References
- Almeida EA, Bainy ACD, Dafre AL, Gomes OF, Medeiros MH, Di Mascio P. 2005. Oxidative stress in digestive gland and gill of the brown mussel (Perna perna) exposed to air and re-submersed. Journal of Experimental Marine Biology and Ecology. 318(1):21–30. doi:https://doi.org/10.1016/j.jembe.2004.12.007
- Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD. 2013. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nature Protocols. 8:1765–1786. doi:https://doi.org/10.1038/nprot.2013.099
- Andrews SF, Krueger F, Seconds-Pichon A, Biggins F, Wingett SF. 2014. A quality control tool for high throughput sequence data. Babraham Bioinformatics. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
- Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Ostell J, Pruitt KD, Sayers EW. 2018. Genbank. Nucleic Acids Research. 46(D1):D41–D47. doi:https://doi.org/10.1093/nar/gkx1094
- Bickler PE, Buck LT. 2007. Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annual Review of Physiology. 69:145–170. doi:https://doi.org/10.1146/annurev.physiol.69.031905.162529
- Box A, Capó X, Tejada S, Catanese G, Grau A, Deudero S, Valencia JM. 2020. Reduced antioxidant response of the fan mussel pinna nobilis related to the presence of Haplosporidium pinnae. Pathogens (Basel, Switzerland). 9(11):932. doi:https://doi.org/10.3390/pathogens9110932
- Bushmanova E, Antipov D, Lapidus A, Prjibelski AD. 2019. rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data. GigaScience. 8(9):giz100. doi:https://doi.org/10.1093/gigascience/giz100
- Chainy GBN, Paital B, Dandapat J. 2016. An overview of seasonal changes in oxidative stress and antioxidant defence parameters in some invertebrate and vertebrate species. Scientifica. 2016. https://doi.org/https://doi.org/10.1155/2016/6126570
- Chan F, Barth JA, Kroeker KJ, Lubchenco J, Menge BA. 2019. The dynamics and impact of ocean acidification and hypoxia: Insights from sustained Investigations in the Northern California current large marine ecosystem. Oceanography. 32(3):62–71. doi:https://doi.org/10.5670/oceanog.2019.312
- Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT. 2000. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor- 1a during hypoxia. Journal of Biological Chemistry. 275:25130–25138. doi:https://doi.org/10.1074/jbc.M001914200
- Chatziargyriou V, Dailianis S. 2010. The role of selenium-dependent glutathione peroxidase (Se-GPx) against oxidative and genotoxic effects of mercury in haemocytes of mussel Mytilus galloprovincialis (Lmk). Toxicology in Vitro. 24(5):1363–1372. doi:https://doi.org/10.1016/j.tiv.2010.04.008
- Chen J, Xiao S, Deng Y, Du X, Yu Z. 2011. Cloning of a novel glutathione S-transferase 3 (GST3) gene and expression analysis in pearl oyster, Pinctada martensii. Fish & Shellfish Immunology. https://doi.org/https://doi.org/10.1016/j.fsi.2011.07.023
- Chen S, Zhou Y, Chen Y, Gu J. 2018. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (Oxford, England). 34(17):i884–i890. doi:https://doi.org/10.1093/bioinformatics/bty560
- D’Autréaux B, Toledano MB. 2007. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nature Reviews Molecular Cell Biology. 8(10):813–824. doi:https://doi.org/10.1038/nrm2256
- De Zoysa M, Whang I, Lee Y, Lee S, Lee JS, Lee J. 2009. Transcriptional analysis of antioxidant and immune defense genes in disk abalone (Haliotis discus discus) during thermal, low-salinity and hypoxic stress. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 154(4):387–395. doi:https://doi.org/10.1016/j.cbpb.2009.08.002
- Diaz RJ, Breitburg DL. 2009. The hypoxic environment. Fish Physiology. Academic Press. 27:1–23. doi:https://doi.org/10.1016/S1546-5098(08)00001-0
- Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. https://doi.org/https://doi.org/10.1093/nar/gkh340
- Figueras A, Moreira R, Sendra M, Novoa B. 2019. Genomics and immunity of the Mediterranean mussel Mytilus galloprovincialis in a changing environment. Fish & Shellfish Immunology. 90:440–445. doi:https://doi.org/10.1016/j.fsi.2019.04.064
- Foyer CH, Lopez-Delgado H, Dat JF, Scott IM. 1997. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiologia Plantarum. 100(2):241–254. doi:https://doi.org/10.1111/j.1399-3054.1997.tb04780.x
- Gaetani GF, Galiano S, Canepa L, Ferraris AM, Kirkman HN. 1989. Catalase and glutathione peroxidase are equally active in detoxification of hydrogen peroxide in human erythrocytes. Blood. 73:334–339. doi:https://doi.org/10.1182/blood.V73.1.334.334
- Gerdol M, De Moro G, Manfrin C, Milandri A, Riccardi E, Beran A, Pallavicini A. 2014. RNA sequencing and de novo assembly of the digestive gland transcriptome in Mytilus galloprovincialis fed with toxinogenic and non-toxic strains of Alexandrium minutum. BMC Research Notes. 7(1):722. doi:https://doi.org/10.1186/1756-0500-7-722
- Gerdol M, Gomez-Chiarri M, Castillo MG, Figueras A, Fiorito G, Moreira R, Venier P. 2018. Immunity in molluscs: recognition and effector mechanisms, with a focus on bivalvia. In: Cooper E., editor, Advances in comparative immunology. Cham: Springer; p. 225–341.
