Regarding the sperm of cold-water fish, the contributions of different bioenergetic pathways, including mitochondrial respiration, to energy production at the spawning temperature and its adaptation at the maximum critical temperature (CTmax) are unclear. The roles of glycolysis, fatty acid oxidation, oxidative phosphorylation (OXPHOS) at 4 °C, and OXPHOS at 15 °C for energy production in burbot (Lota lota) spermatozoa were studied by motility and the oxygen consumption rate (OCR) (with and without pathway inhibitors and the OXPHOS uncoupler). At both temperatures, the effects of the inhibitors and the uncoupler on the motility duration, curvilinear velocity, and track linearity were insignificant; in addition, the OCRs in activation and non-activation media differed insignificantly and were not enhanced after uncoupler treatment. After inhibitor treatment in both media, OXPHOS was insignificantly different at the 2, 30, and 60 s time points at 4 °C but was reduced significantly at the 30 and 60 s time points after treatment with sodium azide at 15 °C. In conclusion, for burbot sperm at both the spawning temperature and the CTmax, the energy synthesized via OXPHOS during motility was insufficient. Therefore, the majority of the energy required to sustain motility was derived from pre-accumulated energy produced and stored during the quiescent state of the spermatozoa.

South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Faculty of Fisheries and Protection of Waters Research Institute of Fish Culture and Hydrobiology University of South Bohemia in Ceske Budejovice Zátiší 728 2 389 25 Vodňany Czech Republic

Zobrazit více v PubMed

McPhail J.D., Paragamian V.L. Burbot biology and life history. In: Paragamian V.L., Willis D.W., editors. Burbot: Biology, Ecology and Management. Volume 128. Fisheries Management Section of the American Fisheries Society; New York, NY, USA: 2000. pp. 11–23.

Harrison P.M., Gutowsky L.F., Martins E.G., Patterson D.A., Cooke S.J., Power M. Temporal plasticity in thermal-habitat selection of burbot Lota lota a diel-migrating winter-specialist. J. Fish Biol. 2016;88:2111–2129. doi: 10.1111/jfb.12990. PubMed DOI

Lahnsteiner F., Mansour N. The effect of temperature on sperm motility and enzymatic activity in brown trout Salmo trutta, burbot Lota lota and grayling Thymallus thymallus. J. Fish Biol. 2012;81:197–209. doi: 10.1111/j.1095-8649.2012.03323.x. PubMed DOI

Dos Santos R.S., Galina A., Da-Silva W.S. Cold acclimation increases mitochondrial oxidative capacity without inducing mitochondrial uncoupling in goldfish white skeletal muscle. Biol. Open. 2013;2:82–87. doi: 10.1242/bio.20122295. PubMed DOI PMC

Egginton S., Sidell B.D. Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am. J. Physiol. 1989;256:R1–R9. doi: 10.1152/ajpregu.1989.256.1.R1. PubMed DOI

Lucassen M., Koschnick N., Eckerle L.G., Portner H.O. Mitochondrial mechanisms of cold adaptation in cod (Gadus morhua L.) populations from different climatic zones. J. Exp. Biol. 2006;209:2462–2471. doi: 10.1242/jeb.02268. PubMed DOI

Guderley H. Metabolic responses to low temperature in fish muscle. Biol. Rev. Camb. Philos. Soc. 2004;79:409–427. doi: 10.1017/S1464793103006328. PubMed DOI

Ingermann R. Fish Spermatology. Alpha Science International Ltda; Oxford, UK: 2008. Energy metabolism and respiration in fish spermatozoa.

Boryshpolets S., Dzyuba B., Drokin S. Pre-spawning water temperature affects sperm respiration and reactivation parameters in male carps. Fish. Physiol. Biochem. 2009;35:661–668. doi: 10.1007/s10695-008-9292-4. PubMed DOI

Rahi D., Dzyuba B., Xin M., Cheng Y., Dzyuba V. Energy pathways associated with sustained spermatozoon motility in the endangered Siberian sturgeon Acipenser Baerii. J. Fish Biol. 2020;97:435–443. doi: 10.1111/jfb.14382. PubMed DOI

Ingermann R.L., Robinson M.L., Cloud J.G. Respiration of steelhead trout sperm: Sensitivity to pH and carbon dioxide. J. Fish Biol. 2003;62:13–23. doi: 10.1046/j.1095-8649.2003.00003.x. DOI

Wick A.N., Drury D.R., Nakada H.I., Wolfe J.B. Localization of the primary metabolic block produced by 2-deoxyglucose. J. Biol. Chem. 1957;224:963–969. doi: 10.1016/S0021-9258(18)64988-9. PubMed DOI

Nelson D., Cox M. Lehninger Principles of Biochemistry. WH Freeman; New York, NY, USA: 2008.

