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Cell and Tissue Research

, Volume 361, Issue 2, pp 619–632 | Cite as

Spermiogenesis and biflagellate spermatozoon of the teleost fish Lampanyctus crocodilus (Myctophiformes, Myctophidae): ultrastructure and characterisation of its sperm basic nuclear proteins

  • E. Ribes
  • M. Cheema
  • R. González-Romero
  • D. Lloris
  • J. Ausió
  • N. SaperasEmail author
Regular article

Abstract

We undertook an ultrastructural study of the spermiogenesis of the lanternfish Lampanyctus crocodilus (Myctophiformes, Myctophidae) with special emphasis on the condensation of chromatin and the biochemical characterisation of its sperm nuclear basic proteins (SNBPs). The round head of the early spermatid of L. crocodilus develops into a curved conical-shaped head in the spermatozoon. Two flagella, present even in the spermatid, are inserted laterally at the convex side of the sperm head. Both flagella possess an axoneme with a 9 + 0 instead of the typical 9 + 2 axonemal structure. Mitochondria undergo a characteristic redistribution during spermiogenesis. A reduced number of them are present lying away from the centrioles at both ends of the concave side of the sperm head. During the chromatin condensation stages in spermiogenesis, fibrogranular structures with granules of 25 ± 5 and 50 ± 5 nm can be observed in the early spermatid and develop into larger granules of about 150 ± 50 nm in the middle spermatid. The latter granules coalesce during the transition to the advanced spermatid and spermatozoon giving rise to highly condensed chromatin in the sperm cell. Protamines are the main SNBPs associated with this chromatin; however, they are unusually large and correspond to the largest protamines described in fish to date. Small stoichiometric amounts of histones and other basic proteins coexist with these protamines in the spermatozoon.

Keywords

Biflagellate sperm Fish spermiogenesis Sperm nuclear basic proteins Myctophiformes Lampanyctus 

Notes

Acknowledgments

We are very grateful to José Antonio Caparrós and the crew of the fishing boats Nus and l’Òstia for kindly providing us with the biological material. We are also thankful to Raquel Sánchez-Giraldo for her help with sample transportation and for her assistance with the FPLC and to Enric Huguet and Sara K. Murase for their help with translations from Japanese. Microscopic observations were performed in the Scientific Technical Services of the University of Barcelona.

