FAQ
Jagiellonian University logo

ATP accumulation in early resting cyst formation towards cryptobiosis in Colpoda cucullus

Publication date: 22.08.2023

Acta Protozoologica, 2023, Volume 62, pp. 39 - 44

https://doi.org/10.4467/16890027AP.23.004.18421

Authors

,
Shuntaro Hakozaki
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan
All publications →
,
Hiroki Yamanobe
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan
All publications →
,
Kazuma Yabuki
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan
All publications →
,
Taiga Shimizu
Department of Chemistry and Biotechnology, Kochi University, Kochi 780-8520, Japan
National Institute of Technology Fukushima College, Iwaki, Fukushima Japan
All publications →
,
Takeru Saito
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan
All publications →
,
Ryota Saito
Department of Chemistry and Biotechnology, Kochi University, Kochi 780-8520, Japan
National Institute of Technology Fukushima College, Iwaki, Fukushima Japan
All publications →
,
Futoshi Suizu
Oncology Pathology, Department of Pathology and Host-Defense, Faculty of Medicine, Kagawa University, Takamatsu 761-0793, Japan
All publications →
,
Tomohiro Suzuki
Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya 321-8505, Japan
All publications →
Yoichiro Sogame
National Institute of Technology Fukushima College, Iwaki, Fukushima Japan
All publications →

Titles

ATP accumulation in early resting cyst formation towards cryptobiosis in Colpoda cucullus

Abstract

Resting cyst formation is a crucial process of cryptobiosis in protists. In colpodid ciliates, cyst formation is accompanied by large-scale morphological changes such as changes of cell shape, resorption of cilia, and formation of a cyst wall; additionally, the cell cycle is arrested. These changes provide acquired tolerance against environmental stresses. During cyst formation, mitochondrial membrane potential is reduced and the level of the ATP synthase beta chain is suppressed, strongly indicating that metabolism has ceased. Here, however, we show that ATP levels are elevated during the initial phases of encystment implying that metabolism may not be completely suppressed. This finding suggests another aspect of resting cyst formation that is not applicable to cryptobiosis.

References

Download references

Asami H., Ohtani Y., Iino R., Sogame Y., Matsuoka T. (2010) Behavior and Ca2+ –induced cell signaling for encystment of Colpoda cucullus. J. Protozool. Res. 20: 1–6

Benčaťová S., Tirjaková E. (2017) A study on resting cysts of an oxytrichid soil ciliate, rigidohymena quadrinucleata (Dragesco and Njine, 1971) Berger, 2011 (Ciliophora, Hypotrichia), including notes on its encystation and excystation process. Acta Protozool. 56: 77–91

Chen F., Xue Y., Pan N., Bhatti M. Z., Niu T., Chen J. (2018) New contribution to the morphology and molecular mechanism of Euplotes encysticus encystment. Sci. Rep. 8: 12795

Chen J., Gao X., Wang B., Chen F., Wu N., Zhang Y. (2014) Proteomic approach to reveal the proteins associated with encystment of the ciliate Euplotes encysticusPLoS One. 9: e97362

Clegg S. J. (2001) Cryptobiosis: a peculiar state of biological organization. Comp. Biochem. and Physiol. B128: 613–624

Corliss J. O., Esser S. C. (1974) Comments on the role of the cyst in the life cycle and survival of free-living protozoa. Trans. Am. Microsc. Soc. 93: 578–593

Funatani R., Kida A., Watoh A., Matsuoka T. (2010) Morphological events during resting cyst formation (encystment) in the ciliated protozoan Colpoda cucullus. Protistology. 6: 204–217

Gao X., Chen F., Niu T., Qu R., Chen J. (2015) Large-scale identification of encystment-related proteins and genes in Pseudourostyla cristata. Sci. Rep. 5: 11360

Gutiérrez J. C., Martín-González A., Matsusaka T. (1990) Towards a generalized model of encystment (cryptobiosis) in ciliates: a review and a hypothesis. BioSystems. 24: 17–24

