Skip to main content
Log in

The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

To advance our knowledge of the model cyanobacterium Synechocystis sp. PCC 6803 we investigated the three-dimensional organization of the cytoplasm using standard transmission electron microscopy and electron tomography. Electron tomography allows a resolution of ~5 nm in all three dimensions, superior to the resolution of most traditional electron microscopy, which is often limited in part by the thickness of the section (70 nm). The thylakoid membrane pairs formed layered sheets that followed the periphery of the cell and converged at various sites near the cytoplasmic membrane. At some of these sites, the margins of thylakoid membranes associated closely along the external surface of rod-like structures termed thylakoid centers, which sometimes traversed nearly the entire periphery of the cell. The thylakoid membranes surrounded the central cytoplasm that contained inclusions such as ribosomes and carboxysomes. Lipid bodies were dispersed throughout the peripheral cytoplasm and often juxtaposed with cytoplasmic and thylakoid membranes suggesting involvement in thylakoid maintenance or biogenesis. Ribosomes were numerous and mainly located throughout the central cytoplasm with some associated with thylakoid and cytoplasmic membranes. Some ribosomes were attached along internal unit-membrane-like sheets located in the central cytoplasm and appeared to be continuous with existing thylakoid membranes. These results present a detailed analysis of the structure of Synechocystis sp. PCC 6803 using high-resolution bioimaging techniques and will allow future evaluation and comparison with gene-deletion mutants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

HVEM:

High voltage electron microscopy

IVEM:

Intermediate voltage electron microscope

3-D:

Three-dimensional

FESEM:

Field-emission scanning electron microscopy

TEM:

Transmission electron microscopy

References

  • Allen MM (1968) Photosynthetic membrane system in Anacystis nidulans. J Bacteriol 96:836–841

    PubMed  CAS  Google Scholar 

  • Asato Y, Ginoza HS (1973) Separation of small circular DNA molecules from blue green alga Anacystis nidulans. Nat New Biol 244:132–133

    Article  PubMed  CAS  Google Scholar 

  • Baumeister W (2002) Electron tomography: towards visualizing the molecular organization of the cytoplasm. Curr Opin Struct Biol 12:679–684

    Article  PubMed  CAS  Google Scholar 

  • Bryant DA, Guglielmi G, Tandeau de Marsac N, Castets AM, Cohen-Bazire G (1979) Structure of cyanobacterial phycobilisomes—model. Arch Microbiol 123:113–127

    Article  CAS  Google Scholar 

  • Carde JP, Joyard J, Douce R (1982) Electron microscopic studies of envelope membranes from spinach plastids. Biol Cell 44:315–324

    Google Scholar 

  • Cassel WA, Hutchinson WG (1954) Nuclear studies on the smaller Myxophyceae. Exp Cell Res 6:134–150

    Article  PubMed  CAS  Google Scholar 

  • Chua NH, Blobel G, Siekevitz P, Palade GE (1973) Attachment of chloroplast polysomes to thylakoid membranes in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 70:1554–1558

    Article  PubMed  CAS  Google Scholar 

  • Dahl R, Staehelin LA (1989) High-pressure freezing for the preservation of biological structure—theory and practice. J Elec Micros Tech 13:165–174

    Article  CAS  Google Scholar 

  • Douce R, Joyard J (1996) Biosynthesis of thylakoid membrane lipids. In: Ort DR, Yocum CF (eds) Oxygenic photosynthesis: the light reactions. Kluwer, Boston, pp 69–101

    Google Scholar 

  • Edwards MR, Berns DS, Ghiorse WC, Holt SC (1968) Ultrastructure of thermophilic blue green alga Synechococcus lividus Copeland. J Phycol 4:283–298

    Article  Google Scholar 

  • Edwards MR, Gantt E (1971) Phycobilisomes of thermophilic blue green alga Synechococcus lividus. J Cell Biol 50:896–900

    Article  PubMed  CAS  Google Scholar 

  • Erlandsen SL, Ottenwaelter C, Frethem C, Chen Y (2001) Cryo field emission scanning electron microscopy. BioTech 31:300–305

