Microsporidia are a large group of unicellular parasites that infect insects and mammals. The simpler life cycle of microsporidia in insects provides a model system for understanding their evolution and molecular interactions with their hosts. However, no complete genome is available for insect-parasitic microsporidian species. The complete genome of Antonospora locustae, a microsporidian parasite that obligately infects insects, is reported here. The genome size of A. locustae is 3 170 203 nucleotides, composed of 17 chromosomes onto which a total of 1857 annotated genes have been mapped and detailed. A unique feature of the A. locustae genome is the presence of an ultra-low GC region of approximately 25 kb on 16 of the 17 chromosomes, in which the average GC content is only 20 %. Transcription profiling indicated that the ultra-low GC region of the parasite could be associated with differential regulation of host defences in the fat body to promote the parasite’s survival and propagation. Phylogenetic gene analysis showed that A. locustae, and the microsporidian family in general, is likely at an evolutionarily transitional position between prokaryotes and eukaryotes, and that it evolved independently. Transcriptomic analysis showed that A. locustae can systematically inhibit the locust phenoloxidase PPO, TCA and glyoxylate cycles, and PPAR pathways to escape melanization, and can activate host energy transfer pathways to support its reproduction in the fat body, which is an insect energy-producing organ. Our study provides a platform and model for studies of the molecular mechanisms of microsporidium–host interactions in an energy-producing organ and for understanding the evolution of microsporidia.

中文翻译：

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单细胞寄生虫（Antonospora locustae）的完整基因组及其与宿主蝗虫的转录相互作用。

微孢子虫是一大群单细胞寄生虫，可感染昆虫和哺乳动物。昆虫中微孢子虫更简单的生命周期为了解它们的进化和与宿主的分子相互作用提供了一个模型系统。然而，昆虫寄生微孢子虫物种没有完整的基因组。Antonospora locustae的完整基因组是一种专感染昆虫的微孢子虫寄生虫，在此报告。蝗虫的基因组大小为3 170 203个核苷酸，由17条染色体组成，共有1857个注释基因被映射和详细描述。A. locustae 的独特特征基因组是在 17 条染色体中的 16 条上存在大约 25 kb 的超低 GC 区域，其中平均 GC 含量仅为 20%。转录分析表明，寄生虫的超低 GC 区域可能与脂肪体内宿主防御的差异调节有关，以促进寄生虫的生存和繁殖。系统发育基因分析表明，蝗虫和一般的微孢子虫家族很可能处于原核生物和真核生物之间的进化过渡位置，并且它是独立进化的。转录组学分析表明，A. locustae可以系统地抑制蝗虫酚氧化酶 PPO、TCA 和乙醛酸循环，以及 PPAR 途径以逃避黑化，并可以激活宿主能量转移途径以支持其在脂肪体中繁殖，脂肪体是昆虫产生能量的器官。我们的研究为研究能量产生器官中微孢子虫-宿主相互作用的分子机制以及理解微孢子虫的进化提供了一个平台和模型。