Endobacteria in the diatom Pinnularia (Bacillariophyceae). I. "Scattered ct-nucleoids" explained: DAPI-DNA complexes stem from exoplastidial bacteria boring into the chloroplasts

Journal of Phycology

Volumn 39, Issue 1, 2003, Pages 122-138

  Schmid, Anna Maria M ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

Author keywords

Chloroplasts; Diatoms; DNA; Endobacteria; Endoplasmic reticulum; Pinnularia; Pyrenoids; RUBISCO; Symbiosis; Trachyneis

Indexed keywords

CYTOLOGY; DIATOM; ENDOSYMBIONT;

ALGAE; BACILLARIOPHYCEAE; BACILLARIOPHYTA; NEGIBACTERIA; PINNULARIA; PINNULARIA NOBILIS; RHODOPHYTA; TRACHYNEIS; TRITICUM AESTIVUM;

EID: 0037327222     PISSN: 00223646     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1529-8817.2003.02084.x     Document Type: Article

References (69)

1. Belcher, J. H. 1969. Some remarks on Mallomonas papillosa Harris and Bradley and M. calceolus Bradley. Nova Hedw. 18:257-70.
2. Cavalier-Smith, T. 1989. The kingdom chromista. In Green, J. C., Leadbeater, B. S. C. & Diver, W. I. [Eds.] The Chromophyte Algae: Problems and Perspectives. Systematics Association Special Vol. 38. Clarendon Press, Oxford, pp. 381-407.
3. Cavalier-Smith, T. 2000. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5:174-82.
4. Cleveland, L. R. & Grimstone, A. V. 1964. The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Proc. R. Soc. Lond. B 159:668-86.
5. Coleman, A. W. 1985. Diversity of plastid DNA configuration among classes of eucaryote algae. J. Phycol. 21:1-16.
6. Crawford, R. M. 1973. The protoplasmic ultrastructure of the vegetative cell of Melosira varians C. A. Agardh. J. Phycol. 9:50-61.
7. Denecke, J. 1996. Mechanisms controlling function, identity and integrity of the plant endoplasmic reticulum. In Smallwood, M., Knox, J. P. & Bowles, D.J. [Eds.] Membranes: Specialized Functions in Plants. Bios Scientific Publishers Ltd., Oxford, pp. 367-82.
8. Doddema, H.J. & van der Veer, J. 1983. Ochromonas monicis sp. nov., a particle feeder with bacterial endosymbionts. Cryptog. Algol. 4:89-97.
9. Dodge, J. D. 1973. The Fine Structure of Algal Cells. Academic Press, London, 261 pp.
10. Drum, R. W., Pankratz, S. & Stoermer, E. F. 1966. Electron microscopy of diatom cells. In Helmcke, J. G. & Krieger, W. [Eds.] Diatomeenschalen im elektronenmikroskopischen Bild. Cramer, Lehre, Germany, Teil VI, plates 514-613.
11. Edgar, L. A. & Zavortink, M. 1983. The mechanism of diatom locomotion. II. Identification of actin. Proc. R. Soc. Lond. B 218:345-8.
12. Geitler, L. 1932. Der Formwechsel der pennaten Diatomeen. Arch. Protistenk. 76:1-226.
13. Geitler, L. 1937a. Chromatophor, Chondriosomen, Plasmabewegung und Kernbau von Pinnularia nobilis und einigen anderen Diatomeen nach Lebendbeobachtungen. Protoplasma 27:534-43.
14. Geitler, L. 1937b. Der Chromatophorenbau der Diatomeen Gyrosigma attenuatum und Nitzschia sigmoidea. Beih. Bot. Centralbl. 57:425-31.
15. Gibbs, S. P. 1981. The chloroplast endoplasmic reticulum: structure, function and evolutionary significance. Int. Rev. Cytol. 72:49-99.
16. Gibbs, S. P. 1990. The evolution of algal chloroplasts. In Wiessner, W., Robinson, D. G. & Starr, R. C. [Eds.] Experimental Phycology: Cell Walls and Surfaces, Reproduction and Photosynthesis. Springer-Verlag, Berlin, Heidelberg, pp. 145-57.
17. Gschöpf, O. 1952. Das Problem der Doppelplättchen und ihnen homologer Gebilde bei den Diatomeen. Öst. Bot. Z. 99:1-36.
18. Harper, M. A. 1976. Migration rhythm of the benthic diatom Pinnularia viridis on pond silt. N. Z. J. Mar. Freshw. Res. 10:381-4.
19. Hess, M. W. 1990. Spurr resin affects the ultrastructure of freeze-fixed/freeze-substituted pollen grains. Ultramicroscopy 34:219-21.
20. Jenkins, R. A. 1970. The fine structure of a nuclear envelope associated endosymbiont of Paramecium. J. Gen. Microbiol. 61:355-9.
21. Jenks, A. & Gibbs, S. P. 2000. Immunolocalization and distribution of form II RUBISCO in the pyrenoid and chloroplast stroma of Amphidinium carterae and form I RUBISCO in the symbiont-derived plastids of Peridinium foliaceum (Dinophyceae). J. Phycol. 36:127-38.
