A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution

Histones and associated chromatin proteins have essential functions in eukaryotic genome organization and regulation. Despite this fundamental role in eukaryotic cell biology, we lack a phylogenetically-comprehensive understanding of chromatin evolution. Here, we combine comparative proteomics and genomics analysis of chromatin in eukaryotes and archaea. Proteomics uncovers the existence of histone post-translational modifications in Archaea. However, archaeal histone modifications are scarce, in contrast with the highly conserved and abundant marks we identify across eukaryotes. Phylogenetic analysis reveals that chromatin-associated catalytic functions (e.g., methyltransferases) have pre-eukaryotic origins, whereas histone mark readers and chaperones are eukaryotic innovations. We show that further chromatin evolution is characterized by expansion of readers, including capture by transposable elements and viruses. Overall, our study infers detailed evolutionary history of eukaryotic chromatin: from its archaeal roots, through the emergence of nucleosome-based regulation in the eukaryotic ancestor, to the diversification of chromatin regulators and their hijacking by genomic parasites

组蛋白（Histones）与相关染色质蛋白在真核生物基因组的组织与调控中发挥核心功能。尽管其在真核细胞生物学中具有基础性作用，但目前学界对染色质演化的系统发育全景认知仍存在缺失。本研究结合比较蛋白质组学与基因组学分析方法，对真核生物与古菌（Archaea）的染色质开展分析。蛋白质组学分析揭示了古菌中存在组蛋白翻译后修饰（post-translational modification）现象，但古菌的组蛋白修饰类型极为匮乏，与我们在真核生物中观测到的高度保守且丰富的修饰标记形成鲜明对比。系统发育分析显示，与染色质相关的催化功能（如甲基转移酶（methyltransferases））具有真核生物起源前的演化源头，而组蛋白修饰阅读器与分子伴侣（chaperones）则是真核生物的创新演化产物。本研究进一步表明，后续的染色质演化以识别蛋白家族的扩张为典型特征，其中包括转座因子（transposable elements）与病毒对这类蛋白的捕获事件。综上，本研究推演了真核生物染色质的完整演化历程：从其古菌起源根基，到真核祖先中核小体（nucleosome）介导的调控机制的诞生，再到染色质调控因子的多样化演化，以及这类因子被基因组寄生虫所攫取的过程。