Skip to main content
Log in

Autolysis of Chlorella variabilis in Starving Paramecium bursaria Help the Host Cell Survive Against Starvation Stress

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The endosymbiosis between Paramecium bursaria and Chlorella spp. is mutualistic. Symbiotic algae localize beneath the host Paramecium cell cortex compete for their attachment sites with preexisting organelle trichocysts. To examine the relationship between P. bursaria trichocysts and their symbiotic algae, algae-bearing or alga-free P. bursaria were starved for several days and the changes in the number of Chlorella sp. and presence or absence of trichocysts were evaluated. We conducted an indirect immunofluorescence microscopy with an anti-trichocyst monoclonal antibody against P. bursaria cells. Indirect immunofluorescence microscopy demonstrated that under starvation and darkness conditions, the immunofluorescence of trichocysts in alga-free P. bursaria decreased much faster than that in the normal algae-bearing P. bursaria. In the latter case, our observations proposed the possibility that the nutrition obtained from symbiotic algal digestion may promote trichocysts synthesis. This algal digestion mechanism may permit host P. bursaria cells to survive for a longer time under starvation condition. To the best of our knowledge, this may be a new benefit that host P. bursaria gain from harboring symbiotic algae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Goetsch W (1924) Die symbiose der süsswasser-hydroiden und ihre künstliche beeinflussung. Z Morp u Okol Tiere 1:660–751

    Article  Google Scholar 

  2. Lee JJ, Soldo AT, Reisser W, Lee MJ, Jeon KW, Görtz HD (1985) The extent of algal and bacterial Endosymbioses in Protozoa. J Protozool 32:391–403

    Article  CAS  Google Scholar 

  3. Van Tright H (1919) A contribution to the physiology of the freshwater sponges (Spongillidae). Tijdschr Ned Dierkd 2:1–20

    Google Scholar 

  4. Harumoto T, Miyake A (1991) Defensive function of trichocysts in Paramecium. J Exp Zool 260:84–92

    Article  Google Scholar 

  5. Brown JA, Nielsen PJ (1974) Transfer of photosynthetically produced carbohydrate from endosymbiotic Chlorellae to Paramecium bursaria. J Protozool 21:569–570

    Article  CAS  Google Scholar 

  6. Hohman TC, McNeil PL, Muscatine L (1982) Phagosome–lysosome fusion inhibited by algal symbionts of Hydra viridis. J Cell Biol 94:56–63

    Article  CAS  Google Scholar 

  7. Muscatine L, Karakashian SJ, Karakashian MW (1967) Soluble extracellular products of algae symbiotic with a ciliate, a sponge and a mutant hydra. Comp Biochem Physiol 20:1–12

    Article  CAS  Google Scholar 

  8. Albers D, Reisser W, Wiessner W (1982) Studies of the nitrogen supply of endosymbiotic chlorellae in green Paramecium bursaria. Plant Sci Lett 25:85–90

    Article  CAS  Google Scholar 

  9. Albers D, Wiessner W (1985) Nitrogen nutrition of endosymbiotic Chlorella spec. Endocytobio Cell Res 2:55–64

    Google Scholar 

  10. Reisser W (1976) The metabolic interactions between Paramecium bursaria Ehrbg. and Chlorella spec. in the Paramecium bursaria−symbiosis. I. The nitrogen and the carbon metabolism. Arc Microbiol 107:357–360

    Article  CAS  Google Scholar 

  11. Reisser W (1980) The metabolic interactions between Paramecium bursaria Ehrbg. and Chlorella spec. in the Paramecium bursaria-symbiosis. III. The influence of different CO2-concentrations and of glucose on the photosynthetic and respiratory capacity of the symbiotic unit. Arc Microbiol 125:291–293

    Article  CAS  Google Scholar 

  12. Kodama Y, Fujishima M (2005) Symbiotic Chlorella sp. of the ciliate Paramecium bursaria do not prevent acidification and lysosomal fusion of host digestive vacuoles during infection. Protoplasma 225:191–203

    Article  Google Scholar 

  13. Siegel R, Karakashian SJ (1959) Dissociation and restoration of endocellular symbiosis in Paramecium bursaria. Anat Rec 134:639

    Google Scholar 

  14. He M, Wang J, Fan X, Liu X, Shi W, Huang N, Zhao F, Miao M (2019) Genetic basis for the establishment of endosymbiosis in Paramecium. ISME J 13:1360–1369

    Article  CAS  Google Scholar 

  15. Gu F, Chen L, Ni B, Zhang X (2002) A comparative study on the electron microscopic enzymo-cytochemistry of Paramecium bursaria from light and dark cultures. Europ J Protistol 38:267–278

    Article  Google Scholar 

  16. Karakashian SJ, Rudzinska MA (1981) Inhibition of lysosomal fusion with symbiont-containing vacuoles in Paramecium bursaria. Exp Cell Res 131:387–393

