588−601. Zhang Yuanqin, Xu Houguo, Cao Lin, et al. Effects of dietary arachidonic acid on the sex steroid hormone synthesis in turbot broodstock before maturation[J]. Journal of Fisheries of China, 2017, 41(4): 588−601.
[11]	于仁成, 罗璇. 我国近海有毒藻和藻毒素的研究现状与展望[J]. 海洋科学集刊, 2016(1): 155−166. Yu Rencheng, Luo Xuan. Status and research perspectives on toxic algae and Phycotoxins in the coastal waters of China[J]. Studia Marina Sinica, 2016(1): 155−166.
[12]	Nakatani T, Masayama A, Kiyota K, et al. Comparison between mouse bioassay and HILIC-MS/MS for quantification of paralytic shellfish toxin in Japanese basket clams and mussels caught off coastal Osaka Bay in Japan[J]. Food Additives & Contaminants: Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment, 2021, 38(11): 1969−1983.
[13]	Faggio C, Tsarpali V, Dailianis S. Mussel digestive gland as a model tissue for assessing xenobiotics: an overview[J]. Science of the Total Environment, 2018, 636: 220−229. doi: 10.1016/j.scitotenv.2018.04.264
[14]	Lassudrie M, Hégaret H, Wikfors G H, et al. Effects of marine harmful algal blooms on bivalve cellular immunity and infectious diseases: a review[J]. Developmental & Comparative Immunology, 2020, 108: 103660.
[15]	Braga A C, Pereira V, Marçal R, et al. DNA damage and oxidative stress responses of mussels Mytilus galloprovincialis to paralytic shellfish toxins under warming and acidification conditions—Elucidation on the organ-specificity[J]. Aquatic Toxicology, 2020, 228: 105619. doi: 10.1016/j.aquatox.2020.105619
[16]	Lushchak V I. Environmentally induced oxidative stress in aquatic animals[J]. Aquatic Toxicology, 2011, 101(1): 13−30. doi: 10.1016/j.aquatox.2010.10.006
[17]	Even Y, Pousse E, Chapperon C, et al. Physiological and comparative proteomic analyzes reveal immune defense response of the king scallop Pecten maximus in presence of paralytic shellfish toxin (PST) from Alexandrium minutum[J]. Harmful Algae, 2022, 115: 102231. doi: 10.1016/j.hal.2022.102231
[18]	Freitas R, Marques F, De Marchi L, et al. Biochemical performance of mussels, cockles and razor shells contaminated by paralytic shellfish toxins[J]. Environmental Research, 2020, 188: 109846. doi: 10.1016/j.envres.2020.109846
[19]	Geret F, Serafim A, Barreira L, et al. Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussatus[J]. Biomarkers, 2002, 7(3): 242−256. doi: 10.1080/13547500210125040
[20]	García-Lagunas N, De Jesus Romero-Geraldo R, Hernández-Saavedra N Y. Changes in gene expression and histological injuries as a result of exposure of Crassostrea gigas to the toxic dinoflagellate Gymnodinium catenatum[J]. Journal of Molluscan Studies, 2016, 82(1): 193−200.
[21]	Balbi T, Auguste M, Ciacci C, et al. Immunological responses of marine bivalves to contaminant exposure: contribution of the-omics approach[J]. Frontiers in Immunology, 2021, 12: 618726. doi: 10.3389/fimmu.2021.618726
[22]	Dong Zhicheng, Chen Yan. Transcriptomics: advances and approaches[J]. Science China Life Sciences, 2013, 56(10): 960−967. doi: 10.1007/s11427-013-4557-2
[23]	Dong Chenfan, Wu Haiyan, Zheng Guanchao, et al. Transcriptome analysis reveals MAPK/AMPK as a key regulator of the inflammatory response in PST detoxification in Mytilus galloprovincialis and Argopecten irradians[J]. Toxins, 2022, 14(8): 516. doi: 10.3390/toxins14080516
[24]	Hu Boyang, Li Moli, Yu Xiaohan, et al. Diverse expression regulation of Hsp70 genes in scallops after exposure to toxic Alexandrium dinoflagellates[J]. Chemosphere, 2019, 234: 62−69. doi: 10.1016/j.chemosphere.2019.06.034
[25]	García-Lagunas N, Romero-Geraldo R, Hernández-Saavedra N Y. Genomics study of the exposure effect of Gymnodinium catenatum, a paralyzing toxin producer, on Crassostrea gigas’ defense system and detoxification genes[J]. PLoS One, 2013, 8(9): e72323. doi: 10.1371/journal.pone.0072323
[26]	Cappello T, Giannetto A, Parrino V, et al. Baseline levels of metabolites in different tissues of mussel Mytilus galloprovincialis (Bivalvia: Mytilidae)[J]. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 2018, 26: 32−39. doi: 10.1016/j.cbd.2018.03.005
[27]	Blanco J, Mariño C, Martín H, et al. Anatomical distribution of diarrhetic shellfish poisoning (DSP) toxins in the mussel Mytilus galloprovincialis[J]. Toxicon, 2007, 50(8): 1011−1018. doi: 10.1016/j.toxicon.2007.09.002
[28]	Qi Hongqing, Liu Ying, Jian Fanjie, et al. Effects of dietary arachidonic acid (ARA) on immunity, growth and fatty acids of Apostichopus japonicus[J]. Fish & Shellfish Immunology, 2022, 127: 901−909.