- Giannetto A, Maisano M, Cappello T, Oliva S, Parrino V, Natalotto A, Fasulo S. 2015. Hypoxia-inducible factor α and Hif-prolyl hydroxylase characterization and gene expression in short-time air-exposed Mytilus galloprovincialis. Marine Biotechnology. 17(6):768–781. doi:https://doi.org/10.1007/s10126-015-9655-7
- Giannetto A, Maisano M, Cappello T, Oliva S, Parrino V, Natalotto A, Fasulo S. 2017. Effects of oxygen availability on oxidative stress biomarkers in the Mediterranean mussel Mytilus galloprovincialis. Marine Biotechnology. 19(6):614–626. doi:https://doi.org/10.1007/s10126-017-9780-6
- Gu H, Shang Y, Clements J, Dupont S, Wang T, Wei S, Wang Y. 2019. Hypoxia aggravates the effects of ocean acidification on the physiological energetics of the blue mussel Mytilus edulis. Marine Pollution Bulletin. 149:110538. doi:https://doi.org/10.1016/j.marpolbul.2019.110538
- Hu M, Wu F, Yuan M, Li Q, Gu Y, Wang Y, Liu Q. 2015. Antioxidant responses of triangle sail mussel Hyriopsis cumingii exposed to harmful algae Microcystis aeruginosa and hypoxia. Chemosphere. 139:541–549. doi:https://doi.org/10.1016/j.chemosphere.2015.07.074
- Istomina AA, Dovzhenko NV, Bel’cheva NN, Chelomin VP. 2011. Activity of antioxidant enzymes in various species of mollusks in conditions of hypoxia/anoxia. Izv. Samar. Nauchn. Tsentra, Ross. Akad. Nauk. 13(1):5.
- Khan FU, Chen H, Gu H, Wang T, Dupont S, Kong H, Wang Y. 2021. Antioxidant responses of the mussel Mytilus coruscus co-exposed to ocean acidification, hypoxia and warming. Marine Pollution Bulletin. 162:111869. doi:https://doi.org/10.1016/j.marpolbul.2020.111869
- Khan FU, Hu M, Kong H, Shang Y, Wang T, Wang X, Wang Y. 2020. Ocean acidification, hypoxia and warming impair digestive parameters of marine mussels. Chemosphere. 256:127096. doi:https://doi.org/10.1016/j.chemosphere.2020.127096
- Kim BM, Haque MN, Lee DH, Nam SE, Rhee JS. 2018. Comparative toxicokinetics and antioxidant response in the microcystin-LR-exposed gill of two marine bivalves, Crassostrea gigas and Mytilus edulis. Journal of Shellfish Research. 37(3):497–506. doi:https://doi.org/10.2983/035.037.0305
- Klimova YS, Chuiko GM, Pesnya DS, Ivanova ES. 2020. Biomarkers of oxidative stress in Freshwater Bivalve mollusks (review). Inland Water Biology. 13(4):674–683. doi:https://doi.org/10.1134/S1995082920060073
- Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods. 9(4):357–359. doi:https://doi.org/10.1038/nmeth.1923
- Li Z, Cha Y, Hu B, Wen C, Jian S, Yi P, Gang Y. 2018. Identification and characterization of two distinct sigma-class glutathione-S-transferase from freshwater bivalve cristaria plicata. Comp. Biochem. Physiol. Part – B Biochem. Mol. Biol. https://doi.org/https://doi.org/10.1016/j.cbpb.2018.03.004.
