Myriapod genomes reveal ancestral horizontal gene transfer and hormonal gene loss in millipedes

Animals have fascinating diversity of life forms. Analyses of the available genome sequence reveals dynamic evolution of gene gain and loss at different lineages in the animal tree of life (e.g. Albalat and Canestro 2016; Sharma et al 2018; Fernandez and Gabaldon 2020; Guijarro-Clarke et al 2020; Jebb et al 2020). Gene gain via another kingdom as well as the evolutionary consequence of gene loss are generally ignored and difficult to interpret. Here we sequenced six new myriapod genomes at key phylogenetic positions of this understudied arthropod lineage (three millipedes and three centipedes). Comparison of myriapod genomes revealed multiple horizontal gene transfer (HGT) of genes shared between centipedes, including glucose/arabinose dehydrogenase that happened at the last common of ancestor of centipedes, while there was no detectable HGT shared between the millipedes. In all millipede lineages, the loss of juvenile hormone O-methyltransferase, a key enzyme in catalysing the last step of sesquiterpenoid hormone methyl farnesoate production in arthropods was revealed. These findings provided the first evidence of shared HGT in the last common ancestor of centipede ancestor, while gene loss event could indeed happen in endocrine system in contrary to the conventional view of stepwise gene gain resulting in diversity of animal physiology for adaptation to environment.

动物界拥有极具魅力的生命形态多样性。现有基因组序列分析显示，在动物生命之树的不同演化支中，基因获得与丢失呈现出动态演化的特征（例如Albalat与Canestro 2016；Sharma等人2018；Fernandez与Gabaldon 2020；Guijarro-Clarke等人2020；Jebb等人2020）。跨界基因获得以及基因丢失的演化后果，通常被学界忽视且难以阐释。本研究对该尚未被充分研究的节肢动物演化支中关键系统发育位置的6个新多足类（myriapod）基因组进行了测序，涵盖3个马陆（millipede）样本与3个蜈蚣（centipede）样本。多足类基因组比对分析显示，蜈蚣类群间存在多起共享的水平基因转移（horizontal gene transfer, HGT）事件，其中包括发生在蜈蚣最近共同祖先中的葡萄糖/阿拉伯糖脱氢酶相关转移；而马陆类群间未检测到共享的水平基因转移事件。在所有马陆演化支中，均出现了保幼激素O-甲基转移酶的丢失——该酶是节肢动物体内催化倍半萜类激素法尼酸甲酯合成最后一步的关键酶。本研究的发现首次提供了蜈蚣最近共同祖先存在共享水平基因转移的证据；同时，基因丢失事件确实可发生在内分泌系统中，这与传统观点相悖：传统观点认为，动物生理多样性是通过逐步的基因获得以适应环境而形成的。