Fei M.J., Yamashita E., Inoue N., Yao M., Yamaguchi H., Tsukihara T., Shinzawa-Itoh K., Nakashima R., Yoshikawa S. X-ray structure of azide-bound fully oxidized cytochrome c oxidase from bovine heart at 2.9 Å resolution. Acta Crystallogr. Sect. D Biol. Crystallogr. 2000;56:529–535. doi: 10.1107/S0907444900002213. PubMed DOI

Hanstein W.G. Uncoupling of oxidative phosphorylation. Trends Biochem. Sci. 1976;1:65–67. doi: 10.1016/S0968-0004(76)80194-6. DOI

Dadras H., Boryshpolets S., Golpour A., Policar T., Blecha M., Dzyuba B. Effects of temperature on sperm motility of burbot Lota lota: Spontaneous activation and calcium dependency. J. Fish Biol. 2019;95:1137–1144. doi: 10.1111/jfb.14110. PubMed DOI

Cheng Y., Vechtova P., Fussy Z., Sterba J., Linhartová Z., Rodina M., Tučková V., Gela D., Samarin A.M., Lebeda I., et al. Changes in Phenotypes and DNA Methylation of In Vitro Aging Sperm in Common Carp Cyprinus carpio. Int. J. Mol. Sci. 2021;22:5925. doi: 10.3390/ijms22115925. PubMed DOI PMC

Lusk S. Conservation of Endangered Freshwater Fish in Europe. Springer; Berlin/Heidelberg, Germany: 1996. The status of the fish fauna in the Czech Republic; pp. 89–98.

Stapanian M.A., Paragamian V.L., Madenjian C.P., Jackson J.R., Lappalainen J., Evenson M.J., Neufeld M.D. Worldwide status of burbot and conservation measures. Fish Fish. 2010;11:34–56. doi: 10.1111/j.1467-2979.2009.00340.x. DOI

Blecha M., Dzyuba B., Boryshpolets S., Horokhovatskyi Y., Dadras H., Malinovskyi O., Sampels S., Policar T. Spermatozoa quality and sperm lipid composition in intensively cultured and wild burbot (Lota lota) Anim. Reprod. Sci. 2018;198:129–136. doi: 10.1016/j.anireprosci.2018.09.011. PubMed DOI

Cott P.A. Ph.D. Thesis. Laurentian University; Sudbury, ON, Canada: 2013. Life History and Reproductive Ecology of a Mid-Winter Spawner: The Burbot (Lota lota)

Dadras H., Golpour A., Dzyuba B., Kristan J., Policar T. Ultrastructural feature of spermatogenic cells and spermatozoon in cultured burbot Lota lota. Tissue Cell. 2019;61:1–7. doi: 10.1016/j.tice.2019.08.005. PubMed DOI

Lahnsteiner F., Berger B., Weismann T., Patzner R. Sperm motility and seminal fluid composition in the burbot, Lota lota. J. Appl. Ichthyol. 1997;13:113–119. doi: 10.1111/j.1439-0426.1997.tb00110.x. DOI

Żarski D., Kucharczyk D., Sasinowski W., Targońska K., Mamcarz A. The influence of temperature on successful reproductions of Burbot, Lota lota (L.) under hatchery conditions. Pol. J. Nat. Sci. 2010;25:93–105. doi: 10.2478/v10020-010-0007-9. DOI

Turner E., Montgomerie R. Ovarian fluid enhances sperm movement in Arctic charr. J. Fish Biol. 2002;60:1570–1579. doi: 10.1111/j.1095-8649.2002.tb02449.x. DOI

Blecha M., Kristan J., Samarin A.M., Rodina M., Policar T. Quality and quantity of pikeperch (Sander lucioperca) spermatozoa after varying cold water treatments. J. Appl. Ichthyol. 2015;31:75–78. doi: 10.1111/jai.12853. DOI

Nynca J., Dietrich G.J., Dobosz S., Grudniewska J., Ciereszko A. Effect of cryopreservation on sperm motility parameters and fertilizing ability of brown trout semen. Aquaculture. 2014;433:62–65. doi: 10.1016/j.aquaculture.2014.05.037. DOI

Nynca J., Judycka S., Liszewska E., Dobosz S., Grudniewska J., Arai K., Fujimoto T., Ciereszko A. Utility of different sugar extenders for cryopreservation and post-thaw storage of sperm from Salmonidae species. Aquaculture. 2016;464:340–348. doi: 10.1016/j.aquaculture.2016.07.014. DOI