[29]	Carrier III J K, Watanabe W O, Harel M, et al. Effects of dietary arachidonic acid on larval performance, fatty acid profiles, stress resistance, and expression of Na⁺/K⁺ ATPase mRNA in black sea bass Centropristis striata[J]. Aquaculture, 2011, 319(1/2): 111−121.
[30]	Gerdol M, Moreira R, Cruz F, et al. Massive gene presence-absence variation shapes an open pan-genome in the Mediterranean mussel[J]. Genome Biology, 2020, 21(1): 275. doi: 10.1186/s13059-020-02180-3
[31]	Murgarella M, Puiu D, Novoa B, et al. A first insight into the genome of the filter-feeder mussel Mytilus galloprovincialis[J]. PLoS One, 2016, 11(3): e151561.
[32]	Yu Rencheng, Zhang Qingchun, Liu Yang, et al. The dinoflagellate Alexandrium catenella producing only carbamate toxins may account for the seafood poisonings in Qinhuangdao, China[J]. Harmful Algae, 2021, 103: 101980. doi: 10.1016/j.hal.2021.101980
[33]	Zhou Zhiwei, Luo Mingdu, Chen Xi, et al. Ion mobility collision cross-section atlas for known and unknown metabolite annotation in untargeted metabolomics[J]. Nature Communications, 2020, 11(1): 4334. doi: 10.1038/s41467-020-18171-8
[34]	Bouallegui Y. Immunity in mussels: an overview of molecular components and mechanisms with a focus on the functional defenses[J]. Fish & Shellfish Immunology, 2019, 89: 158−169.
[35]	Ciacci C, Betti M, Canonico B, et al. Specificity of anti- Vibrio immune response through p38 MAPK and PKC activation in the hemocytes of the mussel Mytilus galloprovincialis[J]. Journal of Invertebrate Pathology, 2010, 105(1): 49−55. doi: 10.1016/j.jip.2010.05.010
[36]	Wu Haiyan, Dong Chenfan, Zheng Guanchao, et al. Formation mechanism and environmental drivers of Alexandrium catenella bloom events in the coastal waters of Qinhuangdao, China[J]. Environmental Pollution, 2022, 313: 120241. doi: 10.1016/j.envpol.2022.120241
[37]	Castrec J, Soudant P, Payton L, et al. Bioactive extracellular compounds produced by the dinoflagellate Alexandrium minutum are highly detrimental for oysters[J]. Aquatic Toxicology, 2018, 199: 188−198. doi: 10.1016/j.aquatox.2018.03.034
[38]	Tan K, Sun Yizhou, Zhang Hongkuan, et al. Effects of harmful algal blooms on the physiological, immunity and resistance to environmental stress of bivalves: special focus on paralytic shellfish poisoning and diarrhetic shellfish poisoning[J]. Aquaculture, 2023, 563: 739000. doi: 10.1016/j.aquaculture.2022.739000
[39]	Hanna V S, Hafez E A A. Synopsis of arachidonic acid metabolism: a review[J]. Journal of Advanced Research, 2018, 11: 23−32. doi: 10.1016/j.jare.2018.03.005
[40]	El Kertaoui N, Lund I, Betancor M B, et al. Dietary DHA and ARA level and ratio affect the occurrence of skeletal anomalies in pikeperch larvae ( Sander lucioperca) through a regulation of immunity and stress related gene expression[J]. Aquaculture, 2021, 544: 737060. doi: 10.1016/j.aquaculture.2021.737060
[41]	Gagné F, Auclair J, Peyrot C, et al. The influence of zinc chloride and zinc oxide nanoparticles on air-time survival in freshwater mussels[J]. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 2015, 172−173: 36−44.
