The marine ciliate Mesodinium rubrum is famous for its ability to acquire and exploit chloroplasts and other cell organelles from some cryptophyte algal species. We sequenced genomes and transcriptomes of free-swimming Teleaulax amphioxeia, as well as well-fed and starved M. rubrum in order to understand cellular processes upon sequestration under different prey and light conditions. From its prey, the ciliate acquires the ability to photosynthesize as well as the potential to metabolize several essential compounds including lysine, glycan, and vitamins that elucidate its specific prey dependency. M. rubrum does not express photosynthesis-related genes itself, but elicits considerable transcriptional control of the acquired cryptophyte organelles. This control is limited as light-dependent transcriptional changes found in free-swimming T. amphioxeia got lost after sequestration. We found strong transcriptional rewiring of the cryptophyte nucleus upon sequestration, where 35% of the T. amphioxeia genes were significantly differentially expressed within well-fed M. rubrum. Qualitatively, 68% of all genes expressed within well-fed M. rubrum originated from T. amphioxeia. Quantitatively, these genes contributed up to 48% to the global transcriptome in well-fed M. rubrum and down to 11% in starved M. rubrum. This tertiary endosymbiosis system functions for several weeks, when deprived of prey. After this point in time, the ciliate dies if not supplied with fresh prey cells. M. rubrum represents one evolutionary way of acquiring photosystems from its algal prey, and might represent a step on the evolutionary way towards a permanent tertiary endosymbiosis.

海洋纤毛虫Mesodinium rubrum以其从某些隐生藻类中获取和利用叶绿体和其他细胞器的能力而闻名。我们对自由游动的Teleaulax amphioxeia以及喂养充足和饥饿的M. rubrum的基因组和转录组进行了测序，以了解在不同猎物和光照条件下隔离时的细胞过程。从猎物身上，纤毛虫获得了光合作用的能力以及代谢多种必需化合物（包括赖氨酸、聚糖和维生素）的潜力，这些化合物阐明了其特定的猎物依赖性。M. rubrum本身不表达光合作用相关基因，但对获得的隐生植物细胞器产生相当大的转录控制。这种控制是有限的，因为在自由游动的T. amphioxeia中发现的光依赖性转录变化在隔离后丢失了。我们发现隐藻细胞核在隔离后发生了强烈的转录重新布线，其中 35% 的T. amphioxeia基因在喂养良好的红色 M. rubrum中显着差异表达。定性地，68% 在喂养良好的红色 M. rubrum中表达的所有基因都来自T. amphioxeia。从数量上讲，这些基因在喂养良好的红色小球藻中对全球转录组的贡献高达 48%在饥饿的红色 M. rubrum中降至 11% 。当猎物被剥夺时，这种三级内共生系统可以运行数周。在这个时间点之后，如果没有提供新鲜的猎物细胞，纤毛虫就会死亡。M. rubrum代表了一种从其藻类猎物中获取光系统的进化方式，并且可能代表了朝着永久性三级内共生的进化方式迈出的一步。