The synthesis of lipids and proteins in vitro in tissues of Cyprinus carpio infected with Bothriocephalus acheilognathi

  • L. L. Yuskiv Stepan Gzhytskyj Lviv National University of Veterinary Medicine and Biotechnologies
  • I. D. Yuskiv Stepan Gzhytskyj Lviv National University of Veterinary Medicine and Biotechnologies
Keywords: intestine; hepatopancreas; skeletal muscle; metabolism; synthesis; fish

Abstract

The problem of the mechanisms of regulation of biochemical processes in carp Cyprinus carpio (Linnaeus, 1758) tissues and organs caused by infection with Bothriocephalus (Schyzocotyle) acheilognathi (Yamaguti, 1934) at different intensities of invasion remains practically unstudied. The purpose of this study was to dedetrmine the intensity of lipid and protein synthesis in vitro when [6-14C]glucose and [2-14C]lysine are used as their precursor in the tissues of the intestine, hepatopancreas and skeletal muscles of carp. The study was conducted on this-year carp with body weight 14.5–20.5 g, at different invasion rates of the helminth B. acheilognathi, which belongs to the family Bothriocephalidae of the Pseudophyllidae order of the Cestoda class of the Plathelminthes phylum. The examined carp were divided into three groups: 1st group of fish was free from intestinal helminths of B. acheilognathi (control); 2nd group of fish was weakly infected with helminths (intensity of invasion was 1–3 helminths per fish); the 3rd group of fish was highly infected (the invasion intensity was 4 worms and more per fish). Our results showed that in fish infected with the helminth B. acheilognathi in comparison to uninfected, the intensity of lipid synthesis in the intestinal wall, hepatopancreas, skeletal muscle was much lower when [6-14C]glucose was used as a predecessor than when [2-14C]lysine was used as a predecessor. In the examined tissues, significant decrease was observed in the synthesis of reserve lipids (mono-, di- and triacylglycerols) in comparison to the structural (phospholipids and cholesterol), which depends on the intensity of the B. acheilognathi invasion. In the metabolic processes in the wall of the intestine, hepatopancreas, skeletal muscle of this-year carp infectd with B. acheilognathi helminths, under in vitro conditions, [6-14C]glucose was used more than [2-14C]lysine. The intensity of protein synthesis in the intestinal wall, hepatopancreas, skeletal muscles of this-year carp infected with the helminth B. acheilognathi under in vitro conditions increased when [6-14C]glucose was added to the incubation medium, on average 7.1–28.3% and decreased when [2-14C]lysine was added, on average 7.8–25.7%.

References

Ahmad, F., Fazili, K. M., Sof, O. M., Sheikh, B. A., & Sof, T. A. (2018). Distribución y patología causada por Bothriocephalus acheilognathi, Yamaguti 1934 (Cestoda: Bothriocephalidae). Revisión bibliográfica. Revista Veterinaria, 29(2), 142–149.

Albaugh, B. N., Arnold, K. M., & Denu, J. M. (2010). KAT(ching) metabolism by the tail: Insight into the links between lysine acetyltransferases and metabolism. ChemBioChem, 12(2), 290–298.

Al-Niaeemi, B. H., & Dawood, M. H. (2017). Tоtal lipids estimation and fatty acids analysis of Bothriocephalus acheilognathi, a parasitic tapeworm of the common carp (Cyprinus carpio L., 1758) from Tigris river-Mosul city. World Journal of Pharmacy and Pharmaceutical Sciences, 6(9), 1641–1651.

Bar, N., & Volkoff, H. (2012). Adaptation of the physiological, endocrine, and digestive system functions to prolonged food deprivation in fish. In: McCue, M. D. (Ed.). Comparative physiology of fasting, starvation, and food limitation. Springer, Heidelberg. Pp. 69–89.

Bertucci, J. I., Blanco, A. M., Sundarrajan, L., Rajeswari, J. J., Velasco, C., & Unniappan, S. (2019). Nutrient regulation of endocrine factors influencing feeding and growth in fish. Frontiers in Endocrinology, 2019, 10.

Britton, J. R., & Andreou, D. (2016). Parasitism as a driver of trophic niche specialisation. Trends in Parasitology, 32(6), 437–445.