Ruiz-Pesini E., Díez-Sánchez C., López-Pérez M.J., Enríquez J.A. The role of the mitochondrion in sperm function: Is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr. Top. Dev. Biol. 2007;77:3–19. PubMed

Storey B.T. Mammalian sperm metabolism: Oxygen and sugar, friend and foe. Int J. Dev. Biol. 2008;52:427–437. doi: 10.1387/ijdb.072522bs. PubMed DOI

Dreanno C., Cosson J., Suquet M., Seguin F., Dorange G., Billard R. Nucleotide content, oxidative phosphorylation, morphology, and fertilizing capacity of turbot (Psetta maxima) spermatozoa during the motility period. Mol. Reprod. Dev. 1999;53:230–243. doi: 10.1002/(SICI)1098-2795(199906)53:2<230::AID-MRD12>3.0.CO;2-H. PubMed DOI

Ingermann R.L., Schultz C.L., Kanuga M.K., Wilson-Leedy J.G. Metabolism of motile zebrafish sperm. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2011;158:461–467. doi: 10.1016/j.cbpa.2010.12.008. PubMed DOI

Perchec G., Jeulin C., Cosson J., Andre F., Billard R. Relationship between sperm ATP content and motility of carp spermatozoa. J. Cell Sci. 1995;108:747–753. doi: 10.1242/jcs.108.2.747. PubMed DOI

Bencic D., Krisfalusi M., Cloud J., Ingermann R. Maintenance of steelhead trout (Oncorhynchus mykiss) sperm at different in vitro oxygen tensions alters ATP levels and cell functional characteristics. Fish. Physiol. Biochem. 1999;21:193–200. doi: 10.1023/A:1007880426488. DOI

Lahnsteiner F., Berger B., Weismann T. Sperm metabolism of the telost fishes Chalcalburnus chalcoides and Oncorhynchus mykiss and its relation to motility and viability. J. Exp. Zool. 1999;284:454–465. doi: 10.1002/(SICI)1097-010X(19990901)284:4<454::AID-JEZ12>3.0.CO;2-O. PubMed DOI

Mansour N., Lahnsteiner F., Berger B. Metabolism of intratesticular spermatozoa of a tropical teleost fish (Clarias gariepinus) Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2003;135:285–296. doi: 10.1016/S1096-4959(03)00083-6. PubMed DOI

Mukai C., Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol. Reprod. 2004;71:540–547. doi: 10.1095/biolreprod.103.026054. PubMed DOI

Nesci S., Spinaci M., Galeati G., Nerozzi C., Pagliarani A., Algieri C., Tamanini C., Bucci D. Sperm function and mitochondrial activity: An insight on boar sperm metabolism. Theriogenology. 2020;144:82–88. doi: 10.1016/j.theriogenology.2020.01.004. PubMed DOI

Lahnsteiner F., Patzner R.A., Weismann T. Energy resources of spermatozoa of the rainbow trout Oncorhynchus mykiss (Pisces, Teleostei) Reprod. Nutr. Dev. 1993;33:349–360. doi: 10.1051/rnd:19930404. PubMed DOI

Lahnsteiner F., Berger B., Weismann T., Patzner R.A. Motility of spermatozoa of Alburnus alburnus (Cyprinidae) and its relationship to seminal plasma composition and sperm metabolism. Fish Physiol. Biochem. 1996;15:167–179. doi: 10.1007/BF01875596. PubMed DOI

Lahnsteiner F., Patzner R., Weismann T. Monosaccharides as energy resources during motility of spermatozoa in Leuciscus cephalus (Cyprinidae, Teleostei) Fish Physiol. Biochem. 1992;10:283–289. doi: 10.1007/BF00004477. PubMed DOI

Dzyuba B., Bondarenko O., Fedorov P., Gazo I., Prokopchuk G., Cosson J. Energetics of fish spermatozoa: The proven and the possible. Aquaculture. 2017;472:60–72. doi: 10.1016/j.aquaculture.2016.05.038. DOI

Pizzino G., Irrera N., Cucinotta M., Pallio G., Mannino F., Arcoraci V., Squadrito F., Altavilla D., Bitto A. Oxidative stress: Harms and benefits for human health. Oxidative Med. Cell. Longev. 2017:8416763. doi: 10.1155/2017/8416763. PubMed DOI PMC

Simčič T., Jesenšek D., Brancelj A. Effects of increased temperature on metabolic activity and oxidative stress in the first life stages of marble trout (Salmo marmoratus) Fish Physiol. Biochem. 2015;41:1005–1014. doi: 10.1007/s10695-015-0065-6. PubMed DOI

Ashton I. Safety and Quality Issues in Fish Processing. Elsevier; CRC Press; Washington, DC, USA: 2002. Understanding lipid oxidation in fish; p. 507.