    CAS  Google Scholar 

  • Falk H (1969) Rough thylakoids—polysomes attached to chloroplast membranes. J Cell Biol 42:582–587

    Article  PubMed  CAS  Google Scholar 

  • Frank J (1992) Electron tomography. Plenum Press, New York

    Google Scholar 

  • Frank J, Wagenknecht T, McEwen BF, Marko M, Hsieh C-E, Mannella C (2002) Three-dimensional imaging of biological complexity. J Struct Biol 138:85–91

    Article  PubMed  Google Scholar 

  • Fraser CM, Eisen JA, Salzberg SL (2000) Microbial genome sequencing. Nature 406:799–803

    Article  PubMed  CAS  Google Scholar 

  • Fuhs GW (1963) Cytochemisch-elektronenmikroskopische Lokalisierung der Ribonukleinsäure und des Assimilats in Cyanophyceen. Protoplasma 56:178–187

    Article  Google Scholar 

  • Gantt E, Conti SF (1969) Ultrastructure of blue-green algae. J Bacteriol 97:1486–1493

    PubMed  CAS  Google Scholar 

  • Giddings TH (2003) Freeze-substitution protocols for improved visualization of membranes in high-pressure frozen samples. J Microsc 212:53–61

    Article  PubMed  MathSciNet  CAS  Google Scholar 

  • Gromov BV, Mamkaeva KA (1976) Connection of thylakoids with plasmalemma in cyanobacteria of genus Synechococcus. Microbiol 45:790–791

    Google Scholar 

  • Hinterstoisser B, Cichna M, Kuntner O, Peschek GA (1993) Cooperation of plasma and thylakoid membranes for the biosynthesis of chlorophyll in cyanobacteria: the role of thylakoid centers. J Plant Physiol 142:407–413

    CAS  Google Scholar 

  • Jagendorf AT, Michaels A (1990) Rough thylakoids—translation on photosynthetic membranes. Plant Sci 71:137–145

    Article  CAS  Google Scholar 

  • Jensen TE (1968) Electron microscopy of polyphosphate bodies in a blue green alga Nostoc pruniforme. Arch Mikrobiol 62:144–152

    Article  Google Scholar 

  • Jensen TE (1984) Cyanobacterial cell inclusions of irregular occurrence: systematic and evolutionary implications. Cytobios 39:35–62

    Google Scholar 

  • Jensen TE (1985) Cell inclusions in the Cyanobacteria. Arch Hydrobiol Suppl Bd 71:33–73

    CAS  Google Scholar 

  • Jensen TE, Bowen CC (1961) Organization of the centroplasm in Nostoc pruniforme. Proc Iowa Acad Sci 68:86–89

    Google Scholar 

  • Jensen TE, Sicko LM (1971) Fine structure of poly-β-hydroxybutyric acid granules in a blue-green alga, Chlorogloea fritschii. J Bacteriol 106:683–686

    PubMed  CAS  Google Scholar 

  • Jost M (1965) Die Ultrastruktur von Oscillatoria rubescens D C. Arch Mikrobiol 50:211–245

    Article  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    CAS  Google Scholar 

  • Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71–76

    Article  PubMed  CAS  Google Scholar 

  • Kunkel DD (1982) Thylakoid centers: structures associated with the cyanobacterial photosynthetic membrane system. Arch Microbiol 133:97–99

    Article  Google Scholar 

  • Ladinsky MS, Kremer JR, Furcinitti PS, McIntosh JR, Howell KE (1994) HVEM tomography of the trans-Golgi network: structural insights and identification of a lace-like vesicle coat. J Cell Biol 127:29–38

    Article  PubMed  CAS  Google Scholar 

  • Ladinsky MS, Mastronarde DN, McIntosh JR, Howell KE, Staehelin LA (1999) Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J Cell Biol 144:1135–1149

    Article  PubMed  CAS  Google Scholar 

  • Lancelle SA, Callaham DA, Hepler PK (1986) A method for rapid freeze fixation of plant cells. Protoplasma 131:153–165

