Hydrozoan sperm-specific H2B histone variants stabilize chromatin and block transcription without enhancing chromatin condensation

Torok, A.; Browne, M. J.; Vilar, J. C.; Patwal, I.; DuBuc, T. Q.; Febrimarsa, F.; Atcheson, E.; Flaus, A.; Frank, U.; Gornik, S. G.

doi:10.1101/2021.08.30.458175

bioRxiv · 10.1101/2021.08.30.458175

Hydrozoan sperm-specific H2B histone variants stabilize chromatin and block transcription without enhancing chromatin condensation

Torok, A.·Browne, M. J.·Vilar, J. C.·Patwal, I.·DuBuc, T. Q.·Febrimarsa, F.·Atcheson, E.·Flaus, A.·Frank, U.·Gornik, S. G.

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Abstract

Many animals achieve sperm chromatin compaction and stabilisation during spermatogenesis by replacing canonical histones with sperm nuclear basic proteins (SNBPs) such as protamines. A number of animals including hydrozoan cnidarians and echinoid sea urchins lack protamines and have instead evolved a distinctive family of sperm-specific histone H2Bs (spH2Bs) with extended N-termini rich in SPKK-related motifs. Sperm packaging in echinoids such as sea urchins is regulated by spH2Bs and their sperm is negatively buoyant for fertilization on the sea floor. Hydroid cnidarians also package sperm with spH2Bs but undertake broadcast spawning and their sperm properties are poorly characterised. We show that sperm chromatin from the hydroid Hydractinia possesses higher stability than its somatic equivalent, with reduced accessibility of sperm chromatin to transposase Tn5 integration in vivo and to endonucleases in vitro. However, nuclear dimensions are only moderately reduced in mature Hydractinia sperm compared to other cell types. Ectopic expression of spH2B in the background of H2B knockdown resulted in downregulation of global transcription and cell cycle arrest in embryos without altering their nuclear density. Taken together, spH2B variants containing SPKK-related motifs act to stabilise chromatin and silence transcription in Hydractinia sperm without significant chromatin compaction. This is consistent with a contribution of spH2B to sperm buoyancy as a reproductive adaptation.

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Torok, A., Browne, M. J., Vilar, J. C., Patwal, I., DuBuc, T. Q., Febrimarsa, F., Atcheson, E., Flaus, A., Frank, U., Gornik, S. G.. 2021-08-30. Hydrozoan sperm-specific H2B histone variants stabilize chromatin and block transcription without enhancing chromatin condensation. https://doi.org/10.1101/2021.08.30.458175

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