- Liddell JR, Hoepken HH, Crack PJ, Robinson SR, Dringen R. 2006. Glutathione peroxidase 1 and glutathione are required to protect mouse astrocytes from iron-mediated hydrogen peroxide toxicity. Journal of Neuroscience Research. 84(3):578–586. doi:https://doi.org/10.1002/jnr.20957
- Lu X, Wang C, Liu B. 2015. The role of Cu/Zn-SOD and Mn-SOD in the immune response to oxidative stress and pathogen challenge in the clam Meretrix meretrix. Fish & Shellfish Immunology. 42(1):58–65. doi:https://doi.org/10.1016/j.fsi.2014.10.027
- Manduzio H, Monsinjon T, Galap C, Leboulenger F, Rocher B. 2004. Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquatic Toxicology. 70(1):83–93. doi:https://doi.org/10.1016/j.aquatox.2004.07.003
- Manduzio H, Rocher B, Durand F, Galap C, Leboulenger F. 2005. The point about oxidative stress in molluscs. Invertebrate Survival Journal. 2(2):91–104.
- Martins JC, Campos A, Osório H, da Fonseca R, Vasconcelos V. 2014. Proteomic profiling of cytosolic glutathione transferases from three bivalve species: Corbicula fluminea, Mytilus galloprovincialis and Anodonta cygnea. Int J Mol Sci. https://doi.org/https://doi.org/10.3390/ijms15021887.
- Mazat JP, Devin A, Ransac S. 2020. Modelling mitochondrial ROS production by the respiratory chain. Cellular and Molecular Life Sciences. 77(3):455–465. doi:https://doi.org/10.1007/s00018-019-03381-1
- Mohamed B, Hajer A, Susanna S, Caterina O, Flavio M, Hamadi B, Aldo V. 2014. Transcriptomic responses to heat stress and nickel in the mussel Mytilus galloprovincialis. Aquatic Toxicology. 148:104–112. doi:https://doi.org/10.1016/j.aquatox.2014.01.004
- Murphy MP. 2009. How mitochondria produce reactive oxygen species. Biochemical Journal. 417(1):1–13. doi:https://doi.org/10.1042/BJ20081386
- Nakhleh L, Jin G, Zhao F, Mellor-Crummey J. 2005. Reconstructing phylogenetic networks using maximum parsimony. In: Proceedings – 2005 IEEE Computational Systems Bioinformatics Conference, CSB 2005. https://doi.org/https://doi.org/10.1109/CSB.2005.47
- Nogueira L, Mello DF, Trevisan R, Garcia D, da Silva Acosta D, Dafre AL, de Almeida EA. 2017. Hypoxia effects on oxidative stress and immunocompetence biomarkers in the mussel Perna perna (Mytilidae, Bivalvia). Marine Environmental Research. 126:109–115. doi:https://doi.org/10.1016/j.marenvres.2017.02.009
- Nunez R. 2001. DNA measurement and cell cycle analysis by flow cytometry. Cur Iss Mol Biol. 3:67–70. https://doi.org/https://doi.org/10.21775/cimb.003.067.
- Ohlemiller KK, McFadden SL, Ding DL, Flood DG, Reaume AG, Hoffman EK, Salvi RJ. 1999. Targeted deletion of the cytosolic Cu/Zn-superoxide dismutase gene (Sod1) increases susceptibility to noise-induced hearing loss. Audiology and Neuro-Otology. 4(5):237–246. doi:https://doi.org/10.1159/000013847
- Osipov AN, Azizova OA, Vladimirov YUA. 1990. Reactive oxygen species and their role in organization. Advances in Biological Chemistry. 31(2):180–208. (In Russian).