    Article  Google Scholar 

  • Lang NJ (1968) The fine structure of blue-green algae. Ann Rev Microbiol 22:15–46

    Article  CAS  Google Scholar 

  • Leak LV (1965) Electron microscopic autoradiography incorporation of H3-thymidine in a blue green alga Anabaena sp. J Ultrastruct Res 12:135–146

    Article  PubMed  CAS  Google Scholar 

  • Leak LV (1967) Studies on preservation and organization of DNA containing regions in a blue green alga: a cytochemical and ultrastructural study. J Ultrastruct Res 20:190–205

    Article  PubMed  CAS  Google Scholar 

  • Marsh BJ, Mastronarde DN, Buttle KF, Howell KE, McIntosh JR (2001) Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high-resolution electron tomography. Proc Natl Acad Sci USA 98:2399–2406

    Article  PubMed  CAS  Google Scholar 

  • Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120:343–352

    Article  PubMed  CAS  Google Scholar 

  • McDonald K, Morphew MK (1993) Improved preservation of ultrastructure in difficult to fix organisms by high pressure freezing and freeze substitution. 1. Drosophila melanogaster and Strongylocentrotus purpuratus embryos. Micros Res Tech 24:465–473

    Article  CAS  Google Scholar 

  • McEwen BF, Frank J (2001) Electron tomographic and other approaches for imaging molecular machines. Curr Opin Neurobiol 11:594–600

    Article  PubMed  CAS  Google Scholar 

  • McIntosh JR (2001) Electron microscopy of cells: a new beginning for a new century. J Cell Biol 153:F25–F32

    Article  PubMed  CAS  Google Scholar 

  • McIntosh JR, Nicastro D, Mastronarde DN (2005) New views of cells in 3D: an introduction to electron tomography. Trends in Cell Biol 15:43–51

    Article  CAS  Google Scholar 

  • Mims CW, Roberson RW, Richardson EA (1988) Ultrastructure of freeze-substituted and chemically fixed basidiospores of Gymnosporangium juniperi-virginianae. Mycologia 80:356–364

    Article  Google Scholar 

  • Mogelsvang S, Marsh BJ, Ladinsky MS, Howell KE (2004) Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5:338–345

    Article  PubMed  CAS  Google Scholar 

  • Moreau P, Bessoule JJ, Mongrand S, Testet E, Vincent P, Cassagne C (1998) Lipid trafficking in plant cells. Prog Lipid Res 37:371–391

    Article  PubMed  CAS  Google Scholar 

  • Nierzwicki-Bauer SA, Balkwill DL, Stevens SE (1983) 3-dimensional ultrastructure of a unicellular cyanobacterium. J Cell Biol 97:713–722

    Article  PubMed  CAS  Google Scholar 

  • Nierzwicki-Bauer SA, Balkwill DL, Stevens SE (1984) The use of high-voltage electron microscopy and semi-thick sections for examination of cyanobacterial thylakoid membrane arrangements. J Microsc 133:55–60

    Google Scholar 

  • O’Toole ET, Giddings TH, McIntosh JR, Dutcher SK (2003) Three-dimensional organization of basal bodies from wild-type and gamma-tubulin deletion strains of Chlamydomonas reinhardtii. Mol Biol Cell 14:2999–3012

    Article  PubMed  CAS  Google Scholar 

  • O’Toole ET, Winey M, McIntosh JR (1999) High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol Biol Cell 10:2017–2031

    PubMed  CAS  Google Scholar 

  • Pankratz HS, Bowen CC (1963) Cytology of blue-green algae. I. The cells of Symploca muscorum. Am J Bot 50:387–399

    Article  Google Scholar 

  • Peat A, Whitton BA (1968) Vegetative cell structure in Anabaenopsis sp. Arch Mikrobiol 63:170–176

    Article  Google Scholar 

  • Philippovich II, Bezsmertanya IN, Oparin AI (1973) On the localization of polyribosomes in the system of chloroplast lamellae. Exp Cell Res 79:159–168