Patterson E., Wall R., Fitzgerald G., Ross R., Stanton C. Health implications of high dietary omega-6 polyunsaturated fatty acids. J. Nutr. Metab. 2012:539426. doi: 10.1155/2012/539426. PubMed DOI PMC

Korpela R., Seppo L., Laakso J., Lilja J., Karjala K., Lähteenmäki T., Solatunturi E., Vapaatalo H., Tikkanen M.J. Dietary habits affect the susceptibility of low-density lipoprotein to oxidation. Eur. J. Clin. Nutr. 1999;53:802–807. doi: 10.1038/sj.ejcn.1600860. PubMed DOI

Dadras H., Dzyuba B., Cosson J., Golpour A., Siddique M.A.M., Linhart O. Effect of water temperature on the physiology of fish spermatozoon function: A brief review. Aquac. Res. 2017;48:729–740. doi: 10.1111/are.13049. DOI

Lahnsteiner F. Spermatozoa of the teleost fish Perca fluviatilis (perch) have the ability to swim for more than two hours in saline solutions. Aquaculture. 2011;314:221–224. doi: 10.1016/j.aquaculture.2011.02.024. DOI

Vladiĉ T., Jätrvi T. Sperm motility and fertilization time span in Atlantic salmon and brown trout—The effect of water temperature. J. Fish Biol. 1997;50:1088–1093.

Alavi S.M., Cosson J. Sperm motility in fishes. I. Effects of temperature and pH: A review. Cell Biol. Int. 2005;29:101–110. doi: 10.1016/j.cellbi.2004.11.021. PubMed DOI

Figueroa E., Lee-Estevez M., Valdebenito I., Watanabe I., Oliveira R.P.S., Romero J., Castillo R.L., Farías J.G. Effects of cryopreservation on mitochondrial function and sperm quality in fish. Aquaculture. 2019;511 doi: 10.1016/j.aquaculture.2019.06.004. DOI

Diepart C., Verrax J., Calderon P.B., Feron O., Jordan B.F., Gallez B. Comparison of methods for measuring oxygen consumption in tumor cells in vitro. Anal. Biochem. 2010;396:250–256. doi: 10.1016/j.ab.2009.09.029. PubMed DOI

Magdanz V., Boryshpolets S., Ridzewski C., Eckel B., Reinhardt K. The motility-based swim-up technique separates bull sperm based on differences in metabolic rates and tail length. PLoS ONE. 2019;14:e0223576. doi: 10.1371/journal.pone.0223576. PubMed DOI PMC

Saito T., Wu C.C., Shiku H., Yasukawa T., Yokoo M., Ito-Sasaki T., Abe H., Hoshi H., Matsue T. Oxygen consumption of cell suspension in a poly(dimethylsiloxane) (PDMS) microchannel estimated by scanning electrochemical microscopy. Analyst. 2006;131:1006–1011. doi: 10.1039/b600080k. PubMed DOI

Strovas T.J., McQuaide S.C., Anderson J.B., Nandakumar V., Kalyuzhnaya M.G., Burgess L.W., Holl M.R., Meldrum D.R., Lidstrom M.E. Direct measurement of oxygen consumption rates from attached and unattached cells in a reversibly sealed, diffusionally isolated sample chamber. Adv. Biosci. Biotechnol. 2010;5:398–408. doi: 10.4236/abb.2010.15053. PubMed DOI PMC

Christen R., Gatti J.L., Billard R. Trout sperm motility. The transient movement of trout sperm is related to changes in the concentration of ATP following the activation of the flagellar movement. Eur. J. Biochem. 1987;166:667–671. doi: 10.1111/j.1432-1033.1987.tb13565.x. PubMed DOI

Billard R., Cosson J., Fierville F., Brun R., Rouault T., Williot P. Motility analysis and energetics of the Siberian sturgeon Acipenser baerii spermatozoa. J. Appl. Ichthyol. 1999;15:199–203. doi: 10.1111/j.1439-0426.1999.tb00234.x. DOI

Inoda T., Ohtake H., Morisawa M. Activation of respiration and initiation of motility in rainbow trout spermatozoa. Zool. Sci. 1988;5:939–945.

