AiM  Vol.2 No.3 , September 2012
Photobiont Flexibility in Paramecium bursaria: Double and Triple Photobiont Co-Habitation
ABSTRACT
The green ciliate, Paramecium bursaria, has evolved a mutualistic relationship with endosymbiotic green algae (photobionts). Under culture conditions, photobionts are usually unified (to be single species) within each P. bursaria strain. In most cases, the algal partners are restricted to either Chlorella variabilis or Micractinium reisseri (Chlorellaceae, Trebouxiophyceae). Both species are characterized by particular physiology and atypical group I intron insertions, although they are morphologically indistinguishable from each other or from other Chlorella-related species. Both algae are exclusive species that are viable only within P. bursaria cells, and therefore their symbiotic relationship can be considered persistent. In a few cases, the other algal species have been reported as P. bursaria photobionts. Namely, P. bursaria have occasionally replaced their photobiont partner. This paper introduces some P. bursaria strains that maintain more than one species of algae for a long period. This situation prompts speculations about flexibility of host-photo-biont relationships, how P. bursaria replaced these photobionts, and the infection theory of the group I introns.

Cite this paper
R. Hoshina and Y. Fujiwara, "Photobiont Flexibility in Paramecium bursaria: Double and Triple Photobiont Co-Habitation," Advances in Microbiology, Vol. 2 No. 3, 2012, pp. 227-233. doi: 10.4236/aim.2012.23027.
References
[1]   Y. Kodama and M. Fujishima, “Infection of Paramecium bursaria by Symbiotic Chlorella Species,” In: M. Fujishima, Ed., Endosymbionts in Paramecium, Springer-Verlag, Berlin, 2009, pp. 31-55. doi:10.1007/978-3-540-92677-1_2

[2]   I. N. Gaponova, E. E. Andronov, A. V. Migunova, et al., “Genomic Dactyloscopy of Chlorella sp., Symbionts of Paramecium bursaria,” Protistology, Vol. 4, 2007, pp. 311-317.

[3]   R. Hoshina and N. Imamura, “Multiple Origins of the Symbioses in Paramecium bursaria,” Protist, Vol. 159, No. 1, 2008, pp. 53-63. doi:10.1016/j.protis.2007.08.002

[4]   R. Hoshina, M. Iwataki and N. Imamura, “Chlorella variabilis and Micractinium reisseri sp. nov. (Chlorellaceae, Trebouxiophyceae): Redescription of the Endosymbiotic Green Algae of Paramecium bursaria (PeniculiaOligohymenophorea) in the 120th Year,” Phycological Research, Vol. 58, No. 3, 2010, pp. 188-201. doi:10.1111/j.1440-1835.2010.00579.x

[5]   R. Hoshina, S. Kamako and N. Imamura, “Phylogenetic Position of Endosymbiotic Green Algae in Paramecium bursaria Ehrenberg from Japan,” Plant Biology, Vol. 6, No. 4, 2004, pp. 447-453. doi:10.1055/s-2004-820888

[6]   R. Hoshina, Y. Kato, S. Kamako and N. Imamura, “Genetic Evidence of ‘American’ and ‘European’ Type Symbiotic Algae of Paramecium bursaria Ehrenberg,” Plant Biology, Vol. 7, No. 5, 2005, pp. 526-532. doi:10.1055/s-2005-865912

[7]   K. V. Kvitko, A. V. Migunova, D. V. Karelov and M. Ju. Prokosheva, “Molecular Taxonomy of Virus-Sensitive Chlorella sp.—Symbionts of Paramecium bursaria,” Protistology, Vol. 2, 2001, pp. 96-104.

[8]   B. Linz, A. Linz, A. V. Migunova and K. V. Kvitko, “Correlation between Virus-Sensitivity and Isoenzyme Spectrum in Symbiotic Chlorella-Like Algae,” Protistology, Vol. 1, 1999, pp. 76-81.

[9]   T. Pr?schold, T. Darienko, P. C. Silva, W. Reisser and L. Krienitz, “The Systematics of Zoochlorella Revisited Employing an Integrative Approach,” Environmental Microbiology, Vol. 13, No. 2, 2011, pp. 350-364. doi:10.1111/j.1462-2920.2010.02333.x

[10]   M. Summerer, B. Sonntag and R. Sommaruga, “Ciliate-symbiont Specificity of Freshwater Endosymbiotic Chlorella (Trebouxiophyceae, Chlorophyta),” Journal of Phycology, Vol. 44, No. 1, 2008, pp. 77-84. doi:10.1111/j.1529-8817.2007.00455.x

[11]   K. Vorobyev, E. Andronov and M. Rautian et al., “An Atypical Chlorella Symbiont from Paramecium bursaria,” Protistology, Vol. 6, 2009, pp. 39-44.

[12]   A. E. Douglas and V. A. R. Huss, “On the Characteristics and Taxonomic Position of Symbiotic Chlorella,” Archives of Microbiology, Vol. 145, No. 1, 1986, pp. 80-84. doi:10.1007/BF00413031

[13]   S. Kamako, R. Hoshina, S. Ueno and N. Imamura, “Establishment of Axenic Endosymbiotic Strains of Japanese Paramecium bursaria and the Utilization of Carbohydrate and Nitrogen Compounds by the Isolated Algae,” European Journal of Protistology, Vol. 41, No. 3, 2005, pp. 193-202. doi:10.1016/j.ejop.2005.04.001

[14]   J. L. Van Etten, “Unusual Life Style of Giant Chlorella Viruses,” Annual Review of Genetics, Vol. 37, 2003, pp. 153-195. doi:10.1146/annurev.genet.37.110801.143915

[15]   J. L. Van Etten, L. C. Lane and R. H. Meints, “Viruses and Viruslike Particles of Eukaryotic Algae,” Microbiological Reviews, Vol. 55, 1991, pp. 586-620.

