Chromatin contortions to fit into the cricket sperm nucleus

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"Spermiogenesis is a radical case of differentiation whereby sperm cells acquire a compact and specialized morphology to accommodate the constraints of sexual reproduction while preserving their main cargo, an intact copy of the paternal genome. In animals, this often involves the replacement of most histones by sperm-specific nuclear basic proteins (SNBPs). Yet, how the SNBP-structured chromatin achieves compaction and shaping is largely unknown. Here, we exploited confocal, electron and super-resolution STORM microscopy observations, coupled with polymer modeling simulations to identify the higher-order architecture of sperm chromatin in the needle-shaped nucleus of the emerging model cricket Gryllus bimaculatus. While we observed an expected nucleosomal organization in precursor cells, SNBP-organized sperm chromatin was strikingly different. In sperm, DNA was structured as ~25nm-thick fibers coiled along the elongated nucleus axis. This chromatin spool further achieved large-scale helical twisting in the final stages of spermiogenesis, favoring its ultracompaction. By establishing a dialog between microscopy observations and polymer simulations, we identified a surprisingly simple biophysical mechanism whereby a nucleated rigidification of chromatin linked to the histone-SNBP transition can largely recapitulate these dramatic transitions. Our work highlights a mode of higher-order genome organization in cricket sperm completely distinct from nucleosomal chromatin, and establishes a multidisciplinary methodological framework to understand this and other types of non-canonical chromatin structures."