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No mutual symbiosis following infection of algae-free Paramecium bursaria with symbiotic algae from Mayorella viridis

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Abstract

The amoeba, Mayorella viridis contains several hundred symbiotic green algae in its cytoplasm. Transmission electron microscopy revealed strong resemblance between symbiotic algae from M. viridis the symbiotic Chlorella sp. in the perialgal vacuoles of Paramecium bursaria and other ciliates. Although it is thought that the M. viridis and symbiotic algae could be model organisms for studying endosymbiosis between protists and green algae, few cell biological observations of the endosymbiosis between M. viridis and their symbiotic algae have been published. In this study, we characterized the specificity of endosymbiotic relationships between green algae and their hosts. Initially, we established stable cultures of M. viridis in KCM medium by feeding with Chlorogonium capillatum. Microscopic analyses showed that chloroplasts of symbiotic algae in M. viridis occupy approximately half of the algal cells, whereas those in P. bursaria occupy entire algal cells. The symbiotic algae in P. bursaria contain several small spherical vacuoles. The labeling of actin filaments using Acti-stain™ 488 Fluorescent Phalloidin revealed no relationship between host actin filaments and symbiotic algal localization, although the host mitochondria were localized around symbiotic algae. Symbiotic algae from M. viridis could infect algae-free P. bursaria but could not support P. bursaria growth without feeding, whereas the original symbiotic algae of P. bursaria supported its growth without feeding. These data indicated the specificity of endosymbiotic algae relationships in M. viridis and P. bursaria.

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References

  • Bonnet L, Brabet J, Comoy N, Guitard J (1981) Nouvelle données sur le thécamoebien filosia Amphitrema flavum (Archer 1877) Penard 1902. Protistologica 17:225–233

    Google Scholar 

  • Cann JP (1981) An ultrastructural study of Mayorella viridis (Leidy) (Amoebida: Paramoebidae), a Rhizopod containing zoochlorellae. Arch Protistenkd 124:353–360

    Article  Google Scholar 

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

    Google Scholar 

  • Esteban GF, Finlay BJ, Clarke KJ (2009) Sequestered organelles sustain aerobic microbial life in anoxic environments. Environ Microbiol 11:544–550

    Article  PubMed  Google Scholar 

  • Fujishima M, Kodama Y (2012) Endosymbionts in Paramecium. Europ J Protistol 48:124–137

    Article  Google Scholar 

  • 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 

  • Jeon KW (2004) Genetic and physiological interactions in the amoeba-bacteria symbiosis. Eukaryot Microbiol 51:502–508

    Article  Google Scholar 

  • Jeon KW, Lorch IJ (1967) Unusual intra-cellular bacterial infection in large, free-living amoebae. Exp Cell Res 48:236–240

    Article  CAS  PubMed  Google Scholar 

  • Karakashian SJ (1963) Growth of Paramecium bursaria as influenced by the presence of algal symbionts. Physiol Zool 36:52–68

    Article  Google Scholar 

  • Kies L (1984) Einzeller mit blaugrünen endosymbionten (Cyanellen) als objekte der symbioseforschung und modellorganismen für die evolution der chloroplasten. Biol Rdsch 22:145–157

    CAS  Google Scholar 

  • 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  PubMed  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Kodama Y, Fujishima M (2009a) 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  PubMed  Google Scholar 

  • Kodama Y, Fujishima M (2009b) 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  PubMed  Google Scholar 

  • 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  PubMed  Google Scholar 

  • Kodama Y, Fujishima M (2012) Cell division and density of symbiotic Chlorella variabilis of the ciliate Paramecium bursaria is controlled by the host’s nutritional conditions during early infection process. Environ Microbiol 14:2800–2811

    Article  PubMed  Google Scholar 

  • Kodama Y, Fujishima M (2016) Paramecium as a model organism for studies on primary and secondary endosymbioses. In: Witzany G, Nowacki M (eds) Biocommunication of ciliates. Springer International Publishing, Switzerland, pp 277–304

    Google Scholar 

  • Kodama Y, Suzuki H, Dohra H, Sugii M, Kitazume T, Yamaguchi K, Shigenobu S, Fujishima M (2014) Comparison of gene expression of Paramecium bursaria with and without Chlorella variabilis symbionts. BMC Genomics 15:183

