Biology BulletinBiology BulletinИзвестия Российской академии наук. Серия биологическая1026-34703034-5367The Russian Academy of Sciences64781810.31857/S1026347024040113VHCVFAКРАТКИЕ СООБЩЕНИЯКРАТКИЕ СООБЩЕНИЯResearch ArticleExpression of pyruvate kinase, malate and octopine dehydrogenase genes in the gills of the Mediterranean mussel Mytilus galloprovincialis (Lamarck, 1819) under conditions of hypoxia and reoxygenationЭкспрессия генов пируваткиназы, малат- и октопиндегидрогеназы в жабрах средиземноморской мидии Mytilus galloprovincialis (Lamarck, 1819) в условиях гипоксии и реоксигенацииLantushenkoA. O.ЛантушенкоА. О.
Russian Federation
alekssoldatov@yandex.ruKohanA. S.КоханА. С.
Russian Federation
alekssoldatov@yandex.ruSoldatovA. A.СолдатовА. А.
Russian Federation
alekssoldatov@yandex.ruDegtyarI. V.ДегтярИ. В.
Russian Federation
alekssoldatov@yandex.ruAndreevaA. Yu.АндрееваА. Ю.
Russian Federation
alekssoldatov@yandex.ruSevastopol State UniversityСевастопольский государственный университетFederal Research Center “A.O. Kovalevsky Institute of Biology of the South Seas of the Russian Academy of Sciences”Федеральный исследовательский центр «Институт биологии южных морей им. А.О. Ковалевского РАН»26102024454154628012025Copyright ©; 2024, Russian Academy of SciencesCopyright ©; 2024, Российская академия наук2024Russian Academy of SciencesРоссийская академия наукhttps://medjrf.com/1026-3470/article/view/647818

The effect of hypoxia on the expression level of pyruvate kinase (PKM), octopine dehydrogenase (OcDH) and malate dehydrogenase (MDH) genes in the gill tissue of the Mediterranean mussel Mytilus galloprovincialis (L., 1819) was studied experimentally. The control group of mollusks was kept at 9–10°C and the oxygen level in the water was 8.5 mgO2 l–1. Experimental – at 9–10°C and 2.2 mgO2 l–1. The exposure was 24 and 72 hours. Some of the individuals were subsequently subjected to the reoxygenation procedure. Under conditions of hypoxia, the expression level of OcDH and MDH genes increased by 3 and 2 times, respectively (p < 0.05). At the same time, OcDH expression showed sensitivity to the oxygen content in the medium. Under the conditions of reoxygenation, the process was completely suppressed. The expression of the PKM gene, on the contrary, did not depend on hypoxic effects and remained at the level of control values.

Исследовали в условиях эксперимента влияние гипоксии на уровень экспрессии генов пируваткиназы (РКМ), октопиндегидрогеназы (OcDH) и малатдегидрогеназы (MDH) в жаберной ткани средиземноморской мидии Mytilus galloprovincialis (L., 1819). Контрольная группа моллюсков содержалась при 9–10оС и уровне кислорода в воде 8.5 мгО2 л–1. Опытная – при 9–10оС и 2.2 мгО2 л–1. Экспозиция – 24 и 72 ч. Часть особей в дальнейшем подвергалась процедуре реоксигенации. В условиях гипоксии происходило повышение уровня экспрессии генов OcDH и MDH соответственно в 3 и 2 раза (p < 0.05). При этом экспрессия OcDH проявляла чувствительность к содержанию кислорода в среде. В условиях реоксигенации процесс полностью подавлялся. Экспрессия гена РКМ, напротив, не зависела от гипоксического воздействия и сохранялась на уровне контрольных значений.

