Table2_Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions.XLSX

Infectious disease outbreaks are causing widespread declines of marine invertebrates including corals, sea stars, shrimps, and molluscs. Dermo is a lethal infectious disease of the eastern oyster Crassostrea virginica caused by the protist Perkinsus marinus. The Pacific oyster Crassostrea gigas is resistant to Dermo due to differences in the host-parasite interaction that is not well understood. We compared transcriptomic responses to P. marinus challenge in the two oysters at early and late infection stages. Dynamic and orchestrated regulation of large sets of innate immune response genes were observed in both species with remarkably similar patterns for most orthologs, although responses in C. virginica were stronger, suggesting strong or over-reacting immune response could be a cause of host mortality. Between the two species, several key immune response gene families differed in their expansion, sequence variation and/or transcriptional response to P. marinus, reflecting evolutionary divergence in host-parasite interaction. Of note, significant upregulation of inhibitors of apoptosis (IAPs) was observed in resistant C. gigas but not in susceptible C. virginica, suggesting upregulation of IAPs is an active defense mechanism, not a passive response orchestrated by P. marinus. Compared with C. gigas, C. virginica exhibited greater expansion of toll-like receptors (TLRs) and positive selection in P. marinus responsive TLRs. The C1q domain containing proteins (C1qDCs) with the galactose-binding lectin domain that is involved in P. marinus recognition, were only present and significantly upregulated in C. virginica. These results point to previously undescribed differences in host defense genes between the two oyster species that may account for the difference in susceptibility, providing an expanded portrait of the evolutionary dynamics of host-parasite interaction in lophotrochozoans that lack adaptive immunity. Our findings suggest that C. virginica and P. marinus have a history of coevolution and the recent outbreaks may be due to increased virulence of the parasite.

传染病暴发正导致珊瑚、海星、虾类及软体动物等海洋无脊椎动物（marine invertebrates）出现大范围种群衰退。多尔姆病（Dermo）是由原生生物海洋Perkins原虫（Perkinsus marinus）引发的美洲牡蛎（Crassostrea virginica）致死性传染病。太平洋牡蛎（Crassostrea gigas）对多尔姆病具有抗性，二者的宿主-寄生虫互作（host-parasite interaction）机制尚未被充分阐明，而该抗性差异正源于此。本研究对两种牡蛎在感染早期与晚期阶段应对P. marinus侵染的转录组应答（transcriptomic response）进行了比较分析。研究发现，两种牡蛎中均有大量先天免疫应答基因（innate immune response genes）被动态且有序地调控，多数直向同源基因（orthologs）的调控模式极为相似；但美洲牡蛎的免疫应答强度更高，这提示强烈或过度活化的免疫应答可能是宿主死亡的诱因。两物种间，若干关键免疫应答基因家族在基因扩增、序列变异及/或应对P. marinus的转录应答层面存在差异，这反映出二者宿主-寄生虫互作的演化分歧。值得注意的是，抗性型太平洋牡蛎中观察到细胞凋亡抑制因子（inhibitors of apoptosis, IAPs）的显著上调，而易感型美洲牡蛎则无此现象，这提示IAPs的上调是一种主动防御机制，而非由P. marinus介导的被动应答。与太平洋牡蛎相比，美洲牡蛎的Toll样受体（toll-like receptors, TLRs）基因家族扩增程度更高，且在应对P. marinus的TLRs中存在正向选择。含有半乳糖结合凝集素结构域（galactose-binding lectin domain）、且参与P. marinus识别过程的C1q结构域蛋白（C1q domain containing proteins, C1qDCs）仅在美洲牡蛎中存在并显著上调。本研究结果揭示了两种牡蛎宿主防御基因（host defense genes）间此前未被报道的差异，这些差异或可解释二者的易感差异；同时为缺乏适应性免疫（adaptive immunity）的冠轮动物（lophotrochozoans）的宿主-寄生虫互作演化动力学提供了更为全面的刻画。本研究表明，美洲牡蛎与P. marinus存在协同演化历史，而近期的传染病暴发或源于该寄生虫毒力的增强。