Fish Physiology and Biochemistry

, Volume 35, Issue 4, pp 607–614 | Cite as

Bioenergetics of fish spermatozoa during semen storage

  • M. S. Ziętara
  • A. Biegniewska
  • E. Rurangwa
  • J. Swierczynski
  • F. Ollevier
  • E. F. SkorkowskiEmail author


This mini-review focuses on changes in ATP and creatine phosphate concentrations in fish sperm under storage conditions. The storage of catfish sperm at 4°C leads to ATP depletion and decreased sperm motility. The rate of intracellular ATP depletion can be diminished through the addition of energetic substrates to the sperm storage medium, with lactate + pyruvate being the most efficient substrates for maintaining ATP concentrations in catfish sperm. The decrease in ATP concentration is closely associated with increases in AMP and hypoxanthine content. In contrast to catfish sperm, carp sperm is able to maintain intracellular ATP concentration close to the physiological level during storage. Collectively, these results suggest that fish species differ in terms of the energy metabolism of their spermatozoa and that the semen storage medium must be carefully selected for a particular fish species so as to maintain the ATP concentration and adenylate energy charge close to physiological values as long as possible.


Adenylate energy charge ATP Carp Catfish Creatine kinase Creatine phosphate Herring Spermatozoa 


  1. Atkinson DE (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7:4030–4034. doi: 10.1021/bi00851a033 CrossRefPubMedGoogle Scholar
  2. Atkinson DE (1977) Cellular energy metabolism and its regulation. Academic Press, New YorkGoogle Scholar
  3. Bencic DC, Krisfalusi M, Cloud JG, Ingermann RL (1999a) ATP levels of chinook salmon (Oncorhynchus tshawytscha) sperm following in vitro exposure to various oxygen tensions. Fish Physiol Biochem 20:389–397. doi: 10.1023/A:1007749703803 CrossRefGoogle Scholar
  4. Bencic DC, Krisfalusi M, Cloud JG, Ingermann RL (1999b) Maintenance of steelhead trout (Oncorhynchus mykiss) sperm at different in vitro oxygen tension alters ATP levels and cell functional characteristics. Fish Physiol Biochem 21:193–200. doi: 10.1023/A:1007880426488 CrossRefGoogle Scholar
  5. Billard R, Cosson M-P (1990) The energetics of fish sperm motility. In: Gagnon C (ed) Control of sperm motility, biological, clinical aspects. CRC Press, Boca Raton, pp 153–173Google Scholar
  6. Christen R, Gatti JL, Billard R (1987) 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 166:667–671. doi: 10.1111/j.1432-1033.1987.tb13565.x CrossRefPubMedGoogle Scholar
  7. Cory JG (2006) Purine and pyrimidine nucleotide metabolism. In textbook of biochemistry with clinical correlations. Wiley-Liss, Hoboken,Google Scholar
  8. Cosson J (2004) The ionic and osmotic factors controlling motility of fish spermatozoa. Aquacult Int 12:69–85. doi: 10.1023/B:AQUI.0000017189.44263.bc CrossRefGoogle Scholar
  9. Cosson MP, Cosson J, Andre F, Billard R (1995) cAMP/ATP relationship in the activation of trout sperm motility: their interaction in membrane-deprived models and in live spermatozoa. Cell Motil Cytoskeleton 31:159–176. doi: 10.1002/cm.970310208 CrossRefPubMedGoogle Scholar
  10. Cosson J, Groison A-L, Suquet M, Fauvel C, Dreanno C, Billard R (2008) Marine fish spermatozoa: racing ephemeral swimmers. Reproduction 136:277–294. doi: 10.1530/REP-07-0522 CrossRefPubMedGoogle Scholar
  11. Dreanno C, Cosson J, Suquet M, Cibert C, Fauvel C, Dorange G, Billard R (1999a) Effect of osmolality, morphology perturbations and intracellular nucleotide content during the movement of sea bass (Dicentrarchus labrax) spermatozoa. J Reprod Fertil 116:113–125. doi: 10.1530/jrf.0.1160113 PubMedCrossRefGoogle Scholar
