Log in

The Sperm Nuclear Basic Proteins (SNBPs) of the Sponge Neofibularia nolitangere: Implications for the Molecular Evolution of SNBPs

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

We have isolated and characterized for the first time, the SNBPs from an organism (Neofibularia nolitangere) of the phylum Porifera (Sponges). We have shown that these proteins consist of histones which, as expected, exhibit an amino acid composition very similar to that of other eukaryotic histones. The finding of histones in the sperm of these primitive organisms provides support to the notion that histones (SNBPs of the histone, H, type) were the proteins present at the onset of SNBP evolution. In contrast, a discrete number of alternative SNBP types (protamine-like, PL; protamine, P, types) seem to have appeared later on in the course of evolution and are found in both protostomes and deuterostomes, most likely as a result of processes of parallel evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

HPLC:

high-performance liquid chromatography

PAGE:

polyacrylamide gel electrophoresis

SDS:

sodium dodecylsulfate

SNBPs:

sperm nuclear basic proteins

TFA:

trifluoroacetic acid

References

  • Ausio J (1992) Presence of a highly specific histone Hl-like protein in the chromatin of the sperm of the bivalve mollusks. Mol Cell Biochem 115: 163–172

    Article  PubMed  CAS  Google Scholar 

  • Ausio J (1995) Histone HI and the evolution of the nuclear spermspecific proteins. In: Jamieson BGM, Ausio J, Justine JL (eds) Advances in spermatozoal taxonomy and phylogeny. Mémoires du Muséum National d’Histoire Naturelle, Paris, 166: 447–462

    Google Scholar 

  • Black JA, Dixon GH (1967) Evolution of protamine: a further example of partial gene duplication. Nature 216: 152–154

    Article  PubMed  CAS  Google Scholar 

  • Bloch DP (1969) A catalog of sperm histones. Genetics (Suppl) 61: 93–111

    CAS  Google Scholar 

  • Bloch DP (1976) Histones of sperm. In: King RC (ed) Handbook of genetics, vol 5. Plenum, NY, pp 139–167

    Google Scholar 

  • Chiva M, Saperas N, Caceres C, Ausio J (1995) Nuclear basic proteins from the sperm of tunicates, cephalochordates, agnathans and fish. In: Jamieson BGM, Ausio J, Justine JL (eds) Advances in spermatozoal taxonomy and phylogeny. Mémoires du Muséum d’Histoire Naturelle, Paris, 166: 501–514

    Google Scholar 

  • Daban M, Martinage A, Kouach M, Chiva M, Subirana JA, Sautière P (1995) Sequence analysis and structural features of the largest known protamine isolated from the sperm of the archaoegastropod Monodonta turbinata. J Mol Evol 40: 663–670

    Article  PubMed  CAS  Google Scholar 

  • Hickman CP Jr, Roberts LS, Larson A (1993) Integrated principles of zoology. 2nd ed. Mosby, St Louis, MO

    Google Scholar 

  • Hoppe WF (1988) Reproductive patterns in three species of large coral reef sponges. Coral Reefs 7: 45–50

    Article  Google Scholar 

  • Hoppe WF, Reichert MJM (1987) Predictable annual mass release of gametes by the coral reef sponge Neofibularia nolitangere (Porifera: Demospongiae). Mar Biol 94: 277–285

    Article  Google Scholar 

  • Hunt JG, Kasinsky HE, Elsey RM, Wright CL, Rice P, Bell JE, Sharp DJ, Kiss AJ, Hunt DF, Arnott DP, Russ MM, Shabanowitz J, Ausio J (1996) Protamines of reptiles. J Biol Chem 271: 23547–23557

    Article  PubMed  CAS  Google Scholar 

  • Isenberg I(1978) Histones. In: Busch H (ed) The cell nucleus, vol 4, part A. Academic Press, New York, pp 135–154

    Google Scholar 

  • Jutglar L, Borrell JI, Ausio J (1991) Primary, secondary and tertiary structure of the core of a histone Hl-like protein from the sperm of Mytilus. J Biol Chem 266: 8184–8191

    PubMed  CAS  Google Scholar 

  • Kasinsky HE (1989) Specificity and distribution of sperm basic proteins. In: Hnilica LS, Stein GS, Stein JL(eds) Histones and other basic nuclear proteins. CRC Press, Boca Ratón, FL, pp 73–163