    Article  PubMed  Google Scholar 

  • Philippovich II, Tongur AM, Alina BA, Oparin AI (1970) Localization and conformation of polyribosomes bound to chloroplast lamellae. Exp Cell Res 62:399–406

    Article  PubMed  CAS  Google Scholar 

  • Pinevich AV (1997) Intracytoplasmic membrane structures in bacteria. Endocyt Cell Res 12:9–40

    Google Scholar 

  • Rawyler A, Meylan-Bettex M, Siegenthaler PA (1995) (Galacto)lipid export from envelope to thylakoid membranes in intact chloroplasts. 2. A general process with a key role for the envelope in the establishment of lipid asymmetry in thylakoid membranes. Biochim Biophys Acta 1233:123–133

    Article  PubMed  Google Scholar 

  • Reynolds ES (1963) 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 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Ris H, Singh RN (1961) Electron microscope studies on blue-green algae. J Biophys Biochem Cytol 9:63–80

    Article  PubMed  CAS  Google Scholar 

  • Roberts TM, Koths KE (1976) Blue green alga Agmenellum quadruplicatum contains covalently closed DNA circles. Cell 9:551–557

    Article  PubMed  CAS  Google Scholar 

  • Robinson C, Woolhead C, Edwards W (2000) Transport of proteins into and across the thylakoid membrane. J Exp Bot 51:369–374

    Article  PubMed  CAS  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Staehelin LA (1986) Chloroplasts structure and supramolecular organization of photosynthetic membranes. In: Staehelin LA, Arntzen CJ (eds) Photosynthesis III photosynthetic membranes and light harvesting systems. Springer-Verlag, New York, pp 1–84

    Google Scholar 

  • Stanier G (1988) Fine structure of cyanobacteria. Meth Enzymol 167:157–242

    Article  Google Scholar 

  • Stanier RY, Cohen-Bazire G (1977) Phototrophic prokaryotes—cyanobacteria. Ann Rev Microbiol 31:225–274

    Article  CAS  Google Scholar 

  • Tauchi-Sato K, Ozeki S, Houjou T, Taguchi R, Fujimoto T (2002) The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J Biol Chem 277:44507–44512

    Article  PubMed  CAS  Google Scholar 

  • Wolk CP (1973) Physiology and cytological chemistry of blue-green algae. Bact Rev 37:32–101

    PubMed  CAS  Google Scholar 

  • Wollman FA, Minai L, Nechushtai R (1999) The biogenesis and assembly of photosynthetic proteins in thylakoid membranes. Biochim Biophys Acta 1411:21–85

    Article  PubMed  CAS  Google Scholar 

  • Zheng HQ, Staehelin LA (2001) Nodal endoplasmic reticulum, a specialized form of endoplasmic reticulum found in gravity-sensing root tip columella cells. Plant Physiol 125:252–265

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the U.S. Department of Energy GTL: Genomics Project, # DE-FG03–01ER15251 (WV, RWR). Electron tomography was performed at the facilities of the Boulder Laboratory for 3-D Electron Microscopy of Cells, University of Colorado, Boulder, CO. The authors wish to thank Drs. Eileen O’Toole and David Mastronarde of the Boulder Laboratory for help and guidance with tomography software. Work done in the Boulder Lab was supported by a grant from the National Institutes of Health (RR-00592, J.R. McIntosh, principal investigator). Electron microscopy at ASU was carried out in the Life Sciences Electron Microscopy Facility (TEM) and the Center for Solid State Sciences (cryo-SEM; NSF MRI Grant CTS-0216530). We thank Dr. Ken Hoober (ASU) for engaging in thoughtful discussions and for helpful suggestions and Dr. Dmitrii Vavilin (ASU) for Russian to English translations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert W. Roberson.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

van de Meene, A.M., Hohmann-Marriott, M.F., Vermaas, W.F. et al. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 184, 259–270 (2006). https://doi.org/10.1007/s00203-005-0027-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-005-0027-y

Keywords

Navigation