Biochemical and molecular-genetic growth indices of rainbow trout (Oncorhynchus mykiss Walb.) in the conditions of the southern region of the Russian Federation in a long-term study

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Abstract

The expression of genes encoding transcriptional myogenic regulatory factors (MRF) in muscles, and the activity of enzymes involved in energy and carbohydrate metabolism in the liver and muscles of rainbow trout Oncorhynchus mykiss Walb., grown under 24-hour lighting and fed at night in aquaculture conditions in one of the southern regions of the Russian Federation for seven months, were studied. The results of the study showed that this regime, introduced into the standard technology of trout growing, had a beneficial effect on its condition and growth. By the end of the study, trout individuals grown under the experimental regime differed from the control variants in having higher expression levels of the MRF genes (myod1, myf5, mlc2, mstn1a) and increased activity of pyruvate kinase and cytochrome c oxidase in the liver. It can be assumed that the introduction of additional lighting and feeding at night into the technology of trout cultivation stimulates aerobic metabolism, promotes the intensification of muscle growth processes in trout individuals and, in general, has a positive effect on the fish organism condition.

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About the authors

M. A. Rodin

Federal Research Center “ Karelian Research Center of the Russian Academy of Sciences”

Author for correspondence.
Email: mikhail.rodin.mr@yandex.ru

Institute of Biology

Russian Federation, st. Pushkinskaya, 11, Petrozavodsk, 185910

M. V. Kuznetsova

Federal Research Center “ Karelian Research Center of the Russian Academy of Sciences”

Email: mikhail.rodin.mr@yandex.ru

Institute of Biology

Russian Federation, st. Pushkinskaya, 11, Petrozavodsk, 185910

M. Yu. Krupnova

Federal Research Center “ Karelian Research Center of the Russian Academy of Sciences”

Email: mikhail.rodin.mr@yandex.ru

Institute of Biology

Russian Federation, st. Pushkinskaya, 11, Petrozavodsk, 185910

A. E. Kuritsyn

Federal Research Center “ Karelian Research Center of the Russian Academy of Sciences”

Email: mikhail.rodin.mr@yandex.ru

Institute of Biology

Russian Federation, st. Pushkinskaya, 11, Petrozavodsk, 185910

N. N. Nemova

Federal Research Center “ Karelian Research Center of the Russian Academy of Sciences”

