Abstract
The activity and expression level of cytoplasmic malate dehydrogenase (MDH 1.1.1.37) gene and adenylate system state in tissues of the Mediterranean mussel Mytilus galloprovincialis Lamarck, 1819 were investigated. The highest values of adenylate energy charge (AEC) (0.66 ± 0.01) and adenylate content (ATP, ADP, and AMP) were observed in the mollusc’s foot. Close AEC values were found in the gills (0.61 ± 0.02). The lowest values were recorded in the hepatopancreas and mantle edge (AEC of 0.46–0.54) indicating moderate depression of physiological processes. A direct relationship between adenylate system state in muscle tissue and MDH activity (R2 above 0.7) was revealed, and thus this parameter can be recommended as a biomarker for energy status assessment in the mollusc’s tissue structures. A direct relationship between gene expression levels and MDH activity was shown for tissues of mussels in the range hepatopancreas → gills → foot. In contrast, in the mantle high levels of gene expression corresponded to a relatively low activity of the enzyme, presumably due to non-homogeneous tissue structure.
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References
Atkinson DE (1968) The energy charge of the adenylate pools as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7(11):4030–4034. https://doi.org/10.1021/bi00851a033
Benali I, Boutiba Z, Merabet A, Chèvre N (2015) Integrated use of biomarkers and condition indices in mussels (Mytilus galloprovincialis) for monitoring pollution and development of biomarker index to assess the potential toxic of coastal sites. Mar Pollut Bull 95:385–394. https://doi.org/10.1016/j.marpolbul.2015.03.041
Beyer J, Green NW, Brooks S, Allan IJ, Ruus A, Gomes T, Bråte ILN, Schøyen M (2017) Blue mussels (Mytilus edulis spp.) as sentinel organisms in coastal pollution monitoring: a review. Mar Environ Res 130:338–365. https://doi.org/10.1016/j.marenvres.2017.07.024
Bowen KL, Johannsson OE, Smith R, Schlechtriem C (2005) RNA/DNA and protein indices in evaluating growth and condition of aguatic organisms: a review. Ann Conf Great Lakes Res 48:34–39
Chang GG, Tong L (2003) Structure and function of malic enzymes, a new class of oxidative decarboxylases. Biochemistry 42(44):12721–12733. https://doi.org/10.1021/bi035251+
Cossu C, Doyotte A, Babut M, Exinger A, Vasseur P (2000) Antioxidant biomarkers in Freshwater Bivalves, Unio tumidus, in response to different contamination profiles of aquatic sediments. Ecotoxicol Environ Saf 45:106–121. https://doi.org/10.1006/eesa.1999.1842
Coyne KJ, Waite JH (2000) In search of molecular dovetails in mussel byssus: from the threads to the stem. J Experimental Bioology 203(9):1425–1431. https://doi.org/10.1242/jeb.203.9.1425
Cui L, Liu C, Lu Y (1996) Studies on mussel’s gills. Shandong Fish - Qilu Yuye 13(5):11–14
De GuglielmoV, Puoti R, Notariale R, Maresca V, Ausió J, Troisi J, Verrillo M, Basile A, Febbraio F, Piscopo M (2019) Alterations in the properties of sperm protamine-like II protein after exposure of Mytilus galloprovincialis (Lamarck 1819) to sub-toxic doses of cadmium. Ecotoxicol Environ Saf 169:600–606. https://doi.org/10.1016/j.ecoenv.2018.11.069
Farrington JW, Tripp BW, Tanabe S, Subramanian A, Sericano JL, Wade TL, Knap AH, Edward D (2016) Goldberg’s proposal of “the mussel watch”: reflections after 40 years. Mar Pollut Bull 110:501–510. https://doi.org/10.1016/j.marpolbul.2016.05.074
Fuentes A, Fernández-Segovia I, Escriche I, Serra JA (2009) Comparison of physico-chemical parameters and composition of mussels (Mytilus galloprovincialis Lmk.) From different spanish origins. Food Chem 112(2):295–302. https://doi.org/10.1016/J.FOODCHEM.2008.05.064
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. Mar Biotechnol 17(6):768–781. https://doi.org/10.1007/s10126-015-9655-7