Gutiérrez J. C., Callejas S., Borniquel S., Benítez L., Martín-González A. (2001) Ciliate cryptobiosis: A microbial strategy against environmental starvation. Int. Microbiol. 4: 151–157

Huen J., Kakihara Y., Ugwu F., Cheung K. L. Y., Ortega J., Houry W. A. (2010) Rvb1–Rvb2: Essential ATP-dependent helicases for critical complexes. Biochem. Cell Biol. 88: 29–40

Jiang C., Wei W., Yan G., Shi T., Miao W. (2019) Transcriptome analysis reveals the molecular mechanism of resting cyst formation in Colpoda aspera. J. Eukaryot. Microbiol. 66: 212–220

Keilin D. (1959) The problem of anabiosis or latent life: History and current concept. Proc. Roy. Soc. Lond. B. 150: 149–191

Li Q., Sun Q., Fan X., Wu N., Ni B., Gu F. (2017) The differentiation of cellular structure during encystment in the soil hypotrichous ciliate Australocirrus cf. australis (Protista, Ciliophora). Anim. Cells Syst. 21: 45–52

Li Y., Wang Y., Zhang S., Maurer-Alcalá X. X., Yan Y. (2022) How ciliated protists survive by cysts: Some key points during encystment and excystment. Front Microbiol. 13: 785502

Matsuoka K., Funadani R., Matsuoka T. (2017) Tolerance of Colpoda cucullus resting cysts to ultraviolet irradiation. J. Protozool. Res. 27: 1–7

Matsuoka T., Sogame Y., Nakamura R., Hasegawa Y., Arikawa M., Suizu F. (2020) Antifreeze water-rich dormant cysts of the terrestrial ciliate Colpoda cucullus Nag-1 at –65°C: Possible involvement of ultra-antifreeze polysaccharides. Acta Protozool. 59: 141–147.

Montalvo F. E., Reeves R. E., Warren L. G. (1971) Aerobic and anaerobic metabolism. Entamoeba histolytica. Exp. Paratistool30: 249–256

Müller H., Achilles-Day U. E. M., Day J. G. (2010) Tolerance of the resting cysts of Colpoda inflata (Ciliophora, Colpodea) and Meseres corlissi (Ciliophora, Spirotrichea) to desiccation and freezing. Europ J. Protistol. 46: 133–142

Nakamura R., Sogame Y., Arikawa M., Suizu F., Matsuoka T. (2020) Tolerance of Colpoda cucullus Nag-1 wet resting cysts to extreme pH (pH 1 and 13): Implications of less permeability of the cyst membrane to H+ and OH–. J. Protozool. Res. 30: 38–46

Pan N., Niu T., Bhatti M. Z., Zhang H., Fan X., Ni B., Chen J. (2019) Novel insights into molecular mechanisms of Pseudourostyla cristata encystment using comparative transcriptomics. Sci. Rep. 9:19109

Pan N., Bhatti M. Z., Zhang W., Ni B., Fan X., Chen J.(2021) Transcriptome analysis reveals the encystment-related lncRNA expression profile and coexpressed mRNAs in Pseudourostyla cristata. Sci. Rep. 11: 827410

Saito R., Koizumi R., Sakai T., Shimizu T., Ono T., Sogame Y. (2020a) Gamma radiation tolerance and protein carbonylation caused by irradiation of resting cysts in the free-living ciliated protist Colpoda cucullus. Acta Protozool. 59: 67–75

Saito R., Sakai T., Koizumi R., Shimizu T., Ono T., Hakozaki S., Kobayashi S., Saito Y., Sogame Y. (2020b). Comparison of the morphology and viability of gamma irradiated vegetative cells, wet cysts, and dry cysts of the soil ciliate Colpoda cucullus. J. Protozool. Res. 30: 20–30

Saito T., Yabuki K., Saito Y., Yamanobe H., Saito R., Hakozaki S., Amano H., Ogawa Y., Sogame Y. (2023). Comparison of the relative tolerance of Colpoda resting cysts and vegetative cells to electrostatic exposure. J. Protozool. Res. 33: 32–42

