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Trichocyst Ribbons of a Cryptomonads Are Constituted of Homologs of R-Body Proteins Produced by the Intracellular Parasitic Bacterium of Paramecium

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Abstract

Trichocysts are ejectile organelles found in cryptomonads, dinoflagellates, and peniculine ciliates. The fine structure of trichocysts differs considerably among lineages, and their evolutionary relationships are unclear. The biochemical makeup of the trichocyst constituents has been studied in the ciliate Paramecium, but there have been no investigations of cryptomonads and dinoflagellates. Furthermore, morphological similarity between the contents of cryptomonad trichocysts and the R-bodies of the endosymbiotic bacteria of Paramecium has been reported. In this study, we identified the proteins of the trichocyst constituents in a red cryptomonad, Pyrenomonas helgolandii, and found their closest relationships to be with rebB that comprises the R-bodies of Caedibacter taeniospiralis (gammaproteobacteria), which is an endosymbiont of Paramecium. In addition, the biochemical makeups of the trichocysts are entirely different between cryptomonads and peniculine ciliates, and therefore, cryptomonad trichocysts have an evolutionary origin independent from the peniculine ciliate trichocysts.

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References

  • Akiba N, Aono T, Toyazaki H, Sato S, Oyaizu H (2010) phrR-like gene praR of Azorhizobium caulinodas ORS571 is essential for symbiosis with Sesbania rostrata and is involved in expression of reb genes. Appl Environ Microbiol 76:3475–3485

    Article  PubMed  CAS  Google Scholar 

  • Anderson E (1962) A cytological study of Chilomonas paramecium with particular reference to the so-called trichocysts. J Euk Microbiol 9:380–395

    Article  CAS  Google Scholar 

  • Anderson TF, Preer JR, Preer LB, Bray M (1964) Studies in killing particles from Paramecium: the structure of refractile bodies from kappa particles. J Microscop 3:395–402

    Google Scholar 

  • Beier CL, Horn M, Michel R, Schweikert M, Görtz H, Wagner M (2002) The genus Caedibacter comprise endosymbionts of Paramecium spp. related to the Richettsiales (alphaproteobacteria) and to Francisella tularensis (Gammaproteobacteria). Appl Environ Microbiol 68:6043–6050

    Article  PubMed  CAS  Google Scholar 

  • Bourrelly P (1970) Les Algues d’Eau Douce. Initiation à la systématique. Tome III: Les Agues Bleues et Rouges, les Eugléniens, Peridiniens et Cryptomonadines. Boubée N (ed), Paris

  • Chou PY, Fasman GD (1974a) Conformational parameters for amino acids in helical, β-sheet, and random coil regions calculated from proteins. Biochemistry 13:211–222

    Article  PubMed  CAS  Google Scholar 

  • Chou PY, Fasman GD (1974b) Prediction of protein conformation. Biochemistry 13:222–245

    Article  PubMed  CAS  Google Scholar 

  • Clay BL, Kugrens P (1999) Systematics of the enigmatic kathablepharids, including EM characterization of the type species, Kathablepharis phoneikoston, and new observation on K. remigera comb. nov. Protist 150:43–59

    Article  PubMed  CAS  Google Scholar 

  • Dilts JA, Quackenbush RL (1986) A mutation in the R body-coding sequence destroys expression of the killer trait in P. tetraurelia. Science 232:641–643

    Article  PubMed  CAS  Google Scholar 

  • Doolittle RF (1981) Similar amino acid sequences: chance or common ancestry. Science 214:149–159

    Article  PubMed  CAS  Google Scholar 

  • Dragesco J (1951) Sur la structure des trichocystes du Flagellés Cryptomonadine Chilomonas paramecium. Bull Microsc Appl 1:172–175

    Google Scholar 

  • Fusté MC, Simon-Pujol MD, Marques AM, Guinea J, Congregado F (1986) Isolation of a new free-living bacterium containing R-bodies. J Gen Microbiol 132:2801–2805

    Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Barioch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, NJ, pp 571–607

    Chapter  Google Scholar 

  • Gautier MC, Garreau de Loubresse N, Madeddu L, Sperling L (1994) Evidence for defects in membrane traffic in Paramecium secretory mutants unable to produce functional storage granules. J Cell Biol 124:893–902

    Article  PubMed  CAS  Google Scholar 

  • Gautier MC, Sperling L, Madeddu L (1996) Cloning and sequence analysis of genes coding for Paramecium secretory granule (trichocyst) proteins. A unique protein fold for a family of polypeptides with different primary structures. J Biol Chem 271:10247–10255

    Article  PubMed  CAS  Google Scholar 

  • Hausmann K (1978) Extrusive organelles in protists. Int Rev Cytol 52:197–276

    Article  PubMed  CAS  Google Scholar 

  • Heruth DP, Pond FR, Dilts JA, Quackenbush RL (1994) Characterization of genetic determination for R body synthesis and assembly in Caedibacter taeniospiralis 47 and 116. J Bacteriol 176:3559–3567

    PubMed  CAS  Google Scholar 

  • Horst MN, Basha SMM, Baumbach GA, Mansfield EH, Roberts RM (1980) Alkaline urea solubilizaiton, two-dimensional electrophoresis and lectin staining of mammalian cell plasma membrane and plant seed proteins. Anal Biochem 102:399–408

    Article  PubMed  CAS  Google Scholar 

  • Hovasse R (1965) Trichocystes corps trichocystoides, cnidocystes et colloblastes. Protoplasmatologia 3:1–57

