Abstract
Glaucocystis nostochinearum is a eukaryotic organism with “chloroplasts” that have usually been assumed to be “cyanelles” — i.e., endosymbiotic cyanobacteria. Previous attempts by others to support this assumption by demonstrating the presence of a limiting peptidoglycan envelope have been unsuccessful.
In the present study disruption of intact Glaucocystis cells with a glass tissue homogenizer permitted the isolation of the uniquely-shaped cyanelles. That these cyanelles were lunited by a peptidoglycan-containing envelope was concluted from the following evidence: (1) stability of isolated cyanelles in distilled water as determined by the preservation of their intactness and peculiar asymmetrical shape; (2) lysozyme sensitivity as demonstrated by lysis of isolated cyanelles when treated with low concentrations of lysozyme; (3) inhibition of the lysozyme-mediated lysis by N-acetyl-glucosamine-2, a known competitive inhibitor of lysozyme, (4) visualization of a thin, electron dense layer between the two limiting membranes around the cyanelle, and (5) isolation and identification of the peptidoglycan-specific amino acid, diaminopimelic acid, from the cyanelles.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Aitken A, Stanier RY (1979) Characterization of peptidoglycan from the cyanelles of Cyanophora paradoxa. J Gen Microbiol 112: 219–223
Chapman DJ (1966) Pigments of the symbiotic algae (cyanomers) of Cyanophora paradoxa and Glaucocystis nostochinearum and two Rhodophycaea, Porphyridium aerugineum and Asterocystis ramosa. Arch Mikrobiol 55: 17–25
Drews G (1973) Fine structure and chemical composition of the cell envelopes. In: Carr NG, Whitton BA (eds) The biology of blue-green algae. Univ of Calif Press, Berkeley, pp 99–116
Floener L, Bothe H (1982) Metabolic activities in Cyanophora paradoxa and its cyanelles. II. Photosynthesis and respiration. Planta 156: 78–83
Fox GE, Stackenbrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LJ, Zablen LB, Blakemore R, Gupta R, Bonen L, Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209: 457–463
Geitler L (1923) Der Zellbau von Glaucocystis nostochinearum und Gloeochaete wittrockiana und die Chromatophoren-Symbiosetheorie von Mereschkowsky. Arch Protistenkd 47: 1–24
Ghuysen JM (1968) Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol Rev 32: 425–464
Golecki JR (1977) Studies on ultrastructure and composition of cell walls of the cyanobacterium Anacystis nidulans. Arch Microbiol 114: 35–41
Giddings TH Jr, Wasmann C, Staehelin LA (1983) Structure of the thylakoids and envelope membranes of the cyanelles of Cyanophora paradoxa. Plant Physiol 71: 409–419
Hall WT, Claus G (1963) Ultrastructural studies on the blue-green algal symbiont in Cyanophora paradoxa Korschikoff. J Cell Biol 19: 551–563
Hall WT, Claus G (1967) Ultrastructural studies on the cyanelles of Glaucocystis nostochinearum Itzigsohn. J Phycol 3: 37–51
Herdman M, Stanier RY (1977) The cyanelle: chloroplast or endosymbiotic prokaryote? FEMS Microbiol Lett 1: 7–12
Holm-Hansen O, Prasad R, Lewin RA (1965) Occurrence of α,ɛ-diaminopimelic acid in algae and flexibacteria. Phycologia 5: 1–14
Imoto T, Johnson LN, North ACT, Phillips DC, Rupley JA (1972) Vertebrate lysozymes. In: Boyer PD (ed) The enzymes, vol VII (3rd edn). Academic Press, NY; London, pp 665–868 [pp 836–841]
Jensen TE, Sicko LM (1971) The effect of lysozyme on cell wall morphology in a blue-green alga, Cylindrospermum sp. J Gen Microbiol 68: 71–75
Jollés P, Saint-Blancard J, Allary M, Périn JP, Cozzone P (1975) On the binding of N-acetylglucosamine and its short polymers to hen lysozyme at physiological temperature (40° C). FEBS Lett 55: 165–167
Kies L (1979) Zur systematischen Einordnung von Cyanophora paradoxa, Gloeochaete wittrockiana und Glaucocystis nostochinearum. Ber Dtsch Bot Ges 92: 445–454