- Pannunzio TM, Storey KB. 1998. Antioxidant defenses and lipidperoxidation during anoxia stress and aerobic recovery in the marine gastropod Littorina littorae. Journal of Experimental Marine Biology and Ecology. 221:277–292. doi:https://doi.org/10.1016/S0022-0981(97)00132-9
- Philipp EE, Wessels W, Gruber H, Strahl J, Wagner AE, Ernst IM, Rosenstiel P. 2012. Gene expression and physiological changes of different populations of the long-lived bivalve Arctica islandica under low oxygen conditions. PLoS One. 7(9):e44621. doi:https://doi.org/10.1371/journal.pone.0044621
- Prego-Faraldo MV, Martínez L, Méndez J. 2018. RNA-Seq analysis for assessing the early response to DSP toxins in Mytilus galloprovincialis digestive gland and gill. Toxins. 10(10):417. doi:https://doi.org/10.3390/toxins10100417
- Rajkumar AP, Qvist P, Lazarus R, Lescai F, Ju J, Nyegaard M, Christensen JH. 2015. Experimental validation of methods for differential gene expression analysis and sample pooling in RNA-seq. BMC Genomics. 16(1):548. doi:https://doi.org/10.1186/s12864-015-1767-y
- Revathy KS, Umasuthan N, Lee Y, Choi CY, Whang I, Lee J. 2012. First molluscan theta-class glutathione S-transferase: identification, cloning, characterization and transcriptional analysis post immune challenges. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 162(1–3):10–23. doi:https://doi.org/10.1016/j.cbpb.2012.02.004
- Sabatini SE, Rocchetta I, Luquet CM, Guido MI, De Molina MDCR. 2011. Effects of sewage pollution and bacterial load on growth and oxidative balance in the freshwater mussel Diplodon chilensis. Limnologica. 41(4):356–362. doi:https://doi.org/10.1016/j.limno.2011.04.004
- Santovito G, Trentin E, Gobbi I, Bisaccia P, Tallandini L, Irato P. 2021. Non-enzymatic antioxidant responses of Mytilus galloprovincialis: Insights into the physiological role against metal-induced oxidative stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 240:108909. doi:https://doi.org/10.1016/j.cbpc.2020.108909
- Seppey M, Manni M, Zdobnov EM. 2019. BUSCO: assessing genome assembly and annotation completeness. In: Kollmar M, editor. Gene prediction. Methods in molecular biology, vol 1962. New York, NY: Humana; https://doi.org/https://doi.org/10.1007/978-1-4939-9173-0_14.
- Shang Y, Wang X, Deng Y, Wang S, Gu H, Wang T, Wang Y. 2020. Diel-cycling seawater acidification and hypoxia impair the physiological and growth performance of marine mussels. Science of The Total Environment. 722:138001. doi:https://doi.org/10.1016/j.scitotenv.2020.138001
- Sies H. 1993. Strategies of antioxidant defense. European Journal of Biochemistry. 215(2):213–219. doi:https://doi.org/10.1111/j.1432-1033.1993.tb18025.x
- Sokolov EP, Markert S, Hinzke T, Hirschfeld C, Becher D, Ponsuksili S, Sokolova IM. 2019. Effects of hypoxia-reoxygenation stress on mitochondrial proteome and bioenergetics of the hypoxia-tolerant marine bivalve Crassostrea gigas. Journal of Proteomics. 194:99–111. doi:https://doi.org/10.1016/j.jprot.2018.12.009
- Spijkers J, Morrison TH, Blasiak R, Cumming GS, Osborne M, Watson J, Österblom H. 2018. Marine fisheries and future ocean conflict. Fish and Fisheries. 19(5):798–806. doi:https://doi.org/10.1111/faf.12291
- Stecher G, Tamura K, Kumar S. 2020. Molecular evolutionary genetics analysis (MEGA) for macOS. Mol. Biol. Evol. https://doi.org/https://doi.org/10.1093/molbev/msz312
- Storey KB, Lant B, Anozie OO, Storey JM. 2013. Metabolic mechanisms for anoxia tolerance and freezing survival in the intertidal gastropod, Littorina littorea. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 165(4):448–459. doi:https://doi.org/10.1016/j.cbpa.2013.03.009
- Sui Y, Hu M, Shang Y, Wu F, Huang X, Dupont S, Wang Y. 2017. Antioxidant response of the hard shelled mussel Mytilus coruscus exposed to reduced pH and oxygen concentration. Ecotoxicology and Environmental Safety. 137:94–102. doi:https://doi.org/10.1016/j.ecoenv.2016.11.023
- Sui Y, Kong H, Huang X, Dupont S, Hu M, Storch D, Wang Y. 2016a. Combined effects of short-term exposure to elevated CO2 and decreased O2 on the physiology and energy budget of the thick shell mussel Mytilus coruscus. Chemosphere. 155:207–216. doi:https://doi.org/10.1016/j.chemosphere.2016.04.054
- Sui Y, Kong H, Shang Y, Huang X, Wu F, Hu M, Wang Y. 2016b. Effects of short-term hypoxia and seawater acidification on hemocyte responses of the mussel Mytilus coruscus. Marine Pollution Bulletin. 108(1–2):46–52. doi:https://doi.org/10.1016/j.marpolbul.2016.05.001
- Sussarellu R, Dudognon T, Fabioux C, Soudant P, Moraga D, Kraffe E. 2013. Rapid mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oyster. Crassostrea gigas. J. Exp. Biol. 216(9):1561–1569. https://doi.org/http://doi.org/10.1242/jeb.075879.