References

  1. Ando T, Watanabe S (1969) A new method for fractionation of protamines and the amino acid sequence of one component of salmine and three components of iridine. Int J Protein Res 1:221–224PubMedCrossRefGoogle Scholar
  2. Ausió J (1988) An unusual cysteine-containing histone H1-like protein and two protamine-like proteins are the major nuclear proteins of the sperm of the bivalve mollusc Macoma nasuta. J Biol Chem 263:10141–10150PubMedGoogle Scholar
  3. Ausió J (1999) Histone H1 and evolution of sperm nuclear basic proteins. J Biol Chem 274:31115–31118PubMedCrossRefGoogle Scholar
  4. Boisson C, Mattei X, Mattei C (1967) Troisième note sur la spermiogenèse de Protopterus annectens (Dipneuste) du Sénégal. Inst Fondam d’Afrique Noire Bull A (Sci Nat) 29:1097–1121Google Scholar
  5. Buesa C, Valle L del, Saperas N, Goethals M, Lloris D, Chiva M (1998) Primary structure of scombrine α: two different species with an identical protamine. Comp Biochem Physiol 119B:145–149Google Scholar
  6. Casas MT, Muñoz-Guerra S, Subirana JA (1981) Preliminary report on the ultrastructure of chromatin in the histone containing spermatozoa of a teleost fish. Biol Cell 40:87–92Google Scholar
  7. Chiva M, Subirana JA (1987) Mètode per a obtenir protamines testiculars riques en arginina. J Biol Mol (Soc Cat Biol) 4:77–80Google Scholar
  8. Chiva M, Kasinsky HE, Mann M, Subirana JA (1988) On the diversity of sperm basic proteins in the vertebrates. VI. Cytochemical and biochemical analysis in birds. J Exp Zool 245:304–317CrossRefGoogle Scholar
  9. Chiva M, Rosenberg E, Kasinsky HE (1990) Nuclear basic proteins in mature testis of the ascidian tunicate Styela montereyensis. J Exp Zool 253:7–19CrossRefGoogle Scholar
  10. Chiva M, Lafargue F, Rosenberg E, Kasinsky HE (1992) Protamines, not histones, are the predominant basic proteins in sperm nuclei of solitary ascidian tunicates. J Exp Zool 263:338–349CrossRefGoogle Scholar
  11. Chiva M, Saperas N, Ribes E (2011) Complex chromatin condensation patterns and nuclear protein transitions during spermiogenesis: examples from mollusks. Tissue Cell 43:367–376PubMedCrossRefGoogle Scholar
  12. De Petrocellis B, Parente A, Tomei L, Geraci G (1983) An H1 histone and a protamine molecule organize the sperm chromatin of the marine worm Chaetopeterus variopedatus. Cell Differ 12:129–135CrossRefGoogle Scholar
  13. Dixon GH, Aiken JM, Jankowski JM, McKenzie DI, Moir R, States JC (1985) Organization and evolution of the protamine genes of salmonid fishes. In: Reeck G, Goodwin G, Puigdomènech P (eds) Chromosomal proteins and gene expression. Plenum, New York, pp 287–314CrossRefGoogle Scholar
  14. Eirín-López JM, Ausió J (2009) Origin and evolution of chromosomal sperm proteins. Bioessays 31:1062–1070PubMedCrossRefGoogle Scholar
  15. Fioretti FM, Febbraio F, Carbone A, Branno M, Carratore V, Fucci L, Ausió J, Piscopo M (2012) A sperm nuclear basic protein from the sperm of the marine worm Chaetopterus variopedatus with sequence similarity to the arginine-rich C-termini of chordate protamine-likes. DNA Cell Biol 31:1392–1402PubMedCrossRefGoogle Scholar
  16. Fishelson L, Delarea Y, Gon O (2006) Testis structure, spermatogenesis, spermatocytogenesis, and sperm structure in cardinal fish (Apogonidae, Perciformes). Anat Embryol 211:31–46PubMedCrossRefGoogle Scholar
  17. Frehlick LJ, Eirín-López JM, Prado A, Su HW, Kasinsky HE, Ausió J (2006) Sperm nuclear basic proteins of two closely related species of scorpaeniform fish (Sebastes maliger, Sebastolobus sp.) with different sexual reproduction and the evolution of fish protamines. J Exp Zool 305A:277–287CrossRefGoogle Scholar
  18. Giménez-Bonafé P, Laszczak M, Kasinsky HE, Lemke MJ, Lewis JD, Iskandar M, He T, Ikonomou MG, White FM, Hunt DF, Chiva M, Ausió J (2000) Characterization and evolutionary relevance of the sperm nuclear basic proteins from stickleback fish. Mol Reprod Dev 57:185–193PubMedCrossRefGoogle Scholar
  19. Hara M (2007) Ultrastructure of spermatozoa of two species of myctophidae; Symbolophorus californiensis and Notoscopelus sp. Jpn J Ichthyol 54:41–46Google Scholar
  20. Hara M, Okiyama M (1998) An ultrastructural review on the spermatozoa of Japanese fishes. Bull Ocean Res Inst Univ Tokyo 33:1–138Google Scholar
  21. Hoffman RA (1963) Gonads, spermatic ducts, and spermatogenesis in the reproductive system of male toadfish, Opsanus tau. Chesap Sci 4:21–29CrossRefGoogle Scholar