22. Kleinig, H. & Sitte, P. 1992. Zellbiologie, 3rd ed. Gustav Fischer, Stuttgart, Jena, New York, 591 pp.
23. Kowallik, K. V. 1992. Origin and evolution of plastids from chlorophyll a+c-containing algae: suggested ancestral relationship to red algal plastids. In Lewin, R. A. [Ed.] Origins of Plastids. Chapman and Hall, New York, London, pp. 223-63.
24. Kowallik, K. V. 1999. Endosymbiose, ein Motor der Evolution. Biol. Heute 1:1-5.
25. Kowallik, K. V., Stoebe, B., Schaffran, I., Kroth-Pancic, P. & Freier, U. 1995. The chloroplast genome of a chlorophyll a+c-containing alga, Odontella sinensis. Plant Mol. Biol. Pep. 13:336-42.
26. Krammer, K. 1992. Pinnularia. Eine Monographie der europäischen Taxa. Bibliotheca Diatomologica Bd. 26, J. Cramer, Berlin, Rúgell, Liechtenstein, 353 pp.
27. Krammer, K. 2000. The genus Pinnularia. In Lange-Bertalot, H. [Ed.] Diatoms of Europe. Vol. 1. A. R. G. Ganter Verlag KG, 703 pp.
28. Lancelle, S. A., Callaham, D. A. & Hepler, P. K. 1986. A method for rapid freeze fixation of plant cells. Protoplasma 131:153-65.
29. Madigan, M. T., Martinko,J. M. & Parker, J. 2000. Biology of Microorganisms, 9th ed. Prentice Hall International Editions, London, UK, 1175 pp.
30. Maier, U. G., Hofmann, C. J. B. & Sitte, P. 1996. Die Evolution von Zellen. Naturwissenschaften 83:103-12.
31. Mann, D. G. 1996. Chloroplast morphology, movements and inheritance in diatoms. In Chaudhary, B. R. & Agrawal, S. B. [Eds.] Cytology, Genetics and Molecular Biology of Algae. SPP Academic Publishing, Amsterdam, The Netherlands, pp. 249-74.
32. Margulis, L. 1993. Symbiosis in Cell Evolution. Microbial Communities in the Archean and Proterozoic Eons, 2nd ed. W.H. Freeman & Company, San Francisco, 452 pp.
33. Mayama, S. & Shihira-Ishikawa, I. 1994a. Putative nucleoids scattered in chloroplast of Pinnularia nobilis (Bacillariophyceae). Jpn. J. Phycol. 42:437-41.
34. Mayama, S. & Shihira-Ishikawa, I. 1994b. Observations on the scattered chloroplast nucleoids in three Pinnularia species, P. major, P. viridis, and P. viridiformis. Abstracts, 5th Intern. Phycol. Congr. Chinese Academy Science, Qingdao, China, p. 27.
35. Mayama, S. & Shihira-Ishikawa, I. 1994c. Distribution types of chloroplast nucleoids in diatoms. Abstracts of the 13th Int. Diatom Symposium, Jean Gilder Congress, Naples, Italy 1994, p. 45.
36. Mayama, S. & Shihira-Ishikawa, I. 1996. Configurations of chloroplast nucleoids in Pinnularia (Bacillariophyceae). Abstracts of the 14th Int. Diatom Symposium, Tokyo 1996, p. 76.
37. McFadden, G. I. 2001. Primary and secondary, endosymbiosis and the origin of plastids. J. Phycol. 37:951-9.
38. Medlin, L. K., Kooistra, W. H. C. F., Potter, D., Saunders, G. W. & Andersen, R. A. 1997. Phylogenetic relationships of the "golden algae" (haptophytes, heterokont chromophytes) and their plastids. Plant Syst. Evol. 11 (Suppl.):187-219.
39. Melkonian, M. 1996. Phylogeny of photosynthetic protists and their plastids. Verh. Dtsch. Zool. Ges. 89:71-96.
40. Mereschkowsky, C. 1910. Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre vonder Entstehung der Organismen. Biologisch. Centralb. 30:278-303.
41. Müller, M. & Moor, H. 1984. Cryofixation of thick specimens by high pressure freezing. In Revel, J.-P., Barnard, T. & Haggis, G.-H. [Eds.] The Science of Biological Specimen Preparation. SEM Inc., AMF O'Hare, Chicago, pp. 131-8.
42. Müller, M., Marti, T. & Kriz, S. 1980. Improved structural preservation by freeze substitution. In Brederoo P. & de Priester W. [Eds.] Electron Microscopy 1980, Vol. II. Proc. 7th Europ. Congr. Electron Microsc., Leiden, pp. 720-21.
43. Pickett-Heaps, J. D., Tippit, D. H. & Andreozzi, J. A. 1978. Cell division in the pennate diatom Pinnularia. I. Early stages in mitosis. Biol. Cell. 33:71-8.
44. Pickett-Heaps, J. D., Tippit, D. H. & Andreozzi, J. A. 1979. Cell division in the pennate diatom Pinnularia. IV. Valve morphogenesis. Biol. Cell. 35:199-206.