    Google Scholar 

  • Krawetz SA, Dixon GH (1988) Sequence similarities of the protamine genes: implications for regulation and evolution. J Mol Evol 27: 291–297

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227: 680–685

    Article  PubMed  CAS  Google Scholar 

  • Lee C, Mazrimas J, Balhorn R (1991) Analysis of protamines isolated from alcohol preserved epididymes. Mol Rep Dev 30: 154–158

    Article  CAS  Google Scholar 

  • Mayes ELV, Johns EW(1982) Accumulated data. In: Johns EW (ed) The HMG chromosomal proteins. Academic Press, New York, pp 223–247

    Google Scholar 

  • Mori N(1993) A genetic fossil: protamine gene as a primordial gene. Naturwissenchaften 80: 222–224

    Article  CAS  Google Scholar 

  • Oliva R, Dixon GH (1991) Vertebrate protamine genes and the histoneto-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40: 25–94

    Article  PubMed  CAS  Google Scholar 

  • Panyim S, Chalkley R (1969) High resolution acrylamide gel electrophoresis of histones. Arch Biochem Biophys 130: 337–346

    Article  PubMed  CAS  Google Scholar 

  • Raff RA (1996) The shape of life. Genes, development, and the evolution of animal form. The University of Chicago Press, Chicago

    Google Scholar 

  • Rizzo PJ, Bradley W, Morris RL (1985) Histones of the unicellular alga Olisthodiscus luteus. Biochemistry 24: 1727–1732

    Article  CAS  Google Scholar 

  • Rocchini C, Zhang F, Ausiö J (1995) Two highly specialized histone H1 proteins are the major chromosomal proteins of the sperm of the sea anemone Urticina (Tealia) crassicornis. Biochemistry 34: 15704–15712

    Article  PubMed  CAS  Google Scholar 

  • Rocchini C, Marx MR, von Carosfeld JS, Kasinsky HE, Rosenberg E, Sommer F, Ausio J (1996) Replacement of nucleosomal histones by histone Hl-like proteins during spermiogenesis in Cnidaria: evolutionary implications. J Mol Evol 42: 240–246

    Article  CAS  Google Scholar 

  • Ruddle FH, Bentley KL, Murtha MT, Risch N (1994) Gene loss and gain in the evolution of the vertebrates. Development (Suppl) 155-161

  • Saperas N, Ausio J, Domenec L, Chiva M (1994) On the evolution of protamines in bony fish: alternatives to the “retroviral horizontal transmission” hypothesis. J Mol Evol 39: 282–295

    Article  PubMed  CAS  Google Scholar 

  • Saperas N, Chiva M, Pfeiffer DC, Kasinsky HE, Ausio J(1997) Sperm nuclear basic proteins (SNBPs) of agnathans and chondrichthyans: variability and evolution of sperm proteins in fish. J Mol Evol 44: (in press)

  • Subirana JA (1983) Nuclear proteins in spermatozoa and their interactions with DNA. In: AndréJ (ed) The sperm cell. Martinus Nijhoff, The Hague

    Google Scholar 

  • Subirana JA, Cozcolluela C, Palau J, Unzeta M (1973) Protamines and other basic proteins from spermatozoa of molluscs. Biochim Biophys Acta 317: 364–379

    CAS  Google Scholar 

  • van Holde KE (1988) Chromatin. Springer Verlag, New York

    Google Scholar 

  • Van Veghel MLJ (1993) Multiple species spawning in Curaçao reefs. Bull Mar Sci 52: 1017–1021

    Google Scholar 

  • von Holt C, de Groot P, Schwager S, Brandt WF (1984) The structure of sea urchin histones and consideration of their function. In: Stein GS, Stein JL, Marzluff WF (eds) Histone genes: structure, organization and regulation. John Wiley, New York, pp 65–105

    Google Scholar 

  • Zuckerkandl E (1994) Molecular pathways to parallel evolution: I. Gene nexuses and their morphological correlates. J Mol Evol 39: 661–678

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ausiö, J., Van Veghel, M.L.J., Gomez, R. et al. The Sperm Nuclear Basic Proteins (SNBPs) of the Sponge Neofibularia nolitangere: Implications for the Molecular Evolution of SNBPs. J Mol Evol 45, 91–96 (1997). https://doi.org/10.1007/PL00006207

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/PL00006207

Key words

Navigation