Abstract
Low temperature frequently influences growth, development, and even survival of aquatic animals. In the present study, physiological and molecular responses to low temperature in Litopenaeus vannamei were investigated. The cDNA sequences of two oxygen-carrying proteins, cytoglobin (Cygb) and neuroglobin (Ngb), were isolated. Protein structure analysis revealed that both proteins share a globin superfamily domain. Real-time PCR analysis indicated that Cygb and Ngb mRNA levels gradually increased during decrease in temperatures from 25 to 15°C and then decreased at 10°C in muscle, brain, stomach, and heart, except for a continuing increase in gills, whereas they showed a different expression trend in the hepatopancreas. Hemocyanin concentration gradually reduced as the temperature decreased. Moreover, the activities of respiratory metabolic enzymes including lactate dehydrogenase (LDH) and succinate dehydrogenase (SDH) were measured, and it was found that LDH activity gradually increased while SDH activity decreased after low-temperature treatment. Finally, damage to gill structure at low temperature was also observed, and this intensified with further decrease in temperature. Taken together, these results show that low temperature has an adverse influence in L. vannamei, which contributes to systematic understanding of the adaptation mechanisms of shrimp at low temperature.
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Abbreviations
- Cygb:
-
cytoglobin
- Hb:
-
hemoglobin
- LDH:
-
lactate dehydrogenase
- Mb:
-
myoglobin
- Ngb:
-
neuroglobin
- ROS:
-
reactive oxygen species
- SDH:
-
succinate dehydrogenase
References
Weber, R. E., and Vinogradov, S. N. (2001) Nonvertebrate hemoglobins: functions and molecular adaptations, Physiol. Rev., 81, 569–628.
Brunori, M. (2001) Nitric oxide, cytochrome c oxidase and myoglobin, Trends Biochem. Sci., 26, 21–23.
Bunn, H. F. (1981) Evolution of mammalian hemoglobin function, Blood, 58, 189–197.
Decker, H., and Jaenicke, E. (2004) Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins, Dev. Comp. Immunol., 28, 673–687.
Pick, C., Hagner-Holler, S., and Burmester, T. (2008) Molecular characterization of hemocyanin and hexamerin from the firebrat Thermobia domestica (Zygentoma), Insect Biochem. Molec., 38, 977–983.
Pan, J. Y., Zhang, Y. L., Wang, S. Y., and Peng, X. X. (2008) Dodecamer is required for agglutination of Litopenaeus vannamei hemocyanin with bacterial cells and red blood cells, Mar. Biotechnol., 10, 645–652.
Glazer, L., Tom, M., Weil, S., Roth, Z., Khalaila, I., Mittelman, B., and Sagi, A. (2013) Hemocyanin with phe-noloxidase activity in the chitin matrix of the crayfish gastrolith, J. Exp. Biol., 216, 1898–1904.
Jaenicke, E., Föll, R., and Decker, H. (1999) Spider hemocyanin binds ecdysone and 20-OH-ecdysone, J. Biol. Chem., 274, 34267–34271.
Paul, R., and Pirow, R. (1998) The physiological significance of respiratory proteins in invertebrates, Zoology, 100, 298–306.
Zielinski, S., Sartoris, F. J., and Pörtner, H. O. (2001) Temperature effects on hemocyanin oxygen binding in an Antarctic cephalopod, Biol. Bull., 200, 67–76.
Fan, L., Wang, A., and Wu, Y. (2013) Comparative proteomic identification of the hemocyte response to cold stress in white shrimp, Litopenaeus vannamei, J. Proteomics, 80, 196–206.
Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Gough, J., Dewilde, S., Moens, L., and Vanfleteren, J. R. (2006) A phylogenomic profile of globins, BMC Evol. Biol., 6,31.
Bjørlykke, G. A., Kvamme, B. O., Slinde, E., and Raae, A. J. (2012) Cloning, expression and purification of Atlantic salmon (Salmo salar L.) neuroglobin, Protein Expres. Purif., 86, 151–156.
Zhu, Y., Sun, Y., Jin, K., and Greenberg, D. A. (2002) Hemin induces neuroglobin expression in neural cells, Blood, 100, 2494–2498.
