A myxozoan genome reveals mosaic evolution in a parasitic cnidarian

Background: Parasite evolution has been conceptualized as a process of genetic loss and simplification. Contrary to this model, there is evidence of expansion and conservation of gene families related to essential functions of parasitism in some parasite genomes, reminiscent of widespread mosaic evolution – where subregions of a genome have different rates of evolutionary change. We found evidence of mosaic genome evolution in the cnidarian Myxobolus honghuensis, a myxozoan parasite of fish, with extremely simple morphology.
Results: We compared M. honghuensis with other myxozoans and free-living cnidarians, and determined that it has the largest myxozoan genome (206 Mb), which is less reduced and less compact due to gene retention, large introns, transposon insertion, but not polyploidy. Relative to other metazoans, the M. honghuensis genome is depleted of neural genes and has only the simplest animal immune components. Conversely, it has relatively more genes involved in stress resistance, tissue invasion, energy metabolism, and cellular processes compared to other myxozoans and free-living cnidarians. We postulate that the expansion of these gene families is the result of evolutionary adaptations to endoparasitism. M. honghuensis retains genes found in free-living Cnidaria, including a reduced nervous system, myogenic components, ANTP class Homeobox genes, and components of the Wnt and Hedgehog pathways.
Conclusions: Our analyses suggest that the M. honghuensis genome evolved as a mosaic of conservative, divergent, depleted, and enhanced genes and pathways. These findings illustrate that myxozoans are not as genetically simple as previously regarded, and their evolution is driven by both genomic streamlining and expansion.

研究背景：长期以来，寄生虫演化被视为以基因丢失与简化为主的过程。但与该模型相悖的是，已有研究在部分寄生虫基因组中发现与寄生核心功能相关的基因家族出现扩张并保守保留的现象，这与广泛存在的镶嵌演化（mosaic evolution）特征相符——即基因组不同亚区域具有差异化的演化速率。本研究在鱼类寄生黏孢子虫（myxozoan）洪湖碘泡虫（Myxobolus honghuensis）中发现了基因组镶嵌演化的证据，该物种形态结构极度简化。
研究结果：本研究通过将洪湖碘泡虫与其他黏孢子虫及自由生活刺胞动物（cnidarian）进行比较后发现，其基因组（206 Mb）是目前已知最大的黏孢子虫基因组，该基因组因基因保留、大尺寸内含子（intron）及转座子（transposon）插入而呈现较低程度的缩减与压缩，并未发生多倍体化（polyploidy）。相较于其他后生动物（metazoans），洪湖碘泡虫的基因组存在神经相关基因缺失的情况，仅保留了最为简化的动物免疫组分。与之相反，相较于其他黏孢子虫与自由生活刺胞动物，该物种中参与抗逆（stress resistance）、组织侵袭（tissue invasion）、能量代谢（energy metabolism）及细胞过程（cellular processes）的基因数量相对更多。我们推测，这类基因家族的扩张是其适应内寄生（endoparasitism）生活的演化结果。洪湖碘泡虫仍保留了自由生活刺胞动物的部分基因，包括简化的神经系统、肌源性组分（myogenic components）、ANTP类同源框基因（Homeobox genes），以及Wnt信号通路与Hedgehog信号通路的相关组分。
研究结论：本研究分析表明，洪湖碘泡虫的基因组演化呈现出保守、分化、缺失与扩增并存的镶嵌式特征。本研究结果显示，黏孢子虫的遗传复杂度并未如既往认知般低下，其演化同时受到基因组精简与基因扩增双重驱动。