Влияние размера тела на состав липидов и жирных кислот митохондрий у мидий Mytilus edulis Linnaeus

Н.Н. Фокина, И.В. Суховская и А.А. Сухотин

Труды Зоологического института РАН, 2024, 328(4): 691–706 · https://doi.org/10.31610/trudyzin/2024.328.4.691

Резюме

Митохондрии играют решающую роль в энергетическом обмене, а зависимость скорости метаболизма от размеров тела (метаболическая аллометрия) может быть связана со свойствами мембран и их липидным составом. В настоящем исследовании изучалось влияние размера тела на состав липидов и жирных кислот митохондрий двустворчатых моллюсков мидий Mytilus edulis L. из Белого моря. Проанализированы мидии разных размеров, в диапазоне от 0.3 до 12.7 г сырой массы мягких тканей. Из тканей жабр были выделены митохондрии и определен их липидный и жирнокислотный состав. Показано, что, в отличие от фосфолипидов и триацилглицеринов, доля стеринов в мембранах митохондрий варьирует в зависимости от размера мидий. В частности, более крупные моллюски имели низкую долю холестерина, но более высокую долю мононенасыщенных жирных кислот. В составе фосфолипидов митохондрий доминировали насыщенные жирные кислоты (НЖК), особенно пальмитиновая (16:0) и стеариновая (18:0) кислоты. Доля НЖК уменьшалась с увеличением массы тела мидий. И наоборот, мононенасыщенные жирные кислоты (МНЖК) показали положительную корреляцию с размером тела, значительно увеличиваясь у более крупных особей. Доля полиненасыщенных жирных кислот (ПНЖК) в митохондриях беломорских мидий была низкой (менее 25% от суммы всех ЖК) и не зависела от массы тела. Пониженные значения ПНЖК характерны для митохондрий двустворчатых моллюсков из арктических морей, а также для долгоживущих видов Bivalvia. Наши данные указывают на относительную стабильность липидного и ЖК состава митохондрий беломорских мидий. Вероятно, подобная черта жирнокислотного профиля фосфолипидов митохондрий является биохимической адаптацией, которая позволяет моллюскам поддерживать эффективный уровень активности мембранно-связанных белков независимо от размера особей.

Ключевые слова

аллометрия, жирные кислоты, липидный состав, митохондрии, размер тела, Mytilus edulis

Поступила в редакцию 22 августа 2024 г. · Принята в печать 27 ноября 2024 г. · Опубликована онлайн 25 декабря 2024 г.

Литература

Abele D., Vázquez-Medina J.P. and Zenteno-Savín T. (Eds) 2011. Oxidative Stress in Aquatic Ecosystems. John Wiley & Sons, Ltd, Chichester, UK, 548 p.

Alkanani T., Parrish C.C., Thompson R.J. and McKenzie C.H. 2007. Role of fatty acids in cultured mussels, Mytilus edulis, grown in Notre Dame Bay, Newfoundland. Journal of Experimental Marine Biology and Ecology, 348: 33–45. https://doi.org/10.1016/j.jembe.2007.02.017

Araújo J., Soares F., Medeiros A., Bandarra N.M., Freire M., Falcão M. and Pousão-Ferreira P. 2020. Depth effect on growth and fatty acid profile of Mediterranean mussel (Mytilus galloprovincialis) produced on a longline off south Portugal. Aquaculture International, 28: 927–946. https://doi.org/10.1007/s10499-019-00504-0

Baptista M., Repolho T., Maulvault A.L., Lopes V.M., Narciso L., Marques A., Bandarra N. and Rosa R. 2014. Temporal dynamics of amino and fatty acid composition in the razor clam Ensis siliqua (Mollusca: Bivalvia). Helgoland Marine Research, 68: 465–482. https://doi.org/10.1007/s10152-014-0402-7

Barnathan G. 2009. Non-methylene-interrupted fatty acids from marine invertebrates: Occurrence, characterization and biological properties. Biochimie, 91: 671–678. https://doi.org/10.1016/j.biochi.2009.03.020