  22. Hulley PA (1984) Myctophidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean, vol I. UNESCO, Paris, pp 429–483Google Scholar
  23. Hunt JG, Kasinsky HE, Elsey RM, Wright CL, Rice P, Bell JE, Sharp DJ, Kiss AJ, Hunt DF, Arnott DP, Russ MM, Shabanowitz J, Ausió J (1996) Protamines of reptiles. J Biol Chem 271:23547–23557PubMedCrossRefGoogle Scholar
  24. Jamieson BGM (1991) Fish evolution and systematics: evidence from spermatozoa. Cambridge University Press, CambridgeGoogle Scholar
  25. Jamieson BGM (2009a) Reproductive biology and phylogeny of fishes (agnathans and bony fishes): phylogeny, reproductive system, viviparity, spermatozoa. Reproductive biology and phylogeny, vol 8A. Science Publishers, EnfieldCrossRefGoogle Scholar
  26. Jamieson BGM (2009b) Ultrastructure of spermatozoa: Neoteleostei: Stenopterygii, Cyclosquamata, Scopelomorpha and Paracanthopterygii. In: Jamieson BGM (ed) Reproductive biology and phylogeny of fishes (agnathans and bony fishes): phylogeny, reproductive system, viviparity, spermatozoa. Reproductive biology and phylogeny series, vol 8A. Science Publishers, Enfield, pp 415–445Google Scholar
  27. Jamieson BGM, Mattei X (2009) Ultrastructure of spermatozoa: Elopomorpha and Clupeomorpha. In:Jamieson BGM (ed) Reproductive biology and phylogeny of fishes (agnathans and bony fishes): phylogeny, reproductive system, viviparity, spermatozoa. Reproductive biology and phylogeny, vol 8A. Science Publishers, Enfield, pp 255–285CrossRefGoogle Scholar
  28. Jespersen Å (1971) Fine structure of the spermatozoon of the Australian lungfish Neoceratodus forsteri (Krefft). J Ultrastr Res 37:178–185Google Scholar
  29. Kasinsky HE, Frehlick LJ, Su HW, Ausió J (2005) Protamines in the internally fertilizing neobatrachian frog Eleutherodactylus coqui. Mol Reprod Dev 70:373–381PubMedCrossRefGoogle Scholar
  30. Kurtz K, Saperas N, Ausió J, Chiva M (2009) Spermiogenic nuclear protein transitions and chromatin condensation. Proposal for an ancestral model of nuclear spermiogenesis. J Exp Zool 312B:149–163CrossRefGoogle Scholar
  31. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  32. Lahnsteiner F (2003) The spermatozoa and eggs of the cardinal fish. J Fish Biol 62:115–128CrossRefGoogle Scholar
  33. Lahnsteiner F, Patzner RA (2007) Sperm morphology and ultrastructure in fish. In: Alavi SMH, Cosson JJ, Coward K, Rafiee G (eds) Fish spermatology. Alpha Science International, Oxford, pp 1–61Google Scholar
  34. Lewis J, Song Y, Jong M de, Bagha S, Ausió J (2003) A walk through vertebrate and invertebrate protamines. Chromosoma 111:473–482Google Scholar
  35. Martínez-Soler F, Kurtz K, Ausió J, Chiva M (2007) Transition of nuclear proteins and chromatin structure in spermiogenesis of Sepia officinalis. Mol Reprod Dev 74:360–370PubMedCrossRefGoogle Scholar
  36. Mattei C, Mattei X (1978) La spermiogenèse d’un poisson téléostéen (Lepadogaster lepadogaster). II. Le spermatozoide. Biol Cell 32:267–274Google Scholar
  37. Mattei C, Mattei X (1984) Spermatozoïdes biflagellés chez un poisson téleóstéen de la famille Apogonidae. J Ultrastr Res 88:223–228CrossRefGoogle Scholar
  38. Mattei C, Mattei X, Marchand B (1978) Elimination de cytoplasme par les spermatides jeunes de deux poissons téléostéens: Citharinus sp. et Lampanyctus sp. C R Soc Biol 172:393–396Google Scholar
  39. Mattei X (1970) Spermiogenèse comparée des poissons. In: Baccetti B (ed) Comparative spermatology. Academic Press, New York, pp 57–69Google Scholar
  40. Mattei X (1991a) Spermatozoon ultrastructure and taxonomy in fishes. In: Baccetti B (ed) Proceedings of the VIth International Congress on spermatology, Siena. Raven, New York, pp 985–990Google Scholar
  41. Mattei X (1991b) Spermatozoon ultrastructure and its systematic implications in fishes. Can J Zool 69:3038–3055CrossRefGoogle Scholar
  42. Mattei X, Mattei C (1976) Spermatozoïdes à deux flagelles de type 9 + 0 chez Lampanyctus sp. (poisson Myctophidae). J Microsc Biol Cell 25:187–188Google Scholar
  43. Mattos E, Santos MNS, Azevedo C (2002) Biflagellate spermatozoon structure of the hermaphrodite fish Satanoperca jurupari (Heckel, 1840) (Teleostei, Cichlidae) from the Amazon river. Braz J Biol 62:847–852CrossRefGoogle Scholar
  44. Nelson JS (2006) Fishes of the world, 4th edn. Wiley, HobokenGoogle Scholar
  45. Okamoto Y, Muta E, Ota S (1987) Primary structures of M6 and M7 of mugiline beta (Mugil japonicus). J Biochem 101:1017–1024PubMedGoogle Scholar