    Google Scholar 

  • Hovasse R, Mignot JP, Joyon L (1967) Nouvelles observations sur les trichocystes des Cryptomonadines et les “R dodies” des particules Kappa de Paramecium aurelia killer. Protistologica 3:241–255

    Google Scholar 

  • Jeblick J, Kusch J (2005) Sequence, transcription activity, and evolutionary origin of the R-body coding plasmid pKAP298 from the intracellular parasitic bacterium. J Mol Evol 60:164–173

    Article  PubMed  CAS  Google Scholar 

  • Kanabrocki JA, Quackenbush BL, Pond FR (1986) Organization and expression of genetic determinants for synthesis and assembly of type 51 R bodies. J Bacteriol 168:40–48

    PubMed  CAS  Google Scholar 

  • Kugrens P, Lee RE, Corliss JO (1994) Ultrastructure, biogenesis, and function of extrusive organelles in selected non-ciliate protist. Protoplasma 181:164–190

    Article  Google Scholar 

  • Lalucat JO, Meyer O, Meyer F, Pares R, Schlegel HG (1979) R bodies in newly isolated free-living hydrogen-oxidizing bacteria. Arch Microbiol 121:9–15

    Article  CAS  Google Scholar 

  • Leander BS, Keeling PJ (2003) Morphostasis in alveoliate evolution. Trends Ecol Evol 18:395–402

    Article  Google Scholar 

  • Mignot JP (1965) Étude ultrastructurale de Cyathomonas truncata From. (Flagellé cryptomonadine). J Microsc 4:239–252

    Google Scholar 

  • Morrall S, Greenwood AD (1980) A comparison of the periodic substructure of the trichocysts of the Cryptophyceae and Prasinophyceae. BioSystems 12:71–83

    Article  PubMed  CAS  Google Scholar 

  • Okamoto N, Inouye I (2005) The katablepharids are a distant sister group of the Cryptophyta: a proposal for Katablepharidophyta divisio nova/Kathablepharida phylum novum based on SSU rDNA and beta-tubulin phylogeny. Protist 156:163–179

    Article  PubMed  CAS  Google Scholar 

  • Pond FR, Gibson I, Llucat J, Quackenbush RL (1989) R-body-producing bacteria. Microbiol Rev 53:25–67

    PubMed  CAS  Google Scholar 

  • Preer JR, Preer LB, Jurand A (1974) Kappa and other endosymbionts in Paramecium aurelia. Bacteriol Rev 38:113–163

    PubMed  CAS  Google Scholar 

  • Provasoli L (1966) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Proceedings of the US-Japan conference held at Hakone. Jpn Soc Plant Physiol, Tokyo, pp 63–75

  • Quackenbush RL (1978) Genetic relationships among bacterial endosymbionts of Paramecium aurelia: deoxyribonucleotide sequence relationships among members of Caedibacter. J Gen Microbiol 108:181–187

    CAS  Google Scholar 

  • Quackenbush RL, Burbach JA (1983) Cloning and expression of DNA sequences associated with the killer trait of Paramecium tetraurelia stock 47. Proc Natl Acad Sci USA 80:250–254

    Article  PubMed  CAS  Google Scholar 

  • Quakenbush RL (1987) The killer trait. In: Görtz HD (ed) Current topics in Paramecium research. Springer, Berlin, pp 406–418

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Rhiel E, Westermann M (2011) Isolation, purification and some ultrastructural details of discharged ejectisomes of cryptophytes. Protoplasma 249(1):107–115

    Article  PubMed  Google Scholar 

  • Schägger H, Jagow G (1987) Tricine–sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–376

    Article  PubMed  Google Scholar 

  • Schuster FL (1968) The gullet and trichocysts of Cyathomonas truncata. Exp Cell Res 49:277–284

    Article  PubMed  CAS  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–42

    Article  PubMed  CAS  Google Scholar 

  • Tindall SH, Devito LD, Nelson DL (1989) Biochemical characterization of the proteins of Paramecium secretory granules. J Cell Sci 92:441–447

    PubMed  CAS  Google Scholar 

  • Wehrmeyer W (1970) Struktur, Entwicklung und abbau von trichocysten in Cryptomonas und Hemiselmis (Cryptophyceae). Plotoplasma 70:295–315

    Article  Google Scholar 

  • Wells B, Horne RW (1983) The ultrastructure of Pseudomonas avenae. II. Intracellular refractile (R-body) structure. Micron Microsc Acta 14:329–344

    Article  Google Scholar 

  • Yamagishi T, Kawai H (2011) Cortical F-actin reorganization and a contractile ring-like structure found during the cell cycle in the red cryptomonad, Pyrenomonas helgolandii. J Phycol 47:1121–1130

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr Eric C. Henry for his valuable comments on the manuscript. A part of this study was supported by the scientific research grant of the Japan Society for Promotion of Sciences to H. K. (Project Numbers: 18370037, 22370034).

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  1. Kobe University Research Center for Inland Seas, Kobe, 657-8501, Japan

    Takahiro Yamagishi, Atsushi Kai & Hiroshi Kawai

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  1. Takahiro Yamagishi
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  2. Atsushi Kai
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  3. Hiroshi Kawai
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Correspondence to Takahiro Yamagishi.

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Yamagishi, T., Kai, A. & Kawai, H. Trichocyst Ribbons of a Cryptomonads Are Constituted of Homologs of R-Body Proteins Produced by the Intracellular Parasitic Bacterium of Paramecium . J Mol Evol 74, 147–157 (2012). https://doi.org/10.1007/s00239-012-9495-2

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