Korschikov AA (1930) Glaucosphaera vacuolata, a new member of the Glaucophyceae. Arch Protistenkd 70: 217–222
Lefort M (1965) Sur le chromatoplasma d'une Cyanophycée endosymbiotique: Glaucocystis nostochinearum Itzigs. C R. Hébd Séances Acad Sci D 261: 233–236
Lewin RA (1974) Biochemical taxonomy. In: Stewart WDP (ed) Algal physiology and biochemistry Univ of Calif Press, Berkeley, pp 1–39
Margulis L (1970) Origin of eukaryotic cells. Yale Univ Press, New Haven, Conn
Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Zentralbl 25: 593–604
Mollenhauer HH (1964) Plastic embedding mixtures for use in electron microscopy. Stain Technol 39: 111–114
Pascher A (1914) Über Symbiosen von Spaltpilzen und Flagellaten. Ber Dtsch Bot Ges 32: 339–351
Pickett-Heaps J (1972) Cell division in Cyanophora paradoxa. New Phytol 71: 561–567
Robinson DG, Preston RD (1971a) Studies on the fine structure of Glaucocystis nosstochinearum Itzigs. I. Wall structure. J Exp Bot 22: 635–643
Robinson DG, Preston RD (1971b) Studies on the fine structure of Glaucocystis nosstochinearum Itzigs. II. Membrane morphology and taxonomy. Br Phycol J 6: 113–128
Rupley JA (1964) The hydrolysis of chitin by concentrated hydrochloric acid, and the preparation of low-molecular-weight substrates for lysozyme. Biochim Biophys Acta 83: 245–255
Schenk HEA (1970) Nachweis einer lysozymempfindlichen Stützmembran der Endocyanellen von Cyanophora paradoxa Korschikoff. Z Naturforsch B 25: 656
Schenk HEA (1971) Isolierung der Endocyanellen aus Glaucocystis nostochinearum Itz. mit Hilfe eines querschnittvariablen Durchlaufhomogenisators und chemische Charakterisierung der Hüllmembran. Hoppe-Seyler's Z Physiol Chem 352: 321–324
Schenk HEA, Hofer I (1972) About the light and dark fixation of CO2 in the cyanoms Cyanophora paradoxa and Glaucocystis nostochinearum and their endocyanelles. In: Forti G, Avron M, Melandri A (eds) Proceedings of the Second International Congress on Photosynthesis Research, vol 3. W. Junk, The Hague, pp 2095–2099
Schnepf E (1965) Struktur der Zellwände und Cellulosefibrillen bei Glaucocystis Planta 67: 213–224
Schnepf E, Koch W, Deichgräber G (1966) Zur Cytologic und taxonomischen Einordnung von Glaucocystis. Arch Mikrobiol 55: 149–174
Sharon N (1967) The chemical structure of lysozyme substrates and their cleavage by the enzyme. Proc R Soc Lond B 167: 402–415
Skuja H (1948) Taxonomie des Phytoplanktons einiger Seen in Uppland, Sweden. Symb Bot Upsal 9: 1–400
Skuja H (1954) Glaucophyta. In: Engler A (ed) Syllabus der Pflanzenfamilien. Borntraeger, Berlin, pp 56–57
Stanier RY (1970) Some aspects of the biology of cells and their possible evolutionary significance. In: Charles HP, Knight BCJG (eds) Organization and control in prokaryotic and eukaryotic cells, 20th Symposium of the Society for General Microbiology, vol 20. Cambridge Univ Press, Cambridge, pp 1–38
Tilden J (1910) Minnesota algae. Univ of Minnesota Press, Minneapolis
Trench RK, Pool RR, Logan M, Engelland A (1978) Aspects of the relation between Cyanophora paradoxa (Korschikoff) and its endosymbiotic cyanelles Cyanocyta korschikoffiana (Hall and Claus). Proc R Soc Lond B 202: 423–443
Ueda K (1961) Structure of plant cells with special reference to lower plants. VI. Structure of chloroplasts in algae. Cytologia 26: 344–358
West GS (1904) The British freshwater algae. Cambridge Univ Press, Cambridge
West GS, Fritsch FE (1927) A treatise on the British freshwater algae. Cambridge Univ Press, Cambridge
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Scott, O.T., Castenholz, R.W. & Bonnett, H.T. Evidence for a peptidoglycan envelope in the cyanelles of Glaucocystis nostochinearum Itzigsohn. Arch. Microbiol. 139, 130–138 (1984). https://doi.org/10.1007/BF00401987
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00401987