Holm-Hansen O, Booth CR (1966) The measurement of adenosine triphosphate in the Ocean and its ecological significance. Limnol Oceanogr 11(4):510–519. https://doi.org/10.4319/lo.1966.11.4.0510
Kholodov VI, Pirkova AV, Ladygina LV (2017) Cultivation of mussels and oysters in the Black Sea. ООО “IZDATPRINT”, Voronezh
Kolesnikova EE, Golovina IV (2020) Oxidoreductase activities in oxyphilic tissues of the Black Sea Ruff Scorpaena porcus under short-term hydrogen sulfide loading. J Evol Biochem Physiol 56(5):459–470. https://doi.org/10.1134/S0022093020050099
Kulikova AD, Soldatov AA, Andreenko TI (2015) Tissue transaminase activities in the black-sea mollusc Mytilus galloprovincialis Lam. With different shell color. J Evol Biochem Physiol 51(1):23–31. https://doi.org/10.1134/S0022093015010044
Le Gendre R, Morin J, Maheux F, Fournier F, Simon B, Cochard M-L, Pierre-Duplessix O, Dumas F, Harmel B, Paul C, Riou P (2014) DILEMES Dispersion Larvaire de Mytilus Edulis en baie de Seine. 2014 Repport final: France. https://archimer.ifremer.fr/doc/00188/29916/28376.pdf
Lettieri G, Notariale R, Ambrosino A, Di Bonito A, Giarra A, Trifuoggi M, Manna C, Piscopo M (2021) Spermatozoa Transcriptional response and alterations in PL proteins Properties after exposure of Mytilus galloprovincialis to Mercury. Int J Mol Sci 22:1618. https://doi.org/10.3390/ijms22041618
Lettieri G, Carusone N, Notariale R, Prisco M, Ambrosino A, Perrella S, Manna C, Piscopo M (2022) Morphological, gene, and hormonal changes in gonads and In-Creased Micrococcal nuclease accessibility of sperm chromatin Induced by Mercury. Biomolecules 12(1):87. https://doi.org/10.3390/biom12010087
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 – ∆∆CT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Livingstone DR (1991) Origins and evolution of pathways of anaerobic metabolism in the animal kingdom. Am Zool 31:522–534
Lucas JM, Vaccaro E, Waite JH (2002) A molecular, morphometric and mechanical comparison of the structural elements of byssus from Mytilus edulis and Mytilus galloprovincialis. J Experimental Bioology 205(12):1807–1817. https://doi.org/10.1242/jeb.205.12.1807
Maoka T, Etoh T, Borodina AV, Soldatov AA (2011) A series of 19′-hexanoyloxyfucoxanthin derivatives from the sea mussel, Mytilus galloprovincialis, grown in the black sea. Ukraine J Agricultural Food Chem 59(24):13059–13064. https://doi.org/10.1021/jf2035115
Martínez-Gomez C, Robinson CD, Burgeot T, Gubbins M, Halldorsson HP, Albentosa M, Bignell JP, Hylland K, Vethaak D (2017) Biomarkers of general stress in mussels as common indicators for marine biomonitoring programmes in Europe: the ICON experience. Mar Environ Res 124:70–80. https://doi.org/10.1016/j.marenvres.2015.10.012
Niyogi S, Biswas S, Sarker S, Datta AG (2001) Antioxidant enzymes in brackish water oyster, Saccostrea cucullata as potential biomarkers of polyaromatic hydrocarbon pollution in Hooghly Estuery (India): seasonality and its consequences. Sci Total Environ 281:237–246. https://doi.org/10.1016/s0048-9697(01)00850-6
Owen TG, Hochachka PW (1974) Purification and properties of dolphin muscle aspartate and alanine transaminases and their possible roles in the energy metabolism of diving mammals. Biochem J 143:541–553. https://doi.org/10.1042/bj1430541
Piscopo M, Notariale R, Rabbito D, Ausió J, Olanrewaju OS, Guerriero G (2018) Mytilus galloprovincialis (Lamarck, 1819) spermatozoa: hsp70 expression and protamine-like protein property studies. Environ Sci Pollut Res Int 25(13):12957–12966. https://doi.org/10.1007/s11356-018-1570-9
Ribera D, Narbonne JF, Michel X, Livingstone DR, O’Hara S (1991) Responses of antioxidants and lipid peroxidation in mussels to oxidative damage exposure. Comp Biochem Physiol 100 C:177–181. https://doi.org/10.1016/0742-8413(91)90149-n
