Institute of Agrifood Research and Technology, Institute of Biotechnology and Biomedicine, Universitat Autònoma de Barcelona, 08193 Barcelona, Spain.
Institute of Marine Research, Matre Aquaculture Research Station, 5984 Matredal, Norway.
Proc Natl Acad Sci U S A. 2021 Mar 9;118(10). doi: 10.1073/pnas.2019346118.
The primary task of a spermatozoon is to deliver its nuclear payload to the egg to form the next-generation zygote. With polyandry repeatedly evolving in the animal kingdom, however, sperm competition has become widespread, with the highest known intensities occurring in fish. Yet, the molecular controls regulating spermatozoon swimming performance in these organisms are largely unknown. Here, we show that the kinematic properties of postactivated piscine spermatozoa are regulated through a conserved trafficking mechanism whereby a peroxiporin ortholog of mammalian aquaporin-8 (Aqp8bb) is inserted into the inner mitochondrial membrane to facilitate HO efflux in order to maintain ATP production. In teleosts from more ancestral lineages, such as the zebrafish () and the Atlantic salmon (), in which spermatozoa are activated in freshwater, an intracellular Ca-signaling directly regulates this mechanism through monophosphorylation of the Aqp8bb N terminus. In contrast, in more recently evolved marine teleosts, such the gilthead seabream (), in which spermatozoa activation occurs in seawater, a cross-talk between Ca- and oxidative stress-activated pathways generate a multiplier regulation of channel trafficking via dual N-terminal phosphorylation. These findings reveal that teleost spermatozoa evolved increasingly sophisticated detoxification pathways to maintain swimming performance under a high osmotic stress, and provide insight into molecular traits that are advantageous for postcopulatory sexual selection.
精子的主要任务是将其核负荷传递给卵子，以形成下一代受精卵。然而，随着动物王国中一妻多夫制的反复出现，精子竞争已经广泛存在，鱼类中的竞争强度最高。尽管如此，这些生物中调节精子游动性能的分子控制机制在很大程度上仍是未知的。在这里，我们表明，后生鱼类精子的运动学特性受到一种保守的运输机制的调节，该机制通过过氧化物酶体同源物的哺乳动物水通道蛋白-8（Aqp8bb）插入到线粒体内膜，以促进 HO 流出，从而维持 ATP 的产生。在更原始的鱼类谱系中，如斑马鱼（）和大西洋三文鱼（），其精子在淡水中被激活，通过 Aqp8bb N 端的单磷酸化直接调节这种机制的细胞内 Ca 信号。相比之下，在最近进化的海洋鱼类中，如金头鲷（），其精子在海水中被激活，Ca 和氧化应激激活途径之间的串扰通过双重 N 端磷酸化对通道运输进行倍增调节。这些发现表明，鱼类精子进化出越来越复杂的解毒途径，以在高渗透压下维持游动性能，并为了解有利于交配后性选择的分子特征提供了线索。