  12. Dreanno C, Cosson J, Suquet M, Seguin F, Dorange G, Billard R (1999b) Nucleotide content, oxidative phosphorylation, morphology, and fertilizing capacity of turbot (Psetta maxima) spermatozoa during the motility period. Mol Reprod Dev 53:230–243. doi: 10.1002/(SICI)1098-2795(199906)53:2<230:AID-MRD12>3.0.CO;2-H CrossRefPubMedGoogle Scholar
  13. Dreanno C, Seguin F, Cosson J, Suquet M, Billard R (2000) H-NMR and P-NMR analysis of energy metabolism of quiescent and motile turbot (Psetta maxima) spermatozoa. J Exp Zool Part A 286:513–522. doi: 10.1002/(SICI)1097-010X(20000401)286:5<513 CrossRefGoogle Scholar
  14. Gronczewska J, Ziętara MS, Biegniewska A, Skorkowski EF (2003) Enzyme activities in fish spermatozoa with focus on lactate dehydrogenase isoenzymes from herring Clupea harengus. Comp Biochem Physiol 134B:399–406. doi: 10.1016/S1096-4959(02)00192-6 Google Scholar
  15. Grzyb K, Skorkowski EF (2006) Purification and some properties of two creatine kinase isoforms from herring (Clupea harengus) spermatozoa. Comp Biochem Physiol 144B:152–158. doi: 10.1016/j.cbpb.2006.02.002 Google Scholar
  16. Grzyb K, Rychłowski M, Biegniewska A, Skorkowski EF (2003) Quantitative determination of creatine kinase release from herring (Clupea harengus) spermatozoa induced by tributyltin. Comp Biochem Physiol 134C:207–213. doi: 10.1016/S1532-0456(02)00254-5 Google Scholar
  17. Hayashi H, Yamamoto K, Yonekawa H, Morisawa M (1987) Involvement of tyrosine protein kinase in the initiation of flagellar movement in rainbow trout spermatozoa. J Biol Chem 262:16692–16698PubMedGoogle Scholar
  18. Inaba K, Kagami O, Ogawa K (1999) Tctex2-related outer arm dynein light chain is phosphorylated at activation of sperm motility. Biochem Biophys Res Commun 256:177–183. doi: 10.1006/bbrc.1999.0309 CrossRefPubMedGoogle Scholar
  19. Ingermann RL, Robinson ML, Cloud JG (2003) Respiration of steelhead trout sperm: sensitivity to pH and carbon dioxide. J Fish Biol 62:13–23. doi: 10.1046/j.1095-8649.2003.00003.x CrossRefGoogle Scholar
  20. Kime DE, Tveiten H (2002) Unusual motility characteristic of sperm of the wolffish, Anarhichas minor. J Fish Biol 61:1549–1559. doi: 10.1111/j.1095-8649.2002.tb02479.x CrossRefGoogle Scholar
  21. Lahnsteiner F, Patzner RA, Weismann T (1992) Monosaccharides as energy resources during motility of spermatozoa in Leuciscus cephalus (Cyprinidae, Teleostei). Fish Physiol Biochem 10:283–289. doi: 10.1007/BF00004477 CrossRefGoogle Scholar
  22. Lahnsteiner F, Patzner RA, Weismann T (1993) Energy resources of spermatozoa of the rainbow trout (Oncorhynchus mykiss) (Pisces, Teleostei). Reprod Nutr Dev 33:349–360. doi: 10.1051/rnd:19930404 CrossRefPubMedGoogle Scholar
  23. Lahnsteiner F, Berger B, Weismann T (1999) Sperm metabolism of the teleost fishes Chalcalburnus chalcoides and Oncorhynchus mykiss and its relation to motility and viability. J Exp Zool 284:454–465. doi: 10.1002/(SICI)1097-010X(19990901)284:4<454::AID-JEZ12>3.0.CO;2-O CrossRefPubMedGoogle Scholar
  24. Mansour N, Lahnsteiner F, Berger B (2003) Metabolism of intratesticular spermatozoa of a tropical teleost fish (Clarias garienpinus). Comp Biochem Physiol 135B:285–296. doi: 10.1016/S1096-4959(03)00083-6 Google Scholar
  25. Perchec G, Jeulin C, Cosson J, Andre F, Billard R (1995) Relationship between sperm ATP content and motility of carp spermatozoa. J Cell Sci 108:747–753PubMedGoogle Scholar
  26. Rhemrev JP, Lens JW, McDonnell J, Schoemaker J, Vermeiden JP (2001) The postwash total progressively motile sperm cell count is a reliable predictor of total fertilisation failure in vitro fertilisation treatment. Fertil Steril 76:884–891. doi: 10.1016/S0015-0282(01)02826-6 CrossRefPubMedGoogle Scholar
