Chen Zhicheng, Li Jia, Salas-Leiva Dayana E, Chen Miaoying, Chen Shilong, Li Senru, Wu Yanyan, Yi Zhenzhen
Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory for Healthy and Safe Aquaculture, School of Life Science, South China Normal University, Guangzhou, 510631 China.
Department of Biochemistry, University of Cambridge, Cambridge, UK.
Mar Life Sci Technol. 2022 Nov 21;4(4):609-623. doi: 10.1007/s42995-022-00147-w. eCollection 2022 Nov.
Adaptations of ciliates to hypoxic environments have arisen independently several times. Studies on mitochondrion-related organelle (MRO) metabolisms from distinct anaerobic ciliate groups provide evidence for understanding the transitions from mitochondria to MROs within eukaryotes. To deepen our knowledge about the evolutionary patterns of ciliate anaerobiosis, mass-culture and single-cell transcriptomes of two anaerobic species, (class Armophorea) and cf. (class Plagiopylea), were sequenced and their MRO metabolic maps were compared. In addition, we carried out comparisons using publicly available predicted MRO proteomes from other ciliate classes (i.e., Armophorea, Litostomatea, Muranotrichea, Oligohymenophorea, Parablepharismea and Plagiopylea). We found that single-cell transcriptomes were similarly comparable to their mass-culture counterparts in predicting MRO metabolic pathways of ciliates. The patterns of the components of the MRO metabolic pathways might be divergent among anaerobic ciliates, even among closely related species. Notably, our findings indicate the existence of group-specific functional relics of electron transport chains (ETCs). Detailed group-specific ETC functional patterns are as follows: full oxidative phosphorylation in Oligohymenophorea and Muranotrichea; only electron-transfer machinery in Armophorea; either of these functional types in Parablepharismea; and ETC functional absence in Litostomatea and Plagiopylea. These findings suggest that adaptation of ciliates to anaerobic conditions is group-specific and has occurred multiple times. Our results also show the potential and the limitations of detecting ciliate MRO proteins using single-cell transcriptomes and improve the understanding of the multiple transitions from mitochondria to MROs within ciliates.
The online version contains supplementary material available at 10.1007/s42995-022-00147-w.
纤毛虫对缺氧环境的适应已经独立出现过几次。对不同厌氧纤毛虫类群中线粒体相关细胞器（MRO）代谢的研究为理解真核生物中线粒体向MRO的转变提供了证据。为了加深我们对纤毛虫厌氧进化模式的了解，对两种厌氧物种（臂形纲）和cf. （斜口纲）进行了大规模培养和单细胞转录组测序，并比较了它们的MRO代谢图谱。此外，我们还使用了来自其他纤毛虫类群（即臂形纲、毛口纲、膜口纲、寡膜纲、拟睫纲和斜口纲）的公开预测的MRO蛋白质组进行比较。我们发现，在预测纤毛虫的MRO代谢途径方面，单细胞转录组与其大规模培养的对应物具有相似的可比性。MRO代谢途径的组成模式在厌氧纤毛虫中可能存在差异，即使在亲缘关系密切的物种之间也是如此。值得注意的是，我们的研究结果表明存在特定群体的电子传递链（ETC）功能遗迹。详细的特定群体ETC功能模式如下：寡膜纲和膜口纲中存在完整的氧化磷酸化；臂形纲中只有电子传递机制；拟睫纲中存在上述任何一种功能类型；毛口纲和斜口纲中不存在ETC功能。这些发现表明纤毛虫对厌氧条件的适应是特定群体的，并且已经发生了多次。我们的结果还显示了使用单细胞转录组检测纤毛虫MRO蛋白的潜力和局限性，并增进了对纤毛虫内线粒体向MRO多次转变的理解。
在线版本包含可在10.1007/s42995-022-00147-w获取的补充材料。
