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The ciliate Paramecium bursaria allows budding of symbiotic Chlorella variabilis cells singly from the digestive vacuole membrane into the cytoplasm during algal reinfection

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Abstract

The ciliate Paramecium bursaria harbors several hundred symbiotic Chlorella spp. cells in the cytoplasm. Algal re-endosymbiosis can be artificially induced using alga-removed P. bursaria. During algal re-endosymbiosis, algae ingested into the host digestive vacuoles (DVs) avoid digestion by the host lysosomal enzymes and then escape into the cytoplasm by budding off of the DV membrane. The budded alga-enclosing DV membrane then differentiates into the symbiosome or perialgal vacuole (PV) membrane and is localized beneath the host cell cortex. In this study, we determined whether the PV membrane has the ability to recognize the symbiotic alga singly by eliminating other small microspheres in the same DV. To clarify the accuracy of the budding process, we mixed fluorescent-labeled microspheres of diameter 0.20 µm with isolated symbiotic algae during algal re-endosymbiosis. No fluorescence was observed from the PV membrane, as expected, and the budding DVs that enclosed both undigested and digested algae. Additionally, the algal re-endosymbiosis rate was significantly reduced in the presence of microspheres. These observations showed that the host P. bursaria allowed budding of the algae singly from the membranes of DVs without microspheres and this process required close contact between the DV membrane and the algal cell wall.

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Acknowledgements

P. bursaria strains were provided by the National BioResource Project Paramecium (Yamaguchi University, Japan). We would also like to thank Editage (www.editage.jp) for English language editing.

Funding

This work was supported by a Grant-in-Aid for Scientific Research (C) (Grant numbers 17K07513 and 20K06768) from the Japan Society for the Promotion of Science (JSPS) and the Institute for Fermentation (IFO; Osaka, Japan) to Y.K. The authors thank the faculty of Life and Environmental Sciences in Shimane University for the financial support in publishing this report.

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Authors and Affiliations

  1. Institute of Agricultural and Life Sciences, Academic Assembly, Shimane University, Matsue, Shimane, Japan

    Yuuki Kodama

  2. Department of Biological Science, Faculty of Life and Environmental Science, Shimane University, Matsue, Shimane, Japan

    Haruka Sumita

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  1. Yuuki Kodama
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Yuuki Kodama and Haruka Sumita conceived, designed, and performed the experiments. Yuuki Kodama wrote the manuscript.

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Correspondence to Yuuki Kodama.

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Kodama, Y., Sumita, H. The ciliate Paramecium bursaria allows budding of symbiotic Chlorella variabilis cells singly from the digestive vacuole membrane into the cytoplasm during algal reinfection. Protoplasma 259, 117–125 (2022). https://doi.org/10.1007/s00709-021-01645-x

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