Bell J.G. and Sargent J.R. 2003. Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture, 218: 491–499. https://doi.org/10.1016/S0044-8486(02)00370-8

Bergé J.P. and Barnathan G. 2005. Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. In: R. Ulber and Y. Le Gal (Eds). Marine Biotechnology I. Advances in Biochemical Engineering/Biotechnology, vol. 96. Springer, Berlin, Heidelberg: 49–125. https://doi.org/10.1007/b135782

Boël M., Romestaing C., Duchamp C., Veyrunes F., Renaud S., Roussel D. and Voituron Y. 2020. Improved mitochondrial coupling as a response to high mass-specific metabolic rate in extremely small mammals. Journal of Experimental Biology, 223: jeb215558. https://doi.org/10.1242/jeb.215558

Brand M.D., Turner N., Ocloo A., Else P.L. and Hulbert A.J. 2003. Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochemical Journal, 376: 741–748. https://doi.org/10.1042/BJ20030984

Burpee J.L., Bardsley E.L., Dillaman R.M., Watanabe W.O. and Kinsey S.T. 2010. Scaling with body mass of mitochondrial respiration from the white muscle of three phylogenetically, morphologically and behaviorally disparate teleost fishes. Journal of Comparative Physiology B, 180: 967–977. https://doi.org/10.1007/s00360-010-0474-x

Crockett E.L. 1998. Cholesterol function in plasma membranes from ectotherms: membrane-specific roles in adaptation to temperature. American Zoologist, 38: 291–304. https://doi.org/10.1093/icb/38.2.291

Crockett E.L. 2008. The cold but not hard fats in ectotherms: consequences of lipid restructuring on susceptibility of biological membranes to peroxidation, a review. Journal of Comparative Physiology B, 178: 795–809. https://doi.org/10.1007/s00360-008-0275-7

Dudognon T., Lambert C., Quere C., Auffret M., Soudant P. and Kraffe E. 2014. Mitochondrial activity, hemocyte parameters and lipid composition modulation by dietary conditioning in the Pacific oyster Crassostrea gigas. Journal of Comparative Physiology B, 184: 303–317. https://doi.org/10.1007/s00360-013-0800-1

Egorova M.V. and Afanasyev S.A. 2011. Isolation of mitochondria from human and animal cells and tissues: modern methodological techniques. Siberian Medical Journal, 26(1): 22–28. [In Russian].

Ernst R., Ejsing C.S. and Antonny B. 2016. Homeoviscous Adaptation and the Regulation of Membrane Lipids. Journal of Molecular Biology, 428: 4776–4791. https://doi.org/10.1016/j.jmb.2016.08.013

Fiorini R., Pagliarani A., Nesci S., Pirini M., Tucci E. and Ventrella V. 2012. Structural and functional changes in gill mitochondrial membranes from the Mediterranean mussel Mytilus galloprovincialis exposed to tri-N-butyltin. Environmental Toxicology and Chemistry, 31: 877–884. https://doi.org/10.1002/etc.1764

Fokina N.N., Lysenko L.A., Sukhovskaya I.V., Vdovichenko E.A., Borvinskaya E.V., Kantserova N.P., Krupnova M.Yu., Ruokolainen T.R., Smirnov L.P., Vysotskaya R.U., Bakhmet I.N. and Nemova N.N. 2015. Biochemical response of blue mussels Mytilus edulis L. from the White Sea to rapid changes in ambient temperature. Journal of Evolutionary Biochemistry and Physiology, 51(5): 378–387. https://doi.org/10.1134/S0022093015050038

Fokina N.N., Nefedova Z.A., Nemova N.N., Ruokolainen T.R. and Bakhmet I.N. 2013. Effects of various salinity on the White Sea blue mussels Mytilus edulis lipid composition. Proceedings of the Zoological Institute RAS, 317(Supplement 3): 55–62. [In Russian].