Email: mikhail.rodin.mr@yandex.ru

Institute of Biology

Russian Federation, st. Pushkinskaya, 11, Petrozavodsk, 185910

References

  1. Колб В. Г., Камышников В. С. Клиническая биохимия // Минск: Изд-во Беларусь. 1976. 311 с.
  2. Кочетов Г. А. Практическое руководство по энзимологии // М.: Высш. шк. 1980. 272 с.
  3. Мурзина С. А., Провоторов Д. С., Воронин В. П., Кузнецова М. В., Курицын А. Е., Немова Н. Н. Показатели липидного обмена у сеголетков атлантического лосося Salmo Salar, выращиваемых в условиях аквакультуры в Южном Регионе РФ при дифференциальных режимах освещения и кормления // Известия РАН. Сер. Биол. 2023. № 2. С. 134–148. https://doi.org/10.31857/S1026347022700081
  4. Озернюк Н. Д. Энергетический обмен в раннем онтогенезе рыб. М.: Наука. 1985. 175 c.
  5. Aidos L., Cafiso A., Bertotto D., Bazzocchi C., Radaelli G., Di Giancamillo A. How different rearing temperatures affect growth and stress status of Siberian sturgeon Acipenser baerii larvae // J. Fish Biol. 2020. V. 96. № 4. P. 913–924. https://doi.org/10.1111/jf b.14280
  6. Alami-Durante H., Cluzeaud M., Bazin D., Schrama J. W., Saravanan S., Geurden I. Muscle growth mechanisms in response to isoenergetic changes in dietary non-protein energy source at low and high protein levels in juvenile rainbow trout // Comp. Biochem. Physiol. Part A: Mol. Integr. Physiol. 2019. V. 230. P. 91–99. https://doi.org/10.1016/j.cbpa.2019.01.009
  7. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. An overview of the cell cycle. Molecular Biology of the Cell. 4th edition // New York: Garland Science, 2002.
  8. Barimani S., Kazemi M. B., Hazaei K. Effects of different photoperiod regimes on growth and feed conversion rate of young Iranian and French rainbow trout (Oncorhynchus mykiss) // World Appl. Sci. J. 2013. Vol. 21. P. 1440–1444. https://doi.org/10.5829/idosi.wasj.2013.21.10.2700
  9. Bjornsson B. T. The biology of salmon growth hormone: From daylight to dominance // Fish Physiology and Biochemistry. 1997. V. 17. P. 9–24. https://doi.org/10.1023/a:1007712413908
  10. Boeuf G., Falcon J. Photoperiod and growth in fish // Vie Milieu. 2002. V. 51. P. 237–246.
  11. Bower N. I., Johnston I. A. Paralogs of Atlantic salmon myoblast determination factor genes are distinctly regulated in proliferating and differentiating myogenic cells // Am. J. Phys. Regul. Integr. Comp. Phys. 2010. V. 298. P. 1615–1626. https://doi.org/10.1152/ajpregu.00114.2010
  12. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding // Anal. Biochem. 1976. Vol. 72. P. 248–254.
  13. Bücher T., Pfleiderer G. Pyruvate kinase from muscle: Pyruvate phosphokinase, pyruvic phosphoferase, phosphopyruvate transphosphorylase, phosphate-transferring enzyme II, etc. // Methods Enzymol. 1955. V. 1. P. 345–440.
  14. Chapalamadugu K. C., Robison B. D., Drew R. E., Powell M. S., Hill R. A., Amberg J. J., Rodnick K. J., Hardy R. W., Hill M. L., Murdoch G. K. Dietary carbohydrate level affects transcription factor expression that regulates skeletal muscle myogenesis in rainbow trout // Comp. Biochem. Physiol. Part B. Biochem. Mol. Biol. 2009. V. 153. № 1. P. 66–72. https://doi.org/10.1016/j.cbpb.2009.01.013
  15. Churova M. V., Shulgina N. S., Kuritsyn A. E., Krupnova M. Y., Nemova N. N. Muscle-specific gene expression and metabolic enzyme activities in Atlantic salmon Salmo salar L. fry reared under different photoperiod regimes // Comp Biochem Physiol Part B. 2020. V. 239. P. 110330. https://doi.org/10.1016/j.cbpb.2019.110330
  16. Ergün S., Yigit M., Türker A. Growth and feed consumption of young rainbow trout (Oncorhynchus mykiss) exposed to different photoperiods // Isr. J. Aquac. 2003. Vol. 55. P. 132–138.
  17. Facciolo R. M., Crudo M., Giusi G., Alo R., Canonaco M. Light- and dark-dependent orexinergic neuronal signals promote neurodegenerative phenomena accounting for distinct behavioral responses in the teleost Thalassoma pavo // J. Neurosci. Res. 2009. V. 87. P. 748–757. https://doi.org/10.1002/jnr.21886
  18. Gauthier C., Campbell P., Couture P. Physiological correlates of growth and condition in the yellow perch (Perca flavescens) // Comparative Biochemistry and Physiology. Part A. 2008. V. 151. P. 526–532. https://doi.org/10.1016/j.cbpa.2008.07.010
  19. Hevroy E. M., Jordal A-E.O., Hordvik I., Espe M., Hemre G-I., Olsvik P. A. Myosin heavy chain mRNA expression correlates higher with muscle protein accretion than growth in Atlantic salmon, Salmo salar // Aquaculture. 2006. V. 252. № 2. P. 453–461. https://doi.org/10.1016/j.aquaculture.2005.07.003