Britton, J. R., Pegg, J., & Williams, C. F. (2011). Pathological and ecological host consequences of infection by an introduced fish parasite. PLoS One, 6(10), e26365.

Conde-Sieira, M., & Soengas, J. L. (2017). Nutrient sensing systems in fish: Impact on food intake regulation and energy homeostasis. Frontiers in Neuroscience, 2017, 10.

Coop, R. L., & Holmes, P. H. (1996). Nutrition and parasite interaction. International Journal for Parasitology, 26, 951–962.

Deb, A. C. (2011). Fundamentals of biochemistry. New Central Book Agency Ltd., London.

Dogan, G. (2008). Protein metabolism in fishes. Journal of Fisheries, 2(1), 30–40.

Fernandes, T., & McMeans, B. C. (2019). Coping with the cold: Energy storage strategies for surviving winter in freshwater fish. Ecography, 42(12), 2037–2052.

Folch, J., Lees, M., & Stanley, G. H. S. (1957). A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry, 226(1), 497–509.

Gilannejad, N., Martínez-Rodríguez, G., Yúfera, M., & Moyano, F. J. (2018). Modelling digestive hydrolysis of nutrients in fish using factorial designs and desirability function. PLoS One, 13(11), e0206556.

Goolish, E. M. (1991). Aerobic and anaerobic scaling in fish. Biological Reviews, 66(1), 33–56.

He, A.-Y., Ning, L.-J., Chen, L.-Q., Chen, Y.-L., Xing, Q., Li, J.-M., Qiao, F., Li, D.-L., Zhang, M.-L.,& Du, Z.-Y. (2015). Systemic adaptation of lipid metabolism in response to low- and high-fat diet in Nile tilapia (Oreochromis niloticus). Physiological Reports, 3(8), e12485.

Hemre, G.-I., Mommsen, T. P., & Krogdahl, Å. (2002). Carbohydrates in fish nutrition: Effects on growth, glucose metabolism and hepatic enzymes. Aquaculture Nutrition, 8(3), 175–194.

Hrekh, V. I., Blaha, N. A., Dobryanska, H. M., Shemchuk, V. R., Kornyat, S. B., & Yanovich, V. G. (2001). Metabolizm [2-14C]lizynu, [2-14C]tsystynu i 3-fenil-[1-14C]alaninu u skeletnykh myazakh koropa v umovakh in vitro [Metabolism of [2-14C]lysine, [2-14C]cystine and 3-phenyl-[1-14C]alanine in carp skeletal muscle in vitro]. The Animal Biology, 3(1), 88–91 (in Ukrainian).

Hrytsyniak, I. I., Smolianinov, K. B., & Yanovich, V. G. (2010). Obmin lipidiv u ryb [Lipid metabolism in fish]. Triad Plus, Lviv (in Ukrainian).

Kates, M. (1975). Technika lipidologii. Vidilenie, analis i indentifikatsia lipidov [Technique of lipidology. Isolation, analysis and identification of lipids]. Peace, Moscow (in Russian).

Kaushik, S. J., & Seiliez, I. (2010). Protein and amino acid nutrition and metabolism in fish: Current knowledge and future needs. Aquaculture Research, 41(3), 322–332.

Kersten, S. (2001). Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Reports, 2(4), 282–286.

Kovalenko, J., Shlapak, O., Potrokhov, A., & Zin’kovskiy, O. (2019). Effect of antropogenic pollution on physiological and biochemical parameters of fish and composition of their parasitocenoses. Fisheries Science of Ukraine, 49, 72–88.

Kuchta, R., Choudhury, A., & Scholz, T. (2018). Asian fish tapeworm: The most successful invasive parasite in freshwaters. Trends in Parasitology, 34(6), 511–523.

Kuchta, R., Scholz, T., & Bray, R. A. (2008). Revision of the order Bothriocephalidea Kuchta, Scholz, Brabec & Bray, 2008 (Eucestoda) with amended generic diagnoses and keys to families and genera. Systematic Parasitology, 71(2), 81–136.