45. Preisig, H.-R. & Hibberd, D. J. 1984. Virus-like particles and endophytic bacteria in Paraphysomonas and Chromophysomonas (Chrysophyceae). Nord. J. Bot. 4:279-85.
46. Reisser, W. 1990. Participation of algal cell wall surface structures in the formation of host-symbiont-interface of endocytobiotic systems. In Wiessner, W., Robinson, D. G. & Starr, R. C. [Eds.] Experimental Phycology: Cell Walls and Surfaces, Reproduction and Photosynthesis. Springer-Berlin, Heidelberg, pp.55-68.
47. Schmid, A. M. 1989. Geitler's "Plattenband" in the diatom Synedra cf. ulna in the light of TEM investigations. Pl. Syst. Evol. 164:239-52.
48. Schmid, A. M. 1991. A life for cell biology - a life for diatoms. Obituary: Professor Dr. Lothar Geitler (May 18, 1899 - May 1, 1990). Diatom Res. 6:181-93.
49. Schmid, A. M. 1994. Aspects of morphogenesis and function of diatom cell walls with implications for taxonomy. Protoplasma 181:43-60.
50. Schmid, A. M. 2000. "Scattered cp-nucleoids" in diatoms explained: bacteria - inside the endoplasmic reticulum - pierce the plastids of Pinnularia nobilis. J. Phycol. 36:61-2.
51. Schmid, A. M. 2001. Value of pyrenoids in the systematics of the diatoms: their morphology, and ultrastructure. In Economou-Amilli, A. [Ed.] Proceedings of the 16th International Diatom Symposium. University of Athens Press, Athens, 2000, pp. 1-32.
52. Schmid, A. M. 2003. Endobacteria in the diatom Pinnularia (Bacillariophyceae). II. Host cell cycle-dependent translocation and transient chloroplast scars. J. Phycol. 39:139-153.
53. Schmid, A. M., Eberwein, R. & Hesse, M. 1996. Pattern morphogenesis in cell walls of diatoms and pollen grains: a comparison. Protoplasms 193:144-73.
54. Schnepf, E. 1984. The cytological viewpoint of functional compartmentation. In Wiessner W., Robinson D. & Starr R. C. [Eds.] Compartments in Algal Cells and their Interaction. Springer Berlin, Heidelberg, pp.1-10.
55. Sharon, N. & Lis, H. 1989. Lectins as cell recognition molecules. Science 246:227-46.
56. Sitte, P. 1981. Die Endosymbionten Hypothese-eine kritische Betrachtung zur Zell-Evolution. Nova Acta Leopoldina NF56 251:41-58.
57. Sitte, P. 1993. Symbiogenetic evolution of complex cells and complex plastids. Eur. J. Protistol. 29:131-43.
58. Spurr, A. R. 1969. A low viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43.
59. Steinbrecht, R. A. & Müller, M. 1987. Freeze substitution and freeze drying. In Steinbrecht R. A. & Zierold K. [Eds.] Cryotechniques in Biological Electron Microscopy. Springer, Berlin, Heidelberg, pp.149-72.
60. Studer, D., Michel, M. & Müller, M. 1989. High pressure freezing comes of age. Seann. Microsc. 3(Suppl.):253-69.
61. Tamm, S. L. 1978. Membrane specialisations associated with the attachment of prokaryotes to a eucaryotic cell. J. Cell Biol. 79:216a.
62. Tschermak-Woess, E. 1953. Über auffallende Strukturen in den Pyrenoiden einiger Naviculoideen. Österr. Bot. Z. 100:160-78.
63. Tschermak-Woess, E. & Weber, A. 1989. Lothar Geitler on the occasion of his 90th birthday on May 18th 1989. [Foreword of the editors & list of publications of Lothar Geitler since 1979.] Pl. Syst. Evol. 164: No.1-4, 165:No.1-2.
64. van den Hoek, C., Mann, D. G. & Jahns, H. M. 1995. Algae: An Introduction to Phycology. Cambridge University Press, Cambridge, 623 pp.
65. Weber, M. 1989. Thiéry test in combination with a uranyl acetate-lead citrate staining. Stain Technol. 64:147-9.
66. Wenderoth, K. 1980. Photokinese und photophobische Reaktionen der Kieselalge Navicula peregrina. Film no. C-1388, IWF, Institut f. wissenschaftl. Film, Göttingen.
67. Wilcox, L. W. 1986. Prokaryotic endosymbionts in the chloroplast stroma of the dinoflagellate Woloszynskia pascheri. Protoplasma 135:71-9.
68. Wujek, D. E. 1979. Intracellular bacteria in the blue-green alga Pleurocapsa minor. Trans. Am. Micros. Soc. 98:143-5.
69. Wujek, D. E. 1984. Bacteria in the perinuclear cisterns of the chrysophyte Chrysosphaerella. Trans. Kansas Acad. Sci. 87:32-5.