[16]   T. Yamada, H. Onimatsu and J. L. Van Etten, “Chlorella Viruses,” Advances in Virus Research, Vol. 66, 2006, pp. 293-336. doi:10.1016/S0065-3527(06)66006-5

[17]   R. W. Siegel, “Hereditary Endosymbiosis in Paramecium bursaria,” Experimental Cell Research, Vol. 19, No. 2, 1960, pp. 239-252. doi:10.1016/0014-4827(60)90005-7

[18]   T. R. Cech, “Ribozymes, the First 20 Years (Ribozyme Mechanisms and Folding),” Biochemical Society Transactions, Vol. 30, 2002, pp. 1162-1166. doi:10.1042/BST0301162

[19]   P. Haugen, D. M. Simon and D. Bhattacharya, “The Natural History of Group I Introns,” Trends in Genetics, Vol. 21, No. 2, 2005, pp. 111-119. doi:10.1016/j.tig.2004.12.007

[20]   J. J. Cannone, S. Subramanian, M. N. Schnare, et al., “The Comparative RNA Web (CRW) Site: An Online Database of Comparative Sequence and Structure Information for Ribosomal, Intron, and Other RNAs,” BMC Bioinformatics, Vol. 3, 2002, p. 2. doi:10.1186/1471-2105-3-2

[21]   R. Hoshina and N. Imamura, “Eu-Chlorella Large Subunit rDNA Sequences and Group I Introns in Ribosomal DNA of the Paramecian Symbiotic Alga NC64A,” Phycological Research, Vol. 56, No. 1, 2008, pp. 21-32. doi:10.1111/j.1440-1835.2008.00481.x

[22]   R. Hoshina and N. Imamura, “Phylogenetically Close Group I Introns with Different Positions among Paramecium bursaria Photobionts Imply a Primitive Stage of Intron Diversification,” Molecular Biology and Evolution, Vol. 26, No. 6, 2009, pp. 1309-1319. doi:10.1093/molbev/msp044

[23]   Z. Li and Y. Zhang, “Prediction the Secondary Structures and Tertiary Interaction of 211 Group I Inrons in IE Subgroup,” Nucleic Acid Research, Vol. 33, No. 7, 2005, pp. 2118-2128. doi:10.1093/nar/gki517

[24]   D. Bhattacharya, T. Friedland and S. Damberger, “Nuclear-Encoded rDNA Group I Introns: Origin and Phylogenetic Relationships of Insertion Site Lineages in the Green Algae,” Molecular Biology and Evolution, Vol. 13, No. 7, 1996, pp. 978-989. doi:10.1093/oxfordjournals.molbev.a025666

[25]   T. Friedl, A. Besendahl, P. Pfeiffer and D. Bhattacharya, “The Distribution of Group I Introns in Lichen Algae Suggests That Lichenization Facilitates Intron Lateral Transfer,” Molecular Phylogenetics and Evolution, Vol. 14, No. 3, 2000, pp. 342-352. doi:10.1006/mpev.1999.0711

[26]   H. Hosoya, K. Kimura, S. Matsuda et al., “Symbiotic Algae-Free Strains of Green Paramecium Paramecium bursaria Produced by Herbicide Paraquat,” Zoological Science, Vol. 12, No. 6, 1995, pp. 807-810. doi:10.2108/zsj.12.807

[27]   T. Nakayama, S. Watanabe, K. Mitsui, H. Uchida and I. Inouye, “The Phylogenetic Relationship between the Chlamydomonadales and Chlorococcales Inferred from 18S rDNA Sequence Data,” Phycological Research, Vol. 44, 1996, pp. 47-55. doi:10.1111/j.1440-1835.1996.tb00037.x

[28]   R. Hoshina, S. Hayashi and N. Imamura, “Intraspecific Genetic Divergence of Paramecium bursaria and Reconstruction of Paramecian Phylogenetic Tree,” Acta Protozoologica, Vol. 45, 2006, pp. 377-386.

[29]   M. Nakahara, S. Handa, S. Watanabe and H. Deguchi, “Choricystis minor as a New Symbiont of Simultaneous Two-Species Association with Paramecium bursaria and Implications for Its Phylogeny,” Symbiosis, Vol. 36, 2004, pp. 127-151.

[30]   Y. Kodama and M. Fujishima, “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, Vol. 160, No. 2, 2009, pp. 319-329. doi:10.1016/j.protis.2008.11.003

[31]   R. Hoshina and N. Imamura, “Origins of Algal Symbionts of Paramecium bursaria,” In: M. Fujishima, Ed., Endosymbionts in Paramecium, Springer-Verlag, Berlin Heidelberg, 2009, pp. 1-29. doi:10.1007/978-3-540-92677-1_1

[32]   C. Callieri and J. G. Stockner, “Freshwater Autotrophic Picoplankton: A Review,” Journal of Limnology, Vol. 61, 2002, pp. 1-14. doi:10.4081/jlimnol.2002.1

[33]   M. W. Fawley, K. P. Fawley and M. A. Buchheim, “Molecular Diversity among Communities of Freshwater Microchlorophytes,” Microbial Ecology, Vol. 48, No. 4, 2004, pp. 489-499. doi:10.1007/s00248-004-0214-4

[34]   A. E. Douglas, “Host Benefit and the Evolution of Specialization in Symbiosis,” Heredity, Vol. 81, 1998, pp. 599-603. doi:10.1046/j.1365-2540.1998.00455.x

 
 
Top