- Thomas Y, Flye-Sainte-Marie J, Chabot D, Aguirre-Velarde A, Marques GM, Pecquerie L. 2019. Effects of hypoxia on metabolic functions in marine organisms: observed patterns and modelling assumptions within the context of Dynamic energy budget (DEB) theory. Journal of Sea Research. 143:231–242. doi:https://doi.org/10.1016/j.seares.2018.05.001
- Trevisan R, Mello DF, Delapedra G, Silva DG, Arl M, Danielli NM, Dafre AL. 2016. Gills as a glutathione-dependent metabolic barrier in Pacific oysters Crassostrea gigas: absorption, metabolism and excretion of a model electrophile. Aquatic Toxicology. 173:105–119. doi:https://doi.org/10.1016/j.aquatox.2016.01.008
- Umasuthan N, Bathige SDNK, Revathy KS, Lee Y, Whang I, Choi CY, Hae-Chul Park H-C, Lee J. 2012. A manganese superoxide dismutase (MnSOD) from Ruditapes philippinarum: comparative structural- and expressional-analysis with copper/zinc superoxide dismutase (Cu/ZnSOD) and biochemical analysis of its antioxidant activities. Fish & Shellfish Immunology. 33(4):753–765. doi:https://doi.org/10.1016/j.fsi.2012.06.024
- UniProt Consortium. 2019. Uniprot: a worldwide hub of protein knowledge. Nucleic Acids Research. 47(D1):D506–D515. doi:https://doi.org/10.1093/nar/gky1049
- Valdez LB, Arnaiz SL, Bustamante J, Alvarez S, Costa LE, Boveris A. 2000. Free radical chemistry in biological systems. Biological Research. 33(2):65–70. doi:https://doi.org/10.4067/S0716-97602000000200005
- wWelker AF, Campos ÉG, Cardoso LA, Hermes-Lima M. 2012. Role of catalase on the hypoxia/reoxygenation stress in the hypoxia-tolerant Nile tilapia. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 302(9):R1111–R1118. doi:https://doi.org/10.1152/ajpregu.00243.2011
- Welker AF, Moreira DC, Campos ÉG, Hermes-Lima M. 2013. Role of redox metabolism for adaptation of aquatic animals to drastic changes in oxygen availability. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 165(4):384–404. doi:https://doi.org/10.1016/j.cbpa.2013.04.003
- Whalen KE, Morin D, Lin CY, Tjeerdema RS, Goldstone JV, Hahn ME. 2008. Proteomic identification, cDNA cloning and enzymatic activity of glutathione S-transferases from the generalist marine gastropod, cyphoma gibbosum. Arch Biochem Biophys. https://doi.org/https://doi.org/10.1016/j.abb.2008.07.007.
- Wilhelm-Filho D, Gonzalez-Flecha B, Boveris A. 1994. Gill diffusion as a physiological mechanism for hydrogen peroxide elimination by fish. Brazilian Journal of Medical and Biological Research. 27(12):2879–2882.
- Woo S, Denis V, Won H, Shin K, Lee G, Lee TK, Yum S. 2013. Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia. Zoological Studies. 52(1):15. doi:https://doi.org/10.1186/1810-522X-52-15
- Woo S, Jeon HY, Kim SR, Yum S. 2011. Differentially displayed genes with oxygen depletion stress and transcriptional responses in the marine mussel, Mytilus galloprovincialis. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics. 6(4):348–356. doi:https://doi.org/10.1016/j.cbd.2011.07.003
- Yusseppone MS, Rocchetta L, Sabatini SE, Luquet CM. 2018. Inducing the alternative oxidase forms part of the molecular strategy of anoxic survival in freshwater bivalves. Frontiers in Physiology. 9:1–12. https://doi.org/https://doi.org/10.3389/fphys.2018.00100.