Data_Sheet_1_Dinoflagellate Host Chloroplasts and Mitochondria Remain Functional During Amoebophrya Infection.PDF

Dinoflagellates are major components of phytoplankton that play critical roles in many microbial food webs, many of them being hosts of countless intracellular parasites. The phototrophic dinoflagellate Scrippsiella acuminata (Dinophyceae) can be infected by the microeukaryotic parasitoids Amoebophrya spp. (Syndiniales), some of which primarily target and digest the host nucleus. Early digestion of the nucleus at the beginning of the infection is expected to greatly impact the host metabolism, inducing the knockout of the organellar machineries that highly depend upon nuclear gene expression, such as the mitochondrial OXPHOS pathway and the plastid photosynthetic carbon fixation. However, previous studies have reported that chloroplasts remain functional in swimming host cells infected by Amoebophrya. We report here a multi-approach monitoring study of S. acuminata organelles over a complete infection cycle by nucleus-targeting Amoebophrya sp. strain A120. Our results show sustained and efficient photosystem II activity as a hallmark of functional chloroplast throughout the infection period despite the complete digestion of the host nucleus. We also report the importance played by light on parasite production, i.e., the amount of host biomass converted to parasite infective propagules. Using a differential gene expression analysis, we observed an apparent increase of all 3 mitochondrial and 9 out of the 11 plastidial genes involved in the electron transport chains (ETC) of the respiration pathways during the first stages of the infection. The longer resilience of organellar genes compared to those encoded by the nucleus suggests that both mitochondria and chloroplasts remain functional throughout most of the infection. This extended organelle functionality, along with higher parasite production under light conditions, suggests that host bioenergetic organelles likely benefit the parasite Amoebophrya sp. A120 and improve its fitness during the intracellular infective stage.

甲藻（Dinoflagellates）是浮游植物的重要组成类群，在诸多微生物食物网中扮演关键角色，其中多数类群为大量胞内寄生虫的宿主。光合自养型甲藻（phototrophic dinoflagellate）尖刺斯克莱普藻（Scrippsiella acuminata，甲藻纲Dinophyceae）可被微真核寄生生物（microeukaryotic parasitoids）变形虫孢属（Amoebophrya spp.，共生藻目Syndiniales）感染，部分该属寄生生物会优先靶向并降解宿主细胞核。感染初期对细胞核的快速消化，预计将严重干扰宿主代谢，敲除高度依赖核基因表达的细胞器系统，例如线粒体氧化磷酸化通路（mitochondrial OXPHOS pathway）与质体光合碳固定途径。然而既往研究显示，被变形虫孢属寄生的游动宿主细胞内，叶绿体仍维持功能活性。本研究针对靶向细胞核的变形虫孢属菌株A120，采用多手段监测完整感染周期内尖刺斯克莱普藻的细胞器状态。结果表明，尽管宿主细胞核被完全降解，但整个感染期间叶绿体始终保持功能活性，其标志性特征为持续高效的光系统II（photosystem II）活性。本研究同时证实光照对寄生虫增殖的重要影响，即宿主生物量向寄生虫感染性繁殖体的转化量。通过差异基因表达分析，我们观察到感染早期阶段，呼吸通路电子传递链（electron transport chains, ETC）相关的全部3个线粒体基因，以及11个质体基因中的9个，其表达量均出现明显上调。相较于核编码基因，细胞器基因的表达韧性更强，这提示线粒体与叶绿体在感染的大部分阶段均保持功能活性。这种延长的细胞器功能活性，配合光照条件下更高的寄生虫增殖效率，表明宿主生物能细胞器大概率可为变形虫孢属菌株A120提供支持，并提升其在胞内感染阶段的适合度。