[42]	Powell W S, Rokach J. Biosynthesis, biological effects, and receptors of hydroxyeicosatetraenoic acids (HETEs) and oxoeicosatetraenoic acids (oxo-ETEs) derived from arachidonic acid[J]. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 2015, 1851(4): 340−355.
[43]	Lin Yan, Lu Xinchen, Qiu Xinghua, et al. Arachidonic acid metabolism and inflammatory biomarkers associated with exposure to polycyclic aromatic hydrocarbons[J]. Environmental Research, 2022, 212: 113498. doi: 10.1016/j.envres.2022.113498
[44]	Calder P C. Eicosanoids[J]. Essays in Biochemistry, 2020, 64(3): 423−441. doi: 10.1042/EBC20190083
[45]	Liu Yingjie, Chen Zhongxiang, Li Shanwei, et al. Multi-omics profiling and biochemical assays reveal the acute toxicity of environmental related concentrations of Di-(2-ethylhexyl) phthalate (DEHP) on the gill of crucian carp ( Carassius auratus)[J]. Chemosphere, 2022, 307: 135814. doi: 10.1016/j.chemosphere.2022.135814
[46]	Škugor S, Škugor A, Todorčević M, et al. Exposure to lipopolysaccharide induces immune genes in cultured preadipocytes of Atlantic salmon[J]. Fish & Shellfish Immunology, 2010, 29(5): 817−824.
[47]	Samuelsson B. Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation[J]. Science, 1983, 220(4597): 568−575. doi: 10.1126/science.6301011
[48]	Boltaña S, Tridico R, Teles M, et al. Lipopolysaccharides isolated from Aeromonas salmonicida and Vibrio anguillarum show quantitative but not qualitative differences in inflammatory outcome in Sparus aurata (Gilthead seabream)[J]. Fish & Shellfish Immunology, 2014, 39(2): 475−482.
[49]	Tallima H. Clarification of arachidonic acid metabolic pathway intricacies[J]. ACS Omega, 2021, 6(24): 15559−15563. doi: 10.1021/acsomega.1c01952
[50]	Guengerich F P. Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity[J]. Chemical Research in Toxicology, 2001, 14(6): 611−650. doi: 10.1021/tx0002583
[51]	Han J, Park J S, Park Y, et al. Effects of paralytic shellfish poisoning toxin-producing dinoflagellate Gymnodinium catenatum on the marine copepod Tigriopus japonicus[J]. Marine Pollution Bulletin, 2021, 163: 111937. doi: 10.1016/j.marpolbul.2020.111937
[52]	Wei Xiaomeng, Lu Miyu, Duan Guofang, et al. Responses of CYP450 in the mussel Perna viridis after short-term exposure to the DSP toxins-producing dinoflagellate Prorocentrum lima[J]. Ecotoxicology and Environmental Safety, 2019, 176: 178−185. doi: 10.1016/j.ecoenv.2019.03.073
[53]	Maha I F, Xie Xiao, Zhou Suming, et al. Skin metabolome reveals immune responses in yellow drum Nibea albiflora to Cryptocaryon irritans infection[J]. Fish Shellfish Immunology, 2019, 94: 661−674. doi: 10.1016/j.bcp.2018.10.007
[54]	Painefilú J C, Bianchi V A, Krock B, et al. Effects of paralytic shellfish toxins on the middle intestine of Oncorhynchus mykiss: glutathione metabolism, oxidative status, lysosomal function and ATP-binding cassette class C (ABCC) proteins activity[J]. Ecotoxicology and Environmental Safety, 2020, 204: 111069. doi: 10.1016/j.ecoenv.2020.111069
[55]	Li Cong, Deng Xiaobing, Xie Xiaowen, et al. Activation of glutathione peroxidase 4 as a novel anti-inflammatory strategy[J]. Frontiers in Pharmacology, 2018, 9: 1120. doi: 10.3389/fphar.2018.01120