    Article  PubMed  PubMed Central  Google Scholar 

  • Kudryashev M, Lepper S, Stanway R, Bohn S, Baumeister W, Cyrklaff M, Frischknecht F (2010) Positioning of large organelles by a membrane- associated cytoskeleton in Plasmodium sporozoites. Cell Microbiol 12:362–371

    Article  CAS  PubMed  Google Scholar 

  • Leidy J (1874) Notice of some freshwater and terrestrial Rhizopods. Proc Acad Natl Sci Phila 167:86–87

    Google Scholar 

  • Muscatine L, Lenhoff HM (1965) Symbiosis of Hydra and algae. II. Effects of limited food and starvation on growth of symbiotic and aposymbiotic Hydra. Biol Bull 129:316–328

    Article  Google Scholar 

  • 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 

  • Nishijima A, Fujishima M (2007) Chlorella vulgaris and C. sorokiniana cannot be maintained in Paramecium bursaria cell. Jpn. J Protozool 40:28–29

    Google Scholar 

  • Nishimura T, Yamaguchi H, Kodama Y, Nakayama T, Nakayama T, Inouye I (2009) Phylogenetic position of symbiotic chlorella (Trebouxiophyceae, Chlorophyta) of Mayorella Viridis (Amoebozoa) and its symbiotic manner. Meeting Abstract 271. Phycologia 48:94–95

    Google Scholar 

  • Pollard TD, Blanchoin L, Mullins RD (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29:545–576

    Article  CAS  PubMed  Google Scholar 

  • Reisser W (1984) The taxonomy of green algae endosymbiotic in ciliates and a sponge. Br Phycol J 19:309–318

    Article  Google Scholar 

  • Schaeffer AA (1926) Taxonomy of the amebas, with descriptions of thirty-nine new marine and freshwater species. Carnegie institution of Washington, Washington

    Google Scholar 

  • Schönborn W (1965) Untersuchungen über die Zoochlorellen-Symbiose der Hochmoor-Testaceen. Limnologica 3:173–176

    Google Scholar 

  • Sørensen MES, Cameron DD, Brockhurst MA, Wood AJ (2016) Metabolic constraints for a novel symbiosis. R Soc Open Sci 3:150708

    Article  PubMed  PubMed Central  Google Scholar 

  • Stiven AE (1965) The relationship between size, budding rate, and growth efficiency in three species of hydra. Res Popul Ecol 7:1–15

    Article  Google Scholar 

  • Takeda H, Sekiguchi T, Nunokawa S, Usuki I (1998) Species-specificity of Chlorella for establishment of symbiotic association with Paramecium bursaria. Does infectivity depend upon sugar components of the cell wall? Eur J Protistol 34:133–137

    Article  Google Scholar 

  • Tonooka Y, Watanabe T (2002) A natural strain of Paramecium bursaria lacking symbiotic algae. Eur J Protistol 38:55–58

    Article  Google Scholar 

  • 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 

  • Willumsen NBS (1982) Chaos zoochlorellae sp. nov. (Gymnamoebia, Amoebidae) from a Danish freshwater pond. J Nat Hist 16:803–813

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a Grant-in-Aid for Young Scientists (B) [Number 26840119] from the Japan Society for the Promotion of Science to Y. Kodama. The authors thank the faculty of Life and Environmental Science at Shimane University for financial supports and Enago (www.enago.jp) for the English language review.

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Yuuki Kodama conceived and designed the experiments, Shion Kawai and Sotarou Araki performed the experiments, and Yuuki Kodama wrote the paper.

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Correspondence to Yuuki Kodama.

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Shion Kawai, Sotarou Araki, and Yuuki Kodama declare that they have no conflict of interest.

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Kawai, S., Araki, S. & Kodama, Y. No mutual symbiosis following infection of algae-free Paramecium bursaria with symbiotic algae from Mayorella viridis . Symbiosis 75, 51–59 (2018). https://doi.org/10.1007/s13199-017-0517-0

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  • DOI: https://doi.org/10.1007/s13199-017-0517-0

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