Terner C., Korsh G. The Oxidative Metabolism of Pyruvate, Acetate and Glucose in Isolated Fish Spermatozoa. J. Cell. Comp. Physiol. 1963;62:243–249. doi: 10.1002/jcp.1030620303. PubMed DOI

Lahnsteiner F., Caberlotto S. Motility of gilthead seabream Sparus aurata spermatozoa and its relation to temperature, energy metabolism and oxidative stress. Aquaculture. 2012;370–371:76–83. doi: 10.1016/j.aquaculture.2012.09.034. DOI

Lahnsteiner F., Berger B., Weismann T., Patzner R. Determination of semen quality of the rainbow trout, Oncorhynchus mykiss, by sperm motility, seminal plasma parameters, and spermatozoal metabolism. Aquaculture. 1998;163:163–181. doi: 10.1016/S0044-8486(98)00243-9. DOI

Lahnsteiner F., Mansour N., McNiven M.A., Richardson G.F. Fatty acids of rainbow trout (Oncorhynchus mykiss) semen: Composition and effects on sperm functionality. Aquaculture. 2009;298:118–124. doi: 10.1016/j.aquaculture.2009.08.034. DOI

Tocher D.R. Metabolism and functions of lipids and fatty acids in teleost fish. Rev. Fish. Sci. 2003;11:107–184. doi: 10.1080/713610925. DOI

Figueroa E., Valdebenito I., Zepeda A.B., Figueroa C.A., Dumorné K., Castillo R.L., Farias J.G. Effects of cryopreservation on mitochondria of fish spermatozoa. Rev. Aquac. 2017;9:76–87. doi: 10.1111/raq.12105. DOI

Psenicka M., Alavi S.M., Rodina M., Gela D., Nebesarova J., Linhart O. Morphology and ultrastructure of Siberian sturgeon (Acipenser baerii) spermatozoa using scanning and transmission electron microscopy. Biol. Cell. 2007;99:103–115. doi: 10.1042/BC20060060. PubMed DOI

Benito S., Sánchez A., Unceta N., Andrade F., Aldámiz-Echevarria L., Goicolea M.A., Barrio R.J. LC-QTOF-MS-based targeted metabolomics of arginine-creatine metabolic pathway-related compounds in plasma: Application to identify potential biomarkers in pediatric chronic kidney disease. Anal. Bioanal. Chem. 2016;408:747–760. doi: 10.1007/s00216-015-9153-9. PubMed DOI

Brosnan M.E., Brosnan J.T. Renal arginine metabolism. J. Nutr. 2004;134:2791S–2795S. doi: 10.1093/jn/134.10.2791S. PubMed DOI

Simopoulos A.P. An increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity. Nutrients. 2016;8:128. doi: 10.3390/nu8030128. PubMed DOI PMC

Kiessling K.-H., Kiessling A. Selective utilization of fatty acids in rainbow trout (Oncorhynchus mykiss Walbaum) red muscle mitochondria. Can. J. Zool. 1993;71:248–251. doi: 10.1139/z93-035. DOI

Bureau B., Kaushik S., Cho C. Bioenergetics. In: Halver J.E., Hardy R.W., editors. Fish Nutrition. Elsevier; Amsterdam, The Netherlands: 2003. pp. 1–59.

Gambino R., Piscitelli J., Ackattupathil T.A., Theriault J.L., Andrin R.D., Sanfilippo M.L., Etienne M. Acidification of blood is superior to sodium fluoride alone as an inhibitor of glycolysis. Clin. Chem. 2009;55:1019–1021. doi: 10.1373/clinchem.2008.121707. PubMed DOI

Gambino R. Sodium fluoride: An ineffective inhibitor of glycolysis. Ann. Clin. Biochem. 2013;50:3–5. doi: 10.1258/acb.2012.012135. PubMed DOI

Sun Z., Zhang W., Xue X., Zhang Y., Niu R., Li X., Li B., Wang X., Wang J. Fluoride decreased the sperm ATP of mice through inhabiting mitochondrial respiration. Chemosphere. 2016;144:1012–1017. doi: 10.1016/j.chemosphere.2015.09.061. PubMed DOI

Waring W., Evans L., Kirkpatrick C. Glycolysis inhibitors negatively bias blood glucose measurements: Potential impact on the reported prevalence of diabetes mellitus. J. Clin. Pathol. 2007;60:820–923. doi: 10.1136/jcp.2006.039925. PubMed DOI PMC

Evaluation of carp sperm respiration: fluorometry with optochemical oxygen sensor versus polarography