Burmester, T., and Hankeln, T. (2004) Neuroglobin: a respiratory protein of the nervous system, Physiology, 19, 110–113.
Pesce, A., Bolognesi, M., Bocedi, A., Ascenzi, P., Dewilde, S., Moens, L., and Burmester, T. (2002) Neuroglobin and cytoglobin, EMBO Rep., 3, 1146–1151.
Fordel, E., Geuens, E., Dewilde, S., Rottiers, P., Carmeliet, P., Grooten, J., and Moens, L. (2004) Cytoglobin expression is upregulated in all tissues upon hypoxia: an in vitro and in vivo study by quantitative real-time PCR, Biochem. Biophys. Res. Commun., 319, 342–348.
Sanctis, D., Dewilde, S., Pesce, A., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., and Bolognesi, M. (2004) Crystal structure of cytoglobin: the fourth globin type discovered in man displays heme hexa-coordination, J. Mol. Biol., 336, 917–927.
Schmidt, M., Gerlach, F., Avivi, A., Laufs, T., Wystub, S., Simpson, J. C., Nevo, E., Saaler-Reinhardt, S., Reuss, S., and Burmester, T. (2004) Cytoglobin is a respiratory protein in connective tissue and neurons, which is up-regulated by hypoxia, J. Biol. Chem., 279, 8063–8069.
Hankeln, T., Ebner, B., Fuchs, C., Gerlach, F., Haberkamp, M., Laufs, T. L., Roesner, A., Schmidt, M., Weich, B., and Wystub, S. (2005) Neuroglobin and cytoglobin in search of their role in the vertebrate globin family, J. Inorg. Biochem., 99, 110–119.
Fago, A., Hundahl, C., Dewilde, S., Gilany, K., Moens, L., and Weber, R. E. (2004) Allosteric regulation and temperature dependence of oxygen binding in human neuroglobin and cytoglobin–molecular mechanisms and physiological significance, J. Biol. Chem., 279, 44417–44426.
Menz, A., and Bowers, A. B. (1980) Bionomics of Penaeus vannamei Boone and Penaeus stylirostris Stimpson in a lagoon on the Mexican Pacific Coast, Estuar. Coast. Shelf, 10, 685–697.
FAO Year Book: Fishery and Aquaculture Statistics (2016) FAO, Rome.
He, J., Xiu, M., Tang, X., Yue, F., Wang, N., Yang, S., and Chen, Q. (2013) The different mechanisms of hypoxic acclimatization and adaptation in lizard Phrynocephalus vlangalii living on Qinghai-Tibet plateau, J. Exp. Zool. Part A, 319, 117–123.
Qiu, J., Wang, W. N., Wang, L. J., Liu, Y. F., and Wang, A. L. (2011) Oxidative stress, DNA damage and osmolality in the Pacific white shrimp Litopenaeus vannamei exposed to acute low temperature stress, Comp. Biochem. Phys. C, 154, 36–41.
Wyban, J., Walsh, W. A., and Godin, D. M. (1995) Temperature effects on growth, feeding rate and feed conversion of the Pacific white shrimp (Penaeus vannamei), Aquaculture, 138, 267–279.
Villarreal, H., and Ocampo, L. (1993) Effect of size and temperature on the oxygen consumption of the brown shrimp Penaeus californiensis (Holmes, 1900), Comp. Biochem. Phys. A, 106, 97–101.
Paz, P. E., Roy, L. A., Davis, D. A., and Quintero, H. E. (2011) Survival of postlarval Litopenaeus vannamei following acclimation to low salinity waters at different temperatures, J. World Aquacult. Soc., 42, 575–579.
Chen, N., Wang, W. M., and Wang, H. L. (2016) An efficient full-length cDNA amplification strategy based on bioinformatics technology and multiplexed PCR methods, Sci. Rep., 5, 19420.
Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method, Methods, 25, 402–408.
Nickerson, K. W., and VanHolde, K. E. (1971) A comparison of molluscan and arthropod hemocyanin. I. Circular dichroism and absorption spectra, Comp. Biochem. Phys. B, 39, 855–872.
An, M. I., and Choi, C. Y. (2010) Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters, Comp. Biochem. Phys. B, 155, 34–42.
Lushchak, V. I., and Bagnyukova, T. V. (2006) Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes, Comp. Biochem. Phys. C, 143, 36–41.