Fokina N.N., Ruokolainen T.R., Nemova N.N., Martynova D.M. and Sukhotin A.A. 2020. Fatty acids distribution in seston, tissues, and faecal pellets of blue mussels Mytilus edulis L. Doklady Biochemistry and Biophysics, 495: 311–318. https://doi.org/10.1134/S1607672920060046

Folch J., Lees M. and Sloane Stanley G.H. 1957. A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry, 226: 497–509.

Freites L., Fernandez-Reiriz M.J. and Labarta U. 2002. Fatty acid profiles of Mytilus galloprovincialis (Lmk) mussel of subtidal and rocky shore origin. Comparative Biochemistry and Physiology B, 132: 453–461. https://doi.org/10.1016/S1096-4959(02)00057-X

Gillis T. and Ballantyne J. 1999. Mitochondrial membrane composition of two arctic marine bivalve mollusks, Serripes groenlandicus and Mya truncata. Lipids, 34: 53–57. https://doi.org/10.1007/s11745-999-337-0

Glazier D.S. 2015. Body-mass scaling of metabolic rate: what are the relative roles of cellular versus systemic effects? Biology, 4: 187–199. https://doi.org/10.3390/biology4010187

Glazier D.S. 2022. Complications with body-size correction in comparative biology: possible solutions and an appeal for new approaches. Journal of Experimental Biology, 225: jeb243313. https://doi.org/10.1242/jeb.243313

Gonzalez A., Pagé B., Weber J.-M. 2015. Membranes as a possible pacemaker of metabolism in cypriniform fish: does phylogeny matter? The Journal of Experimental Biology, 218: 2563–2572. https://doi.org/10.1242/jeb.117630

Guderley H., Pierre J.St., Couture P. and Hulbert A.J. 1997. Plasticity of the properties of mitochondria from rainbow trout red muscle with seasonal acclimatization. Fish Physiology and Biochemistry, 16: 531–541. https://doi.org/10.1023/A:1007708826437

Hazel J. and Williams E.E. 1990. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Progress in Lipid Research, 29: 167–227. https://doi.org/10.1016/0163-7827(90)90002-3

Hellwig J. 2005. Defining Parameters for a Reproducible TLC-separation of Phospholipids Using ADC2. PhD Thesis. University of Applied Sciences Northwestern Switzerland (FHNW), 63 p.

Hochachka P.W. and Somero G.N. 2002. Biochemical adaptation Mechanism and Process in Physiological Evolution. Oxford University Press, NY, 466 p. https://doi.org/10.1093/oso/9780195117028.001.0001

Hulbert A.J. 2010. Metabolism and longevity: Is there a role for membrane fatty acids? Integrative and Comparative Biology, 50: 808–817. https://doi.org/10.1093/icb/icq007

Hulbert A.J. and Else P.L. 1999. Membranes as possible pacemakers of metabolism. Journal of Theoretical Biology, 199: 257–274. https://doi.org/10.1006/jtbi.1999.0955

Istomina A.A., Zhukovskaya A.F., Mazeika A.N., Barsova E.A., Chelomin V.P., Mazur M.A., Elovskaya O.A., Mazur A.A., Dovzhenko N.V., Fedorets Y.V. and Karpenko A.A. 2023. The relationship between lifespan of marine bivalves and their fatty acids of mitochondria lipids. Biology, 12: 837. https://doi.org/10.3390/biology12060837

Kandyuk R.P. 2006. Sterines in mollusks and their functional role (review). Gidrobiologicheskiy Zhurnal, 42(1): 62–74. [In Russian]. https://doi.org/10.1615/HydrobJ.v42.i3.50

Kapranova L.L., Nekhoroshev M.V., Malakhova L.V., Ryabushko V.I., Kapranov S.V. and Kuznetsova T.V. 2019. Fatty acid composition of gonads and gametes in the Black Sea bivalve mollusk Mytilus galloprovincialis Lam. at different stages of sexual maturation. Journal of Evolutionary Biochemistry and Physiology, 55(6): 448–455. https://doi.org/10.1134/S0022093019060024