Kurovskaya, L., & Stril’ko, G. (2016). Effect of aquatic environment ph on the level of ectoparasite infestation, protein and lysozym content in some cyprinid species. Fisheries Science of Ukraine, 35, 88–101.

Li, P., Mai, K., Trushenski, J., & Wu, G. (2008). New developments in fish amino acid nutrition: Towards functional and environmentally oriented aquafeeds. Amino Acids, 37(1), 43–53.

Meyer-Burgdorff, K.-H., & Rosenow, H. (1995). Protein turnover and energy metabolism in growing carp. Journal of Animal Physiology and Animal Nutrition, 73, 113–122.

Nanware, S. S., Nazneen, U., Bhure, D. B., & Garad, V. B. (2012). Studies on protein content of cestode Cotugnia and its host Gallus gallus domesticus. Journal of Experimental Sciences, 3(1), 40–41.

National Research Council (NRC). (1993). Nutrient Requirements of Fish. National Academy Press, Washington.

Nelson, J. A. (2016). Oxygen consumption rate v. rate of energy utilization of fishes: A comparison and brief history of the two measurements. Journal of Fish Biology, 88(1), 10–25.

Pastorino, P., Bertoli, M., Kušće, M., Giulianini, P. G., Menconi, V., Prearo, M., & Pizzul, E. (2020). Liver lipid accumulation in European Bullhead (Cottus cobio) from a High-Mountain Lake: An adaptive strategy to survive the adverse winter season. Diversity, 12(12), 442.

Prohorova, M. I. (1982). Metody biohimicheskih issledovanij (lipidnyj i energeticheskij obmen) [Methods of biochemical research (lipid and energy metabolism)]. Leningrad University Press, Leningrad (in Russian).

Pylypets, A. Z., & Yanovich, V. G. (2000). Vykorystannia [6-14C]hliukozy, [1-14C]palmitynovoi kysloty i [2-14C]lizynu v enerhetychnykh protsesakh u skeletnykh miazakh koropa riznoho viku v umovakh in vitro [Use of [6-14C]glucose, [1-14C]palmitic acid and [2-14C]lysine in energy processes in skeletal muscles of carp of different ages in vitro]. Scientific and Technical Bulletin of the Institute of Animal Biology Lviv, 2, 79–81 (in Ukrainian).

Řehulka, J., & Minařík, B. (2007). Blood parameters in brook trout Salvelinus fontinalis (Mitchill, 1815), affected by columnaris disease. Aquaculture Research, 38(11), 1182–1197.

Rehulka, J., Minarik, B., Adamec, V., & Rehulkova, E. (2005). Investigations of physiological and pathological levels of total plasma protein in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture Research, 36(1), 22–32.

Romano, N., Kumar, V., Yang, G., Kajbaf, K., Rubio, M. B., Overturf, K., Brezas, A., & Hardy, R. (2020). Bile acid metabolism in fish: Disturbances caused by fishmeal alternatives and some mitigating effects from dietary bile inclusions. Reviews in Aquaculture, 12(3), 1792–1817.

Rui, L. (2014). Energy metabolism in the liver. Comprehensive Physiology, 4, 177–197.

Scholz, T., Kuchta, R., & Williams, C. (2012). Bothriocephalus acheilognathi. In: Patrick, T. K. W., & Buchmann, K. (Eds.). Fish Parasites: Pathobiology and Protection. CABI Publishing. Pp. 282–297.

Schutz, Y. (2011). Protein turnover, ureagenesis and gluconeogenesis. International Journal for Vitamin and Nutrition Research, 81(23), 101–107.

Sébert, P., Mortelette, H., Nicolas, J., Amérand, A., Belhomme, M., & Moisan, C. (2011). In vitro aerobic and anaerobic muscle capacities in the European eel, Anguilla anguilla: Effects of a swimming session. Respiratory Physiology and Neurobiology, 176(3), 118–122.

Seibel, B. A., & Drazen, J. C. (2007). The rate of metabolism in marine animals: Environmental constraints, ecological demands and energetic opportunities. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1487), 2061–2078.

Sheridan, M. A. (1988). Lipid dynamics in fish: Aspects of absorption, transportation, deposition and mobilization. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 90(4), 679–690.