    Article  CAS  Google Scholar 

  17. Kodama Y, Fujishima M (2007) Infectivity of Chlorella species for the ciliate Paramecium bursaria is not based on sugar residues of their cell wall components, but on their ability to localize beneath the host cell membrane after escaping from the host digestive vacuole in the early infection process. Protoplasma 231:55–63

    Article  CAS  Google Scholar 

  18. Kodama Y, Fujishima M (2008) Cycloheximide induces synchronous swelling of perialgal vacuoles enclosing symbiotic Chlorella vulgaris and digestion of the algae in the ciliate Paramecium bursaria. Protist 159:483–494

    Article  Google Scholar 

  19. Miyake A, Harumoto T, Salvi B, Rivola V (1989) Defensive function of extrusomes, pigment granules in Blepharisma and trichocysts in Paramecium, against a carnivorous ciliate Dileptus. J Protozool 36:28A

    Google Scholar 

  20. Sugibayashi R, Harumoto T (2000) Defensive function of trichocysts in Paramecium tetraurelia against heterotrich ciliate Climacostomum virens. Europ J Protistol 36:415–422

    Article  Google Scholar 

  21. Sugibayashi R, Harumoto T (1998) Zool Sci 15(Suppl):25

    Google Scholar 

  22. Kodama Y, Fujishima M (2009) Localization of perialgal vacuoles beneath the host cell surface is not a prerequisite phenomenon for protection from the host's lysosomal fusion in the ciliate Paramecium bursaria. Protist 160:319–329

    Article  Google Scholar 

  23. Kodama Y, Fujishima M (2011) Endosymbiosis of Chlorella species to the ciliate Paramecium bursaria alters the distribution of the host's trichocysts beneath the host cell cortex. Protoplasma 248:325–337

    Article  Google Scholar 

  24. Omura G, Suzaki T (2003) Changes in trichocysts during re-infection of white Paramecium bursaria by Chlorella. Jpn J Protozool 36:69–70 (in Japanese)

    Google Scholar 

  25. Kodama Y, Fujishima M (2009) Timing of perialgal vacuole membrane differentiation from digestive vacuole membrane in infection of symbiotic algae Chlorella vulgaris of the ciliate Paramecium bursaria. Protist 160:65–74

    Article  Google Scholar 

  26. Tsukii Y, Harumoto T, Yazaki K (1995) Evidence for a viral macronuclear endosymbiont in Paramecium caudatum. J Euk Microbiol 42:109–115

    Article  Google Scholar 

  27. Dryl S (1959) Antigenic transformation in Paramecium aurelia after homologous antiserum treatment during autogamy and conjugation. J Protozool 6:25

    Google Scholar 

  28. Fujishima M, Nagahara K, Kojima Y (1990) Changes in morphology, buoyant density and protein composition in differentiation from the reproductive short form to the infectious long form of Holospora obtusa, a macronucleus-specific symbiont of the ciliate Paramecium caudatum. Zool Sci 7:849–860

    CAS  Google Scholar 

  29. Berger J (1980) Feeding behaviour of Didinium nasutum on Paramecium bursaria with Normal or Apochlorotic Zoochlorellae. J Gen Microbiol 118:397–404

    Google Scholar 

  30. Pollack S (1974) Mutations affecting the trichocysts in Paramecium aurelia. I. Morphology and description of the mutants. J Protozool 21:352–362

    Article  CAS  Google Scholar 

  31. Altermatt F, Fronhofer EA, Garnier A et al (2015) Big answers from small worlds: a user's guide for protist microcosms as a model system in ecology and evolution. Methods Ecol Evol 6:218–231

    Article  Google Scholar 

Download references

Acknowledgements

We thank Professor Masahiro Fujishima (Yamaguchi University, Japan) for giving us the valuable monoclonal antibody against trichocysts. This work was supported by a Grant-in-Aid for Scientific Research (C) (No. 17 K07513) from the Japan Society for the Promotion of Science (JSPS) and by the Institute for Fermentation (IFO), Osaka, Japan, to Y.K. The authors thank the faculty of Life and Environmental Sciences in Shimane University for financial supports in publishing this report and we would like to thank Editage (www.editage.jp) for English language editing.

Author information

Authors and Affiliations

Authors

Contributions

Yuuki Kodama conceived and designed the experiments. Yuuki Kodama and Shoya Miyazaki performed the experiments. Yuuki Kodama wrote the manuscript.

Corresponding author

Correspondence to Yuuki Kodama.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kodama, Y., Miyazaki, S. Autolysis of Chlorella variabilis in Starving Paramecium bursaria Help the Host Cell Survive Against Starvation Stress. Curr Microbiol 78, 558–565 (2021). https://doi.org/10.1007/s00284-020-02304-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-02304-9

Keywords

Navigation