  27. Rurangwa E, Biegniewska A, Swierczynski J, Ollevier F, Skorkowski EF (2001) Adenylate energy charge in fish spermatozoa: influence of pituitary hormones? In: Goos HJTh, Rastogi RK, Vaudry H, Pierantoni R (eds) Perspective in comparative endocrinology: unity, diversity. Menduzzi Editore, Bologna, pp 1203–1208Google Scholar
  28. Rurangwa E, Biegniewska A, Słomińska E, Skorkowski EF, Ollevier F (2002) Effect of tributyltin on adenylate content and enzyme activities of teleost sperm: a biochemical approach to study the mechanism of toxicant reduced spermatozoa motility. Comp Biochem Physiol 131C:335–344. doi: 10.1016/S1532-0456(02)00019-4 Google Scholar
  29. Saudrais C, Garber AT, McKay DJ, Dixon GH, Loir M (1996) Creatine kinase in trout male germ cells: purification, gene expression, and localization in the testis. Mol Reprod Dev 44:433–442. doi: 10.1002/(SICI)1098-2795(199608)44:4<433:AID-MRD2>3.0.CO;2-M CrossRefPubMedGoogle Scholar
  30. Saudrais C, Fierville F, Loir M, Le Rumeur E, Cibert C, Cosson J (1998) The use of phosphocreatine plus ADP as energy source for motility of membrane-deprived trout spermatozoa. Cell Motil Cytoskeleton 41:91–106. doi: 10.1002/(SICI)1097-0169(1998)41:2<91:AID-CM1>3.0.CO;2-I CrossRefPubMedGoogle Scholar
  31. Schlegel J, Wyss M, Eppenberger HM, Wallimann T (1990) Functional studies with the octameric and dimeric form of mitochondrial creatine kinase. J Biol Chem 265:9221–9227PubMedGoogle Scholar
  32. Smoleński RT, Lachno DR, Ledingham SJM, Yacoub MH (1990) Determination of sixteen nucleotides, nucleosides and bases using high-performance liquid chromatography and its application to the study of purine metabolism in hearts for transplantation. J Chromatogr A 527:414–420Google Scholar
  33. Tombes RM, Shapiro BM (1989) Energy transport and cell polarity: relationship of phosphagen kinase activity to sperm function. J Exp Zool 251:82–90. doi: 10.1002/jez.1402510110 CrossRefPubMedGoogle Scholar
  34. Tombes RM, Brokaw C, Shapiro BM (1987) Creatine kinase dependent energy transport in sea urchin spermatozoa. Biophys J 52:75–86. doi: 10.1016/S0006-3495(87)83190-9 CrossRefPubMedGoogle Scholar
  35. Volckaert FAM, Galbusera PHA, Hellemans BAS, van den Haute C, Vanstaen D, Ollevier F (1994) Gynogenesis in the African catfish (Clarias gariepinus): I. Induction of meiogynogenesis with thermal and pressure shocks. Aquaculture 128:221–233. doi: 10.1016/0044-8486(94)90311-5 CrossRefGoogle Scholar
  36. Ziętara MS, Słomińska E, Rurangwa E, Ollevier F, Swierczynski J, Skorkowski EF (2004a) In vitro adenine nucleotide catabolism in African catfish spermatozoa. Comp Biochem Physiol 138B:385–389. doi: 10.1016/j.cbpc.2004.04.019 Google Scholar
  37. Ziętara MS, Słomińska E, Świerczyński J, Rurangwa E, Ollevier F, Skorkowski EF (2004b) ATP content and adenine nucleotide catabolism in African catfish spermatozoa stored in various energetic substrates. Fish Physiol Biochem 30:119–127. doi: 10.1007/s10695-005-2493-1 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • M. S. Ziętara
    • 1
  • A. Biegniewska
    • 1
  • E. Rurangwa
    • 2
  • J. Swierczynski
    • 3
  • F. Ollevier
    • 2
  • E. F. Skorkowski
    • 1
    Email author
  1. 1.Laboratory of Comparative BiochemistryGdańsk UniversityGdañskPoland
  2. 2.Laboratory of Aquatic Ecology and Evolutionary BiologyKatholieke Universiteit LeuvenLeuvenBelgium
  3. 3.Department of BiochemistryMedical University of GdañskGdañskPoland

Personalised recommendations