Sogame Y., Kida A., Matsuoka T. (2011) Possible involvement of endocyst in tolerance of the resting cyst of Colpoda cucullus against HCl. Afr. J. Microbiol. Res. 5: 4316–4320

Sogame Y., Kojima K., Takeshita T., Kinoshita E., Matsuoka T. (2012) EF-1αand mitochondrial ATP synthase βchain: Alteration of their expression in encystment-induced Colpoda cucullus. J. Euk. Microbiol. 59: 401–406

Sogame Y., Kojima K., Takeshita T., Kinoshita E., Matsuoka T. (2014) Identification of differentially expressed water-insoluble proteins in the encystment process of Colpoda cucullus by two-dimensional electrophoresis and LC-MS/MS analysis. J. Eukariot. Microbiol. 61: 51–60

Sogame Y., Saito R., Koizumi R., Shimizu T., Ono T. (2019) Evidence of stress recovery in free-living ciliate Colpoda cucullus: The repair capability of resting cysts to damage caused by gamma irradiation. Acta Protozool. 58: 25–29

Sogame Y., Kojima K., Takeshita T., Kikuchi S., Shimada Y., Nakamura R., Arikawa M., Miyata S., Kinoshita S., Suizu F., Matsuoka T. (2020) Analysis of water-soluble proteins by twodimensional electrophoresis in the encystment process of Colpoda cucullus Nag-1 and cytoskeletal dynamics. Acta Protozool. 59: 107–120

Taylor C. V., Strickland A. G. R. (1936) Effects of high vacua and extreme temperatures on the cysts of Colpoda cucullus. Physiol. Zool. 19: 15–26

Uspenskaya Z. I., Lozia-Lozinsky L. K. (1979) Antigen rearrangements in Colpoda maupasi cells after freezing at –196°C, and after shortwave ultraviolet irradiation. Cryobiology. 16: 542–549 44 S. Hakozaki et al.

Verni F., Rosati G. (2011) Resting cysts: a survival strategy in protozoa ciliophoran. Ital. J. Zool. 78: 134–145

Yamane S., Watanabe M., Funadani R., Miyazaki R., Hasegawa Y., Arikawa M., Suizu F., Matsuoka K., Matsuoka T. (2020) Tolerance of Colpoda cucullus Nag-1 resting cysts and presumed structure for protection against UV light. Acta Protozool. 59: 55–60

Information

Information: Acta Protozoologica, 2023, Volume 62, pp. 39 - 44

Article type: Original article

Authors

Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan

Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan

Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan

Department of Chemistry and Biotechnology, Kochi University, Kochi 780-8520, Japan

National Institute of Technology Fukushima College, Iwaki, Fukushima Japan

Department of Applied Chemistry and Biochemistry, National Institute of Technology, Fukushima College, Iwaki 970-8034, Japan

Department of Chemistry and Biotechnology, Kochi University, Kochi 780-8520, Japan

National Institute of Technology Fukushima College, Iwaki, Fukushima Japan

Oncology Pathology, Department of Pathology and Host-Defense, Faculty of Medicine, Kagawa University, Takamatsu 761-0793, Japan

Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya 321-8505, Japan

National Institute of Technology Fukushima College, Iwaki, Fukushima Japan

Published at: 22.08.2023

Received at: 31.05.2023

Accepted at: 24.08.2023

Article status: Open

Licence: CC BY  licence icon

Percentage share of authors:

Shuntaro Hakozaki (Author) - 11.11%
Hiroki Yamanobe (Author) - 11.11%
Kazuma Yabuki (Author) - 11.11%
Taiga Shimizu (Author) - 11.11%
Takeru Saito (Author) - 11.11%
Ryota Saito (Author) - 11.11%
Futoshi Suizu (Author) - 11.11%
Tomohiro Suzuki (Author) - 11.11%
Yoichiro Sogame (Author) - 11.11%

Article corrections:

-

Publication languages:

English