Evans, D. H., Piermarini, P. M., and Choe, K. P. (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste, Physiol. Rev., 85, 97–177.
Salazar-Lugo, R., Mata, C., Oliveros, A., Rojas, L. M., Lemus, M., and Rojas-Villarroel, E. (2011) Histopathological changes in gill, liver and kidney of neotropical fish Colossoma macropomum exposed to paraquat at different temperatures, Environ. Toxicol. Phar., 31, 490–495.
Chen, J. C., Cheng, S. Y., and Chen, C. T. (1994) Changes of haemocyanin, protein and free amino acid levels in the haemolymph of Penaeus japonicus exposed to ambient ammonia, Comp. Biochem. Phys. A, 109, 339–347.
Rutter, J., Winge, D. R., and Schiffman, J. D. (2010) Succinate dehydrogenase assembly, regulation and role in human disease, Mitochondrion, 10, 393–401.
Simon, L. M., and Robin, E. D. (1971) Relationship of cytochrome oxidase activity to vertebrate total and organ oxygen consumption, Int. J. Biochem. Cell B, 2, 569–573.
Viru, M. (1994) Differences in effects of various training regimens on metabolism of skeletal muscles, J. Sports Med. Phys. Fit., 34, 217–227.
Hicks, J. W., and Wang, T. (2004) Hypometabolism in reptiles: behavioural and physiological mechanisms that reduce aerobic demands, Resp. Physiol. Neurobiol., 141, 261–271.
Punkt, K., Adams, V., Linke, A., and Welt, K. (1997) The correlation of cytophotometrically and biochemically measured enzyme activities: changes in the myocardium of diabetic and hypoxic diabetic rats, with and without Ginkgo biloba extract treatment, Acta Histochem., 99, 291–299.
Coates, C. J., Bradford, E. L., Krome, C. A., and Nairn, J. (2012) Effect of temperature on biochemical and cellular properties of captive Limulus polyphemus, Aquaculture, 334, 30–38.
Coates, C. J., and Nairn, J. (2014) Diverse immune functions of hemocyanins, Dev. Comp. Immunol., 45, 43–55.
Sugimoto, H., Makino, M., Sawai, H., Kawada, N., Yoshizato, K., and Shiro, Y. (2004) Structural basis of human cytoglobin for ligand binding, J. Mol. Biol., 339, 873–885.
Kugelstadt, D., Haberkam, M., Hankeln, T., and Burmester, T. (2004) Neuroglobin, cytoglobin, and a novel, eye-specific globin from chicken, Biochem. Biophys. Res. Commun., 325, 719–725.
Garry, D. J., Kanatous, S. B., and Mammen, P. P. (2003) Emerging roles for myoglobin in the heart, Trends Cardiovasc. Med., 13, 111–116.
Fang, J., Ma, I., and Allalunis-Turner, J. (2011) Knockdown of cytoglobin expression sensitizes human glioma cells to radiation and oxidative stress, Radiat. Res., 176, 198–207.
Fordel, E., Thijs, L., Martinet, W., Lenjou, M., Laufs, T., VanBockstaele, D., Moens, L., and Dewilde, S. (2006) Neuroglobin and cytoglobin overexpression protects human SH-SY5Y neuroblastoma cells against oxidative stress-induced cell death, Neurosci. Lett., 410, 146–151.
Guo, X., Philipsen, S., and Tan-Un, K. C. (2007) Study of the hypoxia-dependent regulation of human Cygb gene, Biochem. Biophys. Res. Commun., 364, 145–150.
Tiedke, J., Cubuk, C., and Burmester, T. (2013) Environmental acidification triggers oxidative stress and enhances globin expression in zebrafish gills, Biochem. Biophys. Res. Commun., 441, 624–629.
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Published in Russian in Biokhimiya, 2017, Vol. 82, No. 7, pp. 1097–1106.
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Wu, M., Chen, N., Huang, CX. et al. Effect of low temperature on globin expression, respiratory metabolic enzyme activities, and gill structure of Litopenaeus vannamei . Biochemistry Moscow 82, 844–851 (2017). https://doi.org/10.1134/S0006297917070100
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DOI: https://doi.org/10.1134/S0006297917070100