Department of Entomology and Nematology, University of Florida, Gainesville, USA.
Institute of Ecology and Evolution, University of Edinburgh, Edinburgh, UK.
BMC Genomics. 2023 May 24;24(1):278. doi: 10.1186/s12864-023-09350-0.
Apicomplexa are ancient and diverse organisms which have been poorly characterized by modern genomics. To better understand the evolution and diversity of these single-celled eukaryotes, we sequenced the genome of Ophryocystis elektroscirrha, a parasite of monarch butterflies, Danaus plexippus. We contextualize our newly generated resources within apicomplexan genomics before answering longstanding questions specific to this host-parasite system. To start, the genome is miniscule, totaling only 9 million bases and containing fewer than 3,000 genes, half the gene content of two other sequenced invertebrate-infecting apicomplexans, Porospora gigantea and Gregarina niphandrodes. We found that O. elektroscirrha shares different orthologs with each sequenced relative, suggesting the true set of universally conserved apicomplexan genes is very small indeed. Next, we show that sequencing data from other potential host butterflies can be used to diagnose infection status as well as to study diversity of parasite sequences. We recovered a similarly sized parasite genome from another butterfly, Danaus chrysippus, that was highly diverged from the O. elektroscirrha reference, possibly representing a distinct species. Using these two new genomes, we investigated potential evolutionary response by parasites to toxic phytochemicals their hosts ingest and sequester. Monarch butterflies are well-known to tolerate toxic cardenolides thanks to changes in the sequence of their Type II ATPase sodium pumps. We show that Ophryocystis completely lacks Type II or Type 4 sodium pumps, and related proteins PMCA calcium pumps show extreme sequence divergence compared to other Apicomplexa, demonstrating new avenues of research opened by genome sequencing of non-model Apicomplexa.
顶复动物门是古老而多样的生物，其现代基因组学研究还很不完善。为了更好地了解这些单细胞真核生物的进化和多样性，我们对帝王蝶的寄生虫 Ophryocystis elektroscirrha 的基因组进行了测序。在回答这个宿主-寄生虫系统的长期问题之前，我们将新生成的资源置于顶复动物门基因组学的背景下。首先，基因组非常小，总共只有 900 万个碱基，不到另外两种已测序的感染无脊椎动物的顶复动物 Porospora gigantea 和 Gregarina niphandrodes 的一半。我们发现 O. elektroscirrha 与每个已测序的相关物种共享不同的直系同源物，这表明真正的普遍保守顶复动物基因集实际上非常小。接下来，我们表明来自其他潜在宿主蝴蝶的测序数据可用于诊断感染状态和研究寄生虫序列的多样性。我们从另一种蝴蝶 Danaus chrysippus 中恢复了一个大小相似的寄生虫基因组，它与 O. elektroscirrha 参考基因组高度分化，可能代表一个独特的物种。使用这两个新基因组，我们研究了寄生虫对其宿主摄入和隔离的有毒植物化学物质的潜在进化反应。帝王蝶因它们的 II 型 ATP 酶钠泵的序列变化而能够耐受有毒的卡林内酯，这是众所周知的。我们发现 Ophryocystis 完全缺乏 II 型或 4 型钠泵，与其他顶复动物门相比，相关的 PMCA 钙泵蛋白表现出极端的序列分化，这表明通过对非模式顶复动物门进行基因组测序开辟了新的研究途径。