  46. Oliva R, Dixon GH (1989) Chicken protamine genes are intronless. The complete genomic sequence and organization of the two loci. J Biol Chem 264:12472–12481PubMedGoogle Scholar
  47. Oliva R, Dixon GH (1991) Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40:25–94PubMedCrossRefGoogle Scholar
  48. Piscopo M, Tomei L, De Petrocellis L, Geraci G (1993) Anion-mediated lysine-arginine interaction. Evidence in Chaetopterus variopedatus sperm protamine. FEBS Lett 334:125–127PubMedCrossRefGoogle Scholar
  49. Puckerson ML, Jarvis JUM, Luse SA, Dempsey EW (1974) X-ray analysis coupled with scanning and transmission electron microscopic observations of spermatozoa of the African lungfish, Protopterus aethiopicus. J Zool 172:1–12CrossRefGoogle Scholar
  50. Quagio-Grassiotto I, Ortiz RJ, Sabaj Pérez MH, Oliveira C (2011) Sperm of Doradidae (Teleostei: Siluriformes). Tissue Cell 43:8–23PubMedCrossRefGoogle Scholar
  51. Ribes E, Sánchez de Romero LD, Kasinsky HE, Valle L del, Giménez-Bonafé P, Chiva M (2001) Chromatin reorganization during spermiogenesis of the mollusc Thais hemostoma (Muricidae). Implications for sperm nuclear morphogenesis in cenogatropods. J Exp Zool 289:304–316Google Scholar
  52. Saperas N, Chiva M, Ausió J (1992) Purification and characterization of the protamines and related proteins from the sperm of a tunicate, Styela plicata. Comp Biochem Physiol B 103:969–974Google Scholar
  53. Saperas N, Lloris D, Chiva M (1993a) Sporadic appearance of histones, histone-like proteins, and protamines in sperm chromatin of bony fish. J Exp Zool 265:575–586CrossRefGoogle Scholar
  54. Saperas N, Ribes E, Buesa C, García-Hegart F, Chiva M (1993b) Differences in chromatin condensation during spermiogenesis in two species of fish with distinct protamines. J Exp Zool 265:185–194PubMedCrossRefGoogle Scholar
  55. Saperas N, Ausió J, Lloris D, Chiva M (1994) On the evolution of protamines in bony fish: alternatives to the “retroviral horizontal transmission” hypothesis. J Mol Evol 39:282–295PubMedCrossRefGoogle Scholar
  56. Shain AAB (2006) Semicystic spermatogenesis and biflagellate spermatozoon ultrastructure in the Nile electric catfish Malapterus electricus (Teleostei: Siluriformes: Malapteruridae). Acta Zool 87:215–227Google Scholar
  57. Spadella MA, Oliveira C, Quagio-Grassiotto I (2006) Occurrence of biflagellate spermatozoa in Cetopsidae, Aspredinidae, and Nematogenyidae (Teleostei: Ostariophysi: Siluriformes). Zoomorphology 125:135–145Google Scholar
  58. Stanley HP (1965) Electron microscopic observations on the biflagellate spermatids of the teleost fish Porichthys notatus. Anat Rec 151:477Google Scholar
  59. Subirana JA, Cozcolluela C, Palau J, Unzeta M (1973) Protamines and other basic proteins from spermatozoa of molluscs. Biochim Biophys Acta 317:364–379PubMedCrossRefGoogle Scholar
  60. Suzuki K, Ando T (1972) Studies on protamines. XVII. The complete amino acid sequence of clupeine YI. J Biochem 72:1433–1446PubMedGoogle Scholar
  61. Takamune K, Nishida H, Takai M, Katagiri C (1991) Primary structure of toad sperm protamines and nucleotide sequence of their cDNAs. Eur J Biochem 196:401–406PubMedCrossRefGoogle Scholar
  62. Yao Z, Emerson CJ, Crim LW (1995) Ultrastructure of the spermatozoa and eggs of the ocean pout (Macrozoarces americanus L.), an internally fertilizing marine fish. Mol Reprod Dev 42:58–64PubMedCrossRefGoogle Scholar
  63. Young JW, Blaber SJM, Rose R (1987) Reproductive biology of three species of midwater fishes associated with continental slope of eastern Tasmania, Australia. Mar Biol 95:323–332CrossRefGoogle Scholar
  64. Yulikova EP, Rybin VK, Silaev AB (1979) The primary structure of stellin A. Bioorg Khim 5:5–10Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • E. Ribes
    • 1
  • M. Cheema
    • 2
  • R. González-Romero
    • 2
  • D. Lloris
    • 3
  • J. Ausió
    • 2
  • N. Saperas
    • 4
    Email author
  1. 1.Departament de Biologia Ceŀlular, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Department of Biochemistry and MicrobiologyUniversity of VictoriaVictoriaCanada
  3. 3.Departament de Recursos Marins RenovablesInstitut de Ciències del Mar (CSIC)BarcelonaSpain
  4. 4.Departament d’Enginyeria Química, ETSEIBUniversitat Politècnica de CatalunyaBarcelonaSpain

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