Mytilus galloprovincialishypoxiagene expressiongillsmalate dehydrogenaseoctopine dehydrogenasepyruvate kinaseMytilus galloprovincialisгипоксияэкспрессия геновжабрымалатдегидрогеназаоктопиндегидрогеназапируваткиназаПравительство РФGovernment of the Russian FederationАААА-А18-118021490093-4Allcock A. L., Strugnell J. M., Prodohl P., Piatkowski U., Vecchione M. A new species of Parledoene (Cephalopoda: Octopodidae) from Antarctic Peninsula Waters // Polar Biology. 2007. V. 30. P. 883–893.Andreyeva, A. Y., Gostyukhina, O. L., Kladchenko, E. S., Afonnikov, D. A., Rasskazov, D. A., Lantushenko, A. O., & Vodiasova, E. A. Hypoxia exerts oxidative stress and changes in expression of antioxidant enzyme genes in gills of Mytilus galloprovincialis (Lamarck, 1819) // Marine Biology Research. 2021. V. 17. Iss. 4. P. 369-379.Bacchiocchi S., Principato G. Mitochondrial contribution to metabolic changes in the digestive gland of Mytilus galloprovincialis during anaerobiosis // J. Exp. Zool. 2000. V. 286. Iss. 2. P. 107-113. https://doi.org/10.1002/(sici)1097-010x(20000201)286:2< 107::aid-jez1>3.0.co;2-8.Buck L. T. Succinate and alanine as anaerobic end-products in the diving turtle (Chrysemys picta bellii) // Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology. 2000. V. 126. Iss. 3. P. 409–413. https://doi.org/10.1016/S0305-0491(00)00215-7Chang G. G., Tong L. Structure and function of malic enzymes, a new class of oxidative decarboxylases // Biochemistry. 2003. V. 42. No. 44. P. 12721–12733. https://doi.org/10.1021/bi035251+Chew S. F., Gan J., Ip Y. K. Nitrogen metabolism and excretion in the swamp eel, Monopterus albus, during 6 or 40 days of estivation in mud // Physiol. Biochem. Zool. 2005. V. 78. No 4. P. 620–629. https://doi.org/10.1086/430233Endo N., Kan-no N., Nagahisa E. Purification, characterization, and cDNA cloning of opine dehydrogenases from the polychaete rock worm Marphysa sanguinea // Comp. Biochem. Physiol. B. 2007. V. 14. P. 293–307.Giannetto A., Maisano M., Cappello T., Oliva S., Parrino V., Natalotto A., De Marco G., Barberi C., Romeo O., Mauceri A., Fasulo S. Hypoxia-Inducible Factor α and Hif-prolyl Hydroxylase Characterization and Gene Expression in Short-Time Air-Exposed Mytilus galloprovincialis // Mar. Biotechnol. 2015. V. 17. Iss. 6. P. 3–16. https://doi.org/10.1007/s10126-015-9655-7Gosling E. Ecological genetics of the mussels Mytilus edulis and M. galloprovincialis on Irish coasts // Marine Ecology Progress Series. 1981. V. 4. No 2. P. 221–227. https://doi.org/10.3354/meps004221Heise K., Puntarulo S., Nikinmaa M., Lucassen M., Portner H. O., Abele D. Oxidative stress and HIF-1 DNA binding during stressful cold exposure and recovery in the North Sea eelpout (Zoarces viviparus) // Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2006. V. 143. No 4. P. 494–503. https://doi.org/10.1016/j.cbpa.2006.01.014.Hollenbeck C. M., Johnston I. A. Genomic Tools and Selective Breeding in Molluscs // Front. Genet. 2018. V. 9. P. 1–15. https://doi.org/10.3389/fgene.2018.00253Ju Z., Wells M. C., Heater S. J., Walter R. B. Multiple tissue gene expression analyses in Japanese medaka (Oryzias latipes) exposed to hypoxia // Comp. Biochem. Physiol. C. 2007. V. 145. No 1. P. 134–144. https://doi.org/10.1016/j.cbpc.2006.06.012Karstensen J., Stramma L., Visbeck M. Oxygen minimum zones in the eastern tropical Atlantic and Pacific Oceans // Prog. Oceanogr. 2008. V. 77. P. 331–350. https://doi.org/10.1016/j.pocean.2007.05.009Kimura T., Nakano T., Yamaguchi T. et al. Complementary DNA Cloning and Molecular Evolution of Opine Dehydrogenases in Some Marine Invertebrates // October 2004 Marine Biotechnology. 2004. V. 6. Iss. 5. P. 493–502. https://doi.org/10.1007/s10126-004-2700-6Le Moullac G., Bacca H., Huvet A., Moal J., Pouvreau S., Van Wormhoudt A. Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia // J. Exp. Zool. A Ecol. Genet. Physiol. 2007. V. 307A. Iss. 7. P. 371–382. https://doi.org/10.1002/jez.390Livak, K. J., Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method // Methods. 