  20. Houlihan D. F., Mathers E. M., Foster A. Biochemical correlates of growth rate in fish // Fish Ecophysiology. 1993. V. 9. P. 45–71. https://doi.org/10.1007/978-94-011-2304-4_2
  21. Imsland A. K., Le Francois N. R., Lammare S. G., Ditlecadet D., Sigurosson S., Foss A. Myosin expression levels and enzyme activity in juvenile spotted wolfish (Anarhichas minor) muscle: A method for monitoring growth rates // Can. J. Fish Aquat. Sci. 2006. V. 63. P. 1959–1967. https://doi.org/10.1139/f06-091
  22. Johansen K. A., Overturf K. Alterations in expression of genes associated with muscle metabolism and growth during nutritional restriction and refeeding in rainbow trout // Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2006. V. 144. P. 119–127. https://doi.org/10.1016/j.cbpb.2006.02.001
  23. Johansen K. A., Overturf K. Quantitative expression analysis of genes affecting muscle growth during the development of rainbow trout (Oncorhynchus mykiss) // Mar. Biotech. 2005. V. 7. P. 576–587. https://doi.org/10.1007/s10126-004-5133-3
  24. Johnston I. A. Environment and plasticity of myogenesis in teleost fish. // J. Exp. Biol. 2006. V. 209. № 12. P. 2249–2264. https://doi.org/10.1242/jeb.02153
  25. Johnston I. A., Manthri S., Smart A., Campbell P., Nickell D., Alderson R. Plasticity of muscle fibre number in seawater stages of Atlantic salmon in response to photoperiod manipulation // J. Exp. Biol. 2003. V. 206. № 19. P. 3425–3435. https://doi.org/10. 1242/jeb.00577.
  26. Kuznetsova M. V., Rodin M. A., Shulgina N. S., Krupnova M. Y., Kuritsyn A. E., Murzina S. A., Nemova N. N. The Influence of Different Lighting and Feeding Regimes on the Activity of Metabolic Enzymes in Farmed Atlantic Salmon Fingerlings // Russian Journal of Developmental Biology. 2023. Т. 54. №. 2. С. 147–155. https://doi.org/10.1134/S1062360423020030
  27. Langley B., Thomas M., Bishop A., Sharma M., Gilmour S., Kambadur R. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression // J. Biol. Chem. 2002. V. 277. P. 49831–49840. https://doi.org/10.1074/jbc.M204291200
  28. Leitão N. D.J., Pai-Silva M.D., De Almeida F. L.A., Portella M. C. The influence of initial feeding on muscle development and growth in pacu Piaractus mesopotamicus larvae // Aquaculture. 2011. V. 315. № 1–2. P. 78–85. https://doi.org/10.1016/j.aquaculture.2011.01.006
  29. Livak K. J., Schmittgen T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method // Methods. 2001. V. 25. P. 402–408. https://doi.org/10.1006/meth.2001.1262
  30. Llewellyn L., Sweeney G. E., Ramsurn V. P., Rogers S. A., Wigham T. Cloning and unusual expression profile of the aldolase B gene from Atlantic salmon // Biochim. Biophys. Acta. 1998. V. 1443. P. 375–380. https://doi.org/10.1016/S0167-4781(98)00229-2
  31. Lundova K., Matousek J., Prokesova M., Sebesta R., Policar T., Stejskal V. The effect of timing of extended photoperiod on growth and maturity of brook trout (Salvelinus fontinalis) // Aquac. Res. 2019. V. 50. № 6. P. 1697–1704. https://doi.org/10.1111/are.14053
  32. Macqueen, D.J., Robb, D., Johnston, I. A. Temperature influences the coordinated expression of myogenic regulatory factors during embryonic myogenesis in Atlantic salmon (Salmo salar L.) // J. Exp. Biol. 2007. V. 210. P. 2781–2794. https://doi.org/10.1242/jeb. 006981.
  33. McCormick S.D., Shrimpton J. M., Moriyama S., Björnsson B. T. Differential hormonal responses of Atlantic salmon parr and smolt to increased daylength: A possible developmental basis for smolting // Aquaculture. 2007. V. 273. № 2–3. P. 337–344. https://doi.org/10.1016/j.aquaculture.2007.10.015
  34. Meton I., Mediavilla D., Caseras A., Canto E., Fernandez F., Baanante I. V. Effect of diet composition and ration size on key enzyme activities of glycolysis-gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata) // Br. J. Nutr. 1999. V. 82. P. 223–232. https://doi.org/10.1017/S0007114599001403
  35. Nagasawa K., Giannetto A., Fernandes J. M. Photoperiod influences growth and mll (mixed-lineage leukaemia) expression in Atlantic cod // PLoSOne. 2012. V. 7. № 5. e36908. https://doi.org/10.1371/journal.pone.0036908.
  36. Noble C., Mizusawa K., Tabata M. Does light intensity affect self-feeding and food wastage in group-held rainbow trout and white-spotted charr? // J. Fish. Biol. 2005. V. 66. P. 1387–1399. https://doi.org/10.1111/j.0022-1112.2005.00690.x