Kelly J. and Scheibling R. 2012. Fatty acids as dietary tracers in benthic food webs. Marine Ecology Progress Series, 446: 1–22. https://doi.org/10.3354/meps09559

Khan M.A., Parrish C.C. and Shahidi F. 2006. Effects of Environmental Characteristics of Aquaculture Sites on the Quality of Cultivated Newfoundland Blue Mussels (Mytilus edulis). Journal of Agricultural and Food Chemistry, 54: 2236–2241. https://doi.org/10.1021/jf051587

Kleiber M. 1932. Body size and metabolism. Hilgardia, 6: 315–353.

Kraffe E., Soudant P., Marty Y. and Kervarec N. 2005. Docosahexaenoic acid- and eicosapentaenoic acid-enriched cardiolipin in the Manila clam Ruditapes philippinarum. Lipids, 40(6): 619–625. https://doi.org/10.1007/s11745-005-1423-z

Kraffe E., Tremblay R., Belvin S., LeCoz J.-R., Marty J. and Guderley H. 2008. Effect of reproduction on escape responses, metabolic rates end muscle mitochondrial properties in the scallop Placopecten magellanicus. Marine Biology, 156: 25–38. https://doi.org/10.1007/s00227-008-1062-4

Lin H., Jiang J., Xue C.-H., Zhang B. and Xu J.-C. 2003. Seasonal changes in phospholipids of mussel (Mytilus edulis Linne). Journal of the Science of Food and Agriculture, 83: 133–135. https://doi.org/10.1002/jsfa.1281

Lindstedt S.L. and Hoppeler H. 2023. Allometry: revealing evolution’s engineering principles. Journal of Experimental Biology, 226: jeb245766. https://doi.org/10.1242/jeb.245766

Logue J.A., De Vries A.L., Fodor E. and Cossins A.R. 2000. Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. Journal of Experimental Biology, 203: 2105–2115. https://doi.org/10.1242/jeb.203.14.2105

Munro D. and Blier P.U. 2012. The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranes. Aging Cell, 11: 845–855. https://doi.org/10.1111/j.1474-9726.2012.00847.x

Narváez M., Freites L., Guevara M., Mendoza J., Guderley H., Lodeiros C.J. and Salazar G. 2008. Food availability and reproduction affects lipid and fatty acid composition of the brown mussel, Perna perna, raised in suspension culture. Comparative Biochemistry and Physiology B, 149: 293–302. https://doi.org/10.1016/j.cbpb.2007.09.018

Olsen R.E. and Henderson R.J. 1989. The rapid analysis of neutral and polar marine lipids using double-development HPTLC and scanning densitometry. Journal of Experimental Marine Biology and Ecology, 129: 189–197. https://doi.org/10.1016/0022-0981(89)90056-7

Pazos A.J., Román G., Acosta C.P., Sánchez J.L. and Abad M. 1997. Lipid classes and fatty acid composition in the female gonad of Pecten maximus in relation to reproductive cycle and environmental variables. Comparative Biochemistry and Physiology B, 117: 393–402. https://doi.org/10.1016/S0305-0491(97)00135-1

Porter R.K. 2001. Allometry of mammalian cellular oxygen consumption. Cellular and Molecular Life Sciences, 58: 815–822. https://doi.org/10.1007/PL00000902

Porter R.K. and Brand M.D. 1995. Causes of differences in respiration rate of hepatocytes from mammals of different body mass. American Journal of Physiology, 269: R1213–R1224. https://doi.org/10.1152/ajpregu.1995.269.5.r1213

Porter R.K., Hulbert A.J. and Brand M.D. 1996. Allometry of mitochondria proton leak: influence of membrane surface area and fatty acid composition. American Journal of Physiology, 271: R1550–R1560. https://doi.org/10.1152/ajpregu.1996.271.6.r1550

Prato E., Danieli A., Maffia M. and Biandolino F. 2010. Lipid and Fatty Acid Compositions of Mytilus galloprovincialis Cultured in the Mar Grande of Taranto (Southern Italy): Feeding Strategies and Trophic Relationships. Zoological Studies, 49: 211–219.