Romeo M, Gnassia-Barelli M (1997) Effect of heavy metal on lipid peroxidation in the Mediterranean clam, Ruditapes decussates. Comp Biochem Physiolology 118 C:33–37. https://doi.org/10.1016/S0742-8413(97)00079-0
Rooker JR, Holt GJ (1999) Application of RNA/DNA ratios to evaluate the condition and growth of larval and juvenile red drum (Sciachops ocellatus). Mar Freshw Res 47:12–18. https://doi.org/10.1071/MF9960283
Ruppert EE, Fox RS, Barnes RD (2008) Zoology of invertebrates. Lower coelomic animals, 2 edn. Academy, Moscow, pp 28–99. (in Russian)
Skorkowski EF (1988) Mitochondrial malic enzyme from crustacean and fish muscle. Comp Biochem Physiolology 90B:19–24. https://doi.org/10.1016/0305-0491(88)90031-4
Soldatov AA, Andreenko TI, Golovina IV, Stolbov AY (2010a) Peculiarities of organization of tissue metabolism in mollusc’s with different tolerance to external hypoxia. J Evol Biochem Physiol 46(4):341–349. https://doi.org/10.1134/S0022093010040022
Soldatov AA, Sysoyeva IV, Sysoyev AA, Andreyenko TI (2010b) Adenylate system of tissues of the bivalve mollusk under experimental anoxia. Hydrobiol J 46(5):60–67. https://doi.org/10.1615/HydrobJ.v46.i5.70
Soldatov AA, Gostyukhina OL, Golovina IV (2014) Functional states of antioxidant enzymatic complex of tissues of Mytillus galloprovincialis Lam. Under conditions of oxidative stress. J Evol Biochem Physiol 50(3):206–214. https://doi.org/10.1134/S0022093014030028
Sunila I (1988) Pollution-related histopathological changes in the mussel Mytilus edulis L. in the Baltic Sea. Mar Environ Res 24(1–4):277–280. https://doi.org/10.1016/0141-1136(88)90320-0
Westheide W, Rieger R (2008) Zoology of Invertebrates. Volume 1: from the simplest to molluscs and arthropods. Association of scientific publications KMK, Moscow
Yin Y, Kirsch JF (2007) Identification of functional paralog shift mutations: Conversion of Escherichia coli malate dehydrogenase to a lactate dehydrogenase. PNAS 104(44):17353–17357. https://doi.org/10.1073/pnas.0708265104
Zaika VE, Valovaya NA, Povchun AS (1990) Mytilides of the Black Sea. Naukova dumka, Kiev. (in Russian)
Zuykov M, Pelletier E, Harper DAT (2013) Bivalve mollusks in metal pollution studies: from bioaccumulation to biomonitoring. Chemosphere 93:201–208. https://doi.org/10.1016/j.chemosphere.2013.05.001
Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekee** genes, differentially regulated target genes and sample integrity: BestKeeper – Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515
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State assignment No 121041400077-1; Russian Foundation for Basic Research (grant No 20-04-00037 A); Strategic project No 3, No 121121700318-1.
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Aleksander A. Soldatov: Conceptualization, Supervision, Writing – review & editing, Funding acquisition, Project administration, Formal analysis, Data curation. Irina V. Golovina: Determination of MDР activity. Anastasia O. Lantushenko and Alyona S. Kokhan: Determination of MDG gene expression level. Inna V. Sysoeva and Aleksander A. Sysoev: Assessment of the state of the adenylate system. Evgenia E. Kolesnikova: Translation, Review & editing.
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All procedures using mussels were accomplished in accordance with the European Communities Council Directive (2010/63/EU) and approved by the local Institutional Animal Care and Use Committee (protocol #28 from 15.02. 2018).
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Soldatov, A.A., Golovina, I.V., Lantushenko, A.O. et al. Adenylate System State, Malate Dehydrogenase Activity and Expression Level in Tissues of Mytilus galloprovincialis Lamarck, 1819. Thalassas 39, 739–747 (2023). https://doi.org/10.1007/s41208-023-00563-4
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DOI: https://doi.org/10.1007/s41208-023-00563-4