2001. V. 25. Iss. 4, P. 402–408. https://doi.org/10.1006/meth.2001.1262Livingstone D. R. Origins and evolution of pathways of anaerobic metabolism in the animal kingdom // Am. Zool. 1991. V. 31. P. 522–534.Paulmier A., Ruiz-Pino D. Oxygen minimum zones in the modern ocean // Prog. Oceanogr. 2009. V. 80. P. 113–128. https://doi.org/10.1016/j.pocean.2008.08.001Rabalais N. N., Cai W.-J., Carstensen J. Eutrophication-driven deoxygenation in the coast-al ocean // Oceanography. 2014. V. 27. No 1. P. 172–183. https://doi.org/10.5670/oceanog.2014.21.Rees B. B., Bowman J. A.L., Schulte P. M. Structure and sequence conservation of a putative hypoxia response element in the lactate dehydrogenase-B gene of Fundulus // Biol. Bull. 2001. V. 200. P. 247–251. https://doi.org/10.2307/1543505Soitamo A. J., Raabergh C. M.I., Gassmann M., Sistonen L., Nikinmaa M. Characterization of a Hypoxia-inducible Factor (HIF-1) from Rainbow Trout: Accumulation of protein occurs at normal venous oxygen tension // J. Biol. Chem. 2001. V. 276. No 23. P. 19699–19705. https://doi.org/10.1074/jbc.M009057200.Sokolova I. M., Pörtner H. O. Temperature effects on key metabolic enzymes in Littorina saxatilis and L. obtusata from different latitudes and shore levels // Mar. Biol. 2001. V. 139. P. 113–126.Soldatov A. A., Andreenko T. I., Golovina I. V., Stolbov A. Y. Peculiarities of organization of tissue metabolism in molluscs with different tolerance to external hypoxia // J. Evol. Biochem. Physiol. 2010. V. 46. No 4. P. 341–349. https://doi.org/10.1134/S0022093010040022Soldatov A. A., Andreenko T. I., Sysoeva I. V., Sysoev A. A. Tissue specificity of metabolism in the bivalve mollusc Anadara inaequivalvis Br. under conditions of experimental anoxia // J. Evol. Biochem. Physiol. 2009. V. 45. No 3. P. 349–355. https://doi.org/10.1134/S002209300903003XSoldatov A. A., Golovina I. V., Lantushenko A. O., Kokhan A. S., Sysoeva I. V., Sysoev A. A., Kolesnikova E. E. Adenylate System State, Malate Dehydrogenase Activity and Expression Level in Tissues of Mytilus galloprovincialis Lamarck, 1819 // Thalassas: An International Journal of Marine Sciences. 2023. V. 39. P. 739–747. https://doi.org/10.1007/s41208-023-00563-4Soldatov A. A., Gostyukhina O. L., Golovina I. V. Functional states of antioxidant enzymatic complex of tissues of Mytillus galloprovincialis Lam. under conditions of oxidative stress // J. Evol. Biochem. Physiol. 2014. V. 50. Iss. 3. P. 206–214. https://doi.org/10.1134/S0022093014030028Storey K. B., Dando P. R. Substrate specificities of octopine dehydrogenases from marine invertebrates // Comp. Biochem. Physiol. B Comp. Biochem. 1982. V. 73. P. 521–528. https://doi.org/10.1016/0305-0491(82)90069-4Storey K. B., Storey J. M. Metabolic rate depression in animals: transcriptional and translational controls // Biol. Rev. 2004. V. 79. P. 207–233. https://doi.org/10.1017/s1464793103006195St-Pierre J., Tattersall G. J., Boutilier R. G. Metabolic depression and enhanced O2 affinity of mitochondria in hypoxic hypometabolism // Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000. V. 279. Iss. 4. P. R1205–R1214. https://doi.org/10.1152/ajpregu.2000.279.4.R1205Strugnell J. M., Collins M. A., Allcock A. L. Molecular evolutionary relationships of the octopodid genus Thaumeledone (Cephalopoda: Octopodidae) from the Southern Ocean // Antarctic Science. 2008. V. 20. P. 245–251.Van Hellemond J. J., Van der Klei A., Van Weelden S. W.H. Tielens A. G.M. Biochemical and evolutionary aspects of anaerobically functioning mitochondria // Philos. Trans. R. Soc. B Biol. Sci. 2003. V. 358. P. 205–215. https://doi.org/10.1098/rstb.2002.1182Vázquez-Dorado S., Sanjuan A., Comesaña A. S., Carlos A. Identification of octopine dehydrogenase from Mytilus galloprovincialis // Comparative Biochemistry and Physiology Part B. 2011. V. 160. P. 94–103. https://doi.org/10.1016/j.cbpb.2011.07.003Vázquez-Dorado S., De Carlos A., Comesaña A. S., Andrés Sanjuán A. Phylogenetic comparison of opine dehydrogenase sequences from marine invertebrates // Biochem. Genet. 2013. V. 51. Iss. 1–2. P. 154–65. DOI: 10.1007/s10528-012-9551-zZammit V. A. Possible relationship between energy metabolism of muscle and oxygen binding characteristics of haemocyanin of cephalopods // J. Mar. Biol. Assoc. UK. 1978. V. 58. P. 421–424. DOI: 10.1017/S0025315400028083