Puccinelli E., Noyon M. and McQuaid C.D. 2017. Trophic signatures of co-existing invasive and indigenous mussels: selective feeding or different metabolic pathways? Hydrobiologia, 784: 187–199. https://doi.org/10.1007/s10750-016-2873-9

Renne M.F. and Ernst R. 2023. Membrane homeostasis beyond fluidity: control of membrane compressibility. Trends in Biochemical Sciences, 48: 963–977. https://doi.org/10.1016/j.tibs.2023.08.004

Richoux N.B. and Ndhlovu R.T. 2014. Temporal shifts in the fatty acid profiles of rocky intertidal invertebrates. Marine Biology, 161: 2199–2211. https://doi.org/10.1007/s00227-014-2481-z

Roussel D., Salin K., Dumet A., Romestaing C., Rey B. and Voituron Y. 2015. Oxidative phosphorylation efficiency, proton conductance and reactive oxygen species production of liver mitochondria correlates with body mass in frogs. Journal of Experimental Biology, 218: 3222–3228. https://doi.org/10.1242/jeb.126086

Schmidt-Nielsen K. 1984. Scaling: Why Is Animal Size so Important? Cambridge Univ Press, UK, Cambridge, 241 p. https://doi.org/10.1017/CBO9781139167826

Schmitz G. and Ecker J. 2008. The opposing effects of n-3 and n-6 fatty acids. Progress in Lipid Research, 47: 147–155. https://doi.org/10.1016/j.plipres.2007.12.004

Sinensky M. 1974. Homeoviscous Adaptation – A Homeostatic Process that Regulates the Viscosity of Membrane Lipids in Escherichia coli. PNAS, 71: 522–525. https://doi.org/10.1073/pnas.71.2.522

Sukhotin A., Alexeeva N., Gerasimova M. and Kovalev A. 2024. Body size influence on respiration rate and mitochondrial metrics in Mytilus edulis L. gill tissue. Journal of Evolutionary Biochemistry and Physiology, 60: 1399–1407. https://doi.org/10.1134/S0022093024040112

Sukhotin A., Fokina N., Ruokolainen T., Bock C., Pörtner H.-O. and Lannig G. 2017. Does the Membrane Pacemaker Theory of metabolism explain the size dependence of metabolic rate in marine mussels? Journal of Experimental Biology, 220: 1423–1434. https://doi.org/10.1242/jeb.147108

Sukhotin A., Kovalev A., Sokolov E. and Sokolova I.M. 2020. Mitochondrial performance of a continually growing marine bivalve, Mytilus edulis, depends on body size. Journal of Experimental Biology, 223: jeb.226332. https://doi.org/10.1242/jeb.226332

Ventrella V., Pirini M., Pagliarani A., Trombetti F., Manuzzi M.P. and Borgatti A.R. 2008. Effect of temporal and geographical factors on fatty acid composition of M. galloprovincialis from the Adriatic Sea. Comparative Biochemistry and Physiology B, 149: 241–250. https://doi.org/10.1016/j.cbpb.2007.09.012

White C.R., Marshall D.J., Alton L.A., Arnold P.A., Beaman J.E., Bywater C.L., Condon C., Crispin T.S., Janetzki A., Pirtle E., Winwood-Smith H.S., Angilletta Jr. M.J., Chenoweth S.F., Franklin C.E., Halsey L.G., Kearney M.R., Portugal S.J. and Ortiz-Barrientos D. 2019. The origin and maintenance of metabolic allometry in animals. Nature Ecology & Evolution, 3: 598–603. https://doi.org/10.1038/s41559-019-0839-9

Zhukova N.V. 1991. The pathway of the biosynthesis of non-methylene-interrupted dienoic fatty acids in molluscs. Comparative Biochemistry and Physiology B, 100: 801–804. https://doi.org/10.1016/0305-0491(91)90293-M