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Group-specific functional patterns of mitochondrion-related organelles shed light on their multiple transitions from mitochondria in ciliated protists

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Abstract

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, Metopus laminarius (class Armophorea) and Plagiopyla cf. narasimhamurtii (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.

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Data availability

The 18S rDNA sequences were submitted into GenBank (accession numbers are SAMN29232525 for Metopus laminarius and SAMN29232526 for Plagiopyla cf. narasimhamurtii). And the single-cell transcriptomes and mass-culture transcriptomes of two species were submitted to GenBank under BioProject ID PRJNA851543.

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Acknowledgements

Many thanks to Dr. Alan Warren in Natural History Museum, UK for English improvement. Many thanks to Dr. Zhuo Shen in Sun Yat-sen University, China, for her help in species identification. Also, we thank Prof. Weibo Song in Ocean University of China, Dr. Lei Wu, Ms. Jiahui Xu, Ms. Zijing Quan, and Mr. Jian Wang in South China Normal University, for improving figures. This work is supported by the National Natural Science Foundation of China (Grant Number 32070406), Guangdong Basic and Applied Basic Research Foundation (Grant Number 2022A1515010773), and the Science and Technology Planning Project of Guangzhou (Grant Number 202102080168).

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  1. Zhicheng Chen and Jia Li contributed equally to this article.

Authors and Affiliations

  1. 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

    Zhicheng Chen, Jia Li, Miaoying Chen, Shilong Chen, Senru Li, Yanyan Wu & Zhenzhen Yi

  2. Department of Biochemistry, University of Cambridge, Cambridge, UK

    Dayana E. Salas-Leiva

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  1. Zhicheng Chen
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Contributions

ZY designed the experiments. ZC, JL, and MC completed the experiments. ZY and DS directed data analysis. ZC, JL, MC, SC, SL, and YW analyzed the data. ZC and JL drafted the manuscript. DS and ZY revised the manuscript. All authors edited and approved the final manuscript.

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Correspondence to Zhenzhen Yi.

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Edited by Jiamei Li.

Special topic: Ciliatology.

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Chen, Z., Li, J., Salas-Leiva, D.E. et al. Group-specific functional patterns of mitochondrion-related organelles shed light on their multiple transitions from mitochondria in ciliated protists. Mar Life Sci Technol 4, 609–623 (2022). https://doi.org/10.1007/s42995-022-00147-w

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