  37. Noori A., Mojazi Amiri B., Mirvaghefi A., Rafiee G., Kalvani Neitali B. Enhanced growth and retarded gonadal development of farmed rainbow trout, Oncorhynchus mykiss (Walbaum) following a long-day photoperiod // Aquac. Res. 2015. V. 46. P. 2398–2406. https://doi.org/10.1111/are.12398
  38. Rodin M. A., Kuznetsova M. V., Krupnova M. Yu., Kuritsyn A. E., Murzina S. A., Nemova N. N. Activity of energy and carbohydrate metabolism enzymes in rainbow trout fingerlings (Oncorhynchus mykiss Walb.) when fed two types of commercial feed // Biology Bulletin. 2024a. Vol. 51. № 6. P. 1539–1548. https://doi.org/10.1134/S1062359024609972
  39. Rodin M. A., Kuznetsova M. V., Krupnova M. Yu., Kuritsyn A. E., Nemova N. N. Activities of Energy and Carbohydrate Metabolism Enzymes in Rainbow Trout Оncorhynchus mykiss Walb. upon Introduction of 24-hour Lighting in Aquaculture in Southern Russia // Doklady Biological Sciences. 2024b. https://doi.org/10.1134/S0012496624600441
  40. Shulgina N. S., Kuznetsova M. V., Nemova N. N. The effect of different lighting regimes on some molecular-genetic parameters of juvenile atlantic salmon’s (Salmo salar) muscle growth under artificial reproduction conditions // Russ. J. Dev. Biol. 2022. V. 53. № 6. P. 472–489. https://doi.org/10.1134/S106236042206008X
  41. Smith L. Spectrophotometric assay of cytochrome c oxidase // Methods in Biochem. Analysis. 1955. V. 2. P. 427–434. https://doi.org/10.1002/9780470110188.ch13
  42. Sonmez A. Y., Hisar O., Hisar S. A., Alak G., Aras M. S., Yanik T. The effects of different photoperiod regimes on growth, feed conversion rate and survival of rainbow trout (Oncorhynchus mykiss) fry // J. Anim. Vet. Adv. 2009. V. 8. № 4. P. 760–763. https://doi.org/10.5829/idosi.wasj.2013.21.10.2700
  43. Taylor J., Migaud H. Timing and duration of constant light affects rainbow trout (Oncorhynchus mykiss) growth during autumn–spring grow-out in freshwater // Aquac. Res. 2009. V. 40. № 13. P. 1551–1558. https://doi.org/10.1111/j.1365-2109.2009.02260.x
  44. Taylor J. F., Migaud H., Porter M. J.R., Bromage N. R. Photoperiod influences growth rate and plasma insulin-like growth factor-I levels in juvenile rainbow trout, Oncorhynchus mykiss // Gen. Comp. Endocrinol. 2005. V. 142. № 1–2. P. 169–185. https://doi.org/10.1016/j.ygcen.2005.02.006
  45. Thomas M., Langley B., Berry C., Sharma M., Kirk S., Bass J., Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation // J. Biol. Chem. 2000. V. 275. P. 40235–40243. https://doi.org/10.1074/jbc.M004356200
  46. Tian W. N., Braunstein L. D., Pang J., Stuhlmeier K. M., Xi Q. C., Tian X., Stanton R. C. Importance of glucose-6-phosphate dehydrogenase activity for cell growth // J. Biol. Chem. 1998. V. 273. P. 10609–10617. https://doi.org/10.1074/jbc.273.17.10609
  47. Treberg J. R., Lewis J. M., Driedzic W. R. Comparison of liver enzymes in osmerid fishes: key differences between a glycerol accumulating species, rainbow smelt (Osmerus mordax), and a species that does not accumulate glycerol, capelin (Mallotus villosus) // Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2002. V. 132. P. 433–438. https://doi.org/10.1016/S1095-6433(02)00083-1
  48. Türker A. Effect of photoperiod on growth of trout (Oncorhynchus mykiss) in cold ambient sea water // Isr. J. Aquac. 2009. Vol. 61. P. 57–62.
  49. Watabe, S., Ikeda, D. Diversity of the pufferfish (Takifugu rubripes) fast skeletal myosin heavy chain genes // Comp. Biochem. Physiol. 2006. V. 1. P. 28–34. https://doi.org/10.1016/j.cbd.2005.12.001
  50. Wootton R. J. Growth: Еnvironmental effects // Encyclopedia of fish physiology: From genome to environment / Ed. Farrell A. P. San Diego: Academic Press. 2011. V. 3. P. 1629–1632.

Supplementary files

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1. JATS XML
2. Fig. 1. Average monthly temperature.

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3. Fig. 2. Average weight and specific growth rate (numbers on graphs) of trout individuals grown under different lighting and feeding regimes.

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4. Fig. 3. Enzyme activity in the liver of trout individuals grown under different lighting and feeding regimes. LDH activity is presented as a value/20. * – differences between experimental groups are significant, p < 0.05.

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5. Fig. 4. Enzyme activity in the muscles of trout individuals grown under different lighting and feeding conditions. CO activity is presented as a value*200. * – differences between experimental groups are significant, p < 0.05.

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