Shimeno, S., Kheyyali, D., & Takeda, M. (1990). Metabolic adaptation to prolonged starvation of carp. Nippon Suisan Gakkaishi, 56(1), 35–41.

Stahl, E. (1965). Chromatografia v tonkih sloyah [Chromatography in thin layers]. Peace, Moscow (in Russian).

Storch, D., & Pörtner, H. O. (2003). The protein synthesis machinery operates at the same expense in eurythermal and cold stenothermal pectinids. Physiological and Biochemical Zoology, 76(1), 28–40.

Tao, Y.-F., Qiang, J., Bao, J.-W., Chen, D.-J., Yin, G.-J., Xu, P., & Zhu, H.-J. (2018). Changes in physiological parameters, lipid metabolism, and expression of microRNAs in genetically improved farmed tilapia (Oreochromis niloticus) with fatty liver induced by a high-fat diet. Frontiers in Physiology, 9, 1521.

Tocher, D. R. (2010). Fatty acid requirements in ontogeny of marine and freshwater fish. Aquaculture Research, 41(5), 717–732.

Tocher, D. R., & Glencross, B. D. (2015). Lipids and fatty acids. In: Lee, C.-S., Lim, C., Gatlin, D. M., & Webster, C. D. (Eds.). Dietary nutrients, additives, and fish health. Wiley-Blackwell, Canada. Pp. 47–94.

Tocher, D. R., & Sargent, J. R. (1990). Incorporation into phospholipid classes and metabolism via desaturation and elongation of various 14C-labelled (n-3) and (n-6) polyunsaturated fatty acids in trout astrocytes in primary culture. Journal of Neurochemistry, 54(6), 2118–2124.

Tok, N. C., Jain, K. K., Prabu, D. L., Sahu, N. P., Munilkumar, S., Pal, A. K., Siddiah, G. M., & Kumar, P. (2016). Metabolic and digestive enzyme activity of Pangasianodon hypophthalmus (Sauvage, 1878) fingerlings in response to alternate feeding of different protein levels in the diet. Aquaculture Research, 48(6), 2895–2911.

Vargas-Chacoff, L., Muñoz, J. L. P., Hawes, C., Oyarzún, R., Pontigo, J. P., Saravia, J., González, M. P., Morera, F. J., Labbé, B. S., Bertrán, C., Mardones, O., Pino, J., & Wadsworth, S. (2016). Atlantic salmon (Salmo salar) and Coho salmon (Oncorhynchus kisutch) display differential metabolic changes in response to infestation by the ectoparasite Caligus rogercresseyi. Aquaculture, 464, 469–479.

Vlizlo, V. V., Fedoruk, R. S., & Ratych, I. B. (2012). Laboratorni metody doslidzhen’ u biolohiji, tvarynnytstvi ta veterynarnij medytsyni [Laboratory methods in biology, animal husbandry and veterinary medicine]. Spolom, Lviv (in Ukrainian).

Wang, J., Liang, X.-F., He, S., Li, J., Huang, K., Zhang, Y.-P., & Huang, D. (2018). Lipid deposition pattern and adaptive strategy in response to dietary fat in Chinese perch (Siniperca chuatsi). Nutrition and Metabolism, 15, 77.

Yuskiv, I. D. (2006). Morfometrychni ta fiziolohichni pokaznyky rostu koropa pry вotriotsefalozniy invazii [Morphometric and physiological indicators of carp growth during Вotrіocephalus invasion]. Scientific Bulletin of the Lviv National Academy of Veterinary Medicine S. Z. Gzhytskyi, Lviv, 8(2), 224–229 (in Ukrainian).

Yuskiv, L. L., & Yuskiv, I. D. (2020). The lipid metabolism in carp during invasion by the tapeworn Bothriocephalus acheilognathi. Regulatory Mechanisms in Biosystems, 11(2), 214–219.

Published
2021-03-11
How to Cite
Yuskiv, L. L., & Yuskiv, I. D. (2021). The synthesis of lipids and proteins in vitro in tissues of Cyprinus carpio infected with Bothriocephalus acheilognathi . Regulatory Mechanisms in Biosystems, 12(1), 78-85. https://doi.org/10.15421/022112