Cryo-electron tomography reveals the comparative three-dimensional architecture of Prochlorococcus, a globally important marine cyanobacterium

Journal of Bacteriology

Volumn 189, Issue 12, 2007, Pages 4485-4493

  Ting, Claire S ^a   Hsieh, Chyongere ^b   Sundararaman, Sesh ^a   Mannella, Carmen ^b   Marko, Michael ^b  

^a WILLIAMS COLLEGE   (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENOME; BACTERIAL MEMBRANE; BIOSYNTHESIS; CRYOELECTRON TOMOGRAPHY; CYANOBACTERIUM; GENOMICS; GEOMETRY; IMAGE ANALYSIS; MARINE BACTERIUM; MICROBIAL DIVERSITY; NONHUMAN; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROCHLOROCOCCUS; STRAIN DIFFERENCE; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; TOMOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL MEMBRANE; CELL WALL; CRYOELECTRON MICROSCOPY; CYTOPLASM; GENOME, BACTERIAL; INCLUSION BODIES; MOLECULAR SEQUENCE DATA; PEPTIDOGLYCAN; PROCHLOROCOCCUS; SEQUENCE ALIGNMENT;

PROCHLOROCOCCUS;

EID: 34250338914     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01948-06     Document Type: Article

References (54)

1. 2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J. Exp. Bot. 54:609-622.
2. Bergthorsson, U., and H. Ochman. 1998. Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol. Biol. Evol. 15:9-16.
3. Campbell, L., H. B. Liu, H. A. Nolla, and D. Vaulot. 1997. Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at Station ALOHA during the 1991-1994 ENSO event. Deep-Sea Res. Part I 44:167.
4. Crowther, R. A., D. J. DeRosier, and A. Klug. 1970. The reconstruction of a three-dimensional structure from its projections and its application to electron microscopy. Proc. R. Soc. Lond. A 317:319-340.
5. Dmitriev, B., F. Toukach, and S. Ehlers. 2005. Towards a comprehensive view of the bacterial cell wall. Trends Microbiol. 13:569-574.
6. Dubochet, J., M. Adrian, J. J. Chang, J. C. Homo, J. Lepault, A. W. McDowall, and P. Schultz. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129-228.
7. DuRand, M. D., R. J. Olson, and S. W. Chisholm. 2001. Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep-Sea Res. Part II 48:1983-2003.
8. Forster, F., O. Medalia, N. Zauberman, W. Baumeister, and D. Fass. 2005. Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102:4729-4734.
9. Frank, J., T. Wagenknecht, B. F. McEwen, M. Marko, C. E. Hsieh, and C. A. Mannella. 2002. Three-dimensional imaging of biological complexity. J. Struct. Biol. 138:85-91.
10. Frank, J., M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith. 1996. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116:190-199.
11. Giddings, T. H., N. W. Withers, and L. A. Staehelin. 1980. Supramolecular structure of the stacked and unstacked regions of the photosynthetic membranes of Prochloron sp., a prokaryote. Proc. Natl. Acad. Sci. USA 77:352-356.
12. Grimm, R., H. Singh, R. Rachel, D. Typke, W. Zillig, and W. Baumeister. 1998. Electron tomography of ice-embedded prokaryotic cells. Biophys. J. 74:1031-1042.
13. Grunewald, K., P. Desai, D. C. Winkler, J. B. Heymann, D. M. Belnap, W. Baumeister, and A. C. Steven. 2003. Three-dimensional structure of the herpes simplex virus from cryo-electron tomography: Science 302:1396- 1398.
14. Hess, W. R., G. Rocap, C. S. Ting, F. Larimer, S. Stilwagen, J. Lamerdin, and S. W. Chisholm. 2001. The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynthesis Res. 70:53-71.
15. Hoiczyk, E., and A. Hansel. 2000. Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J. Bacteriol. 182:1191-1199.
16. Hsieh, C. E., A. Lieth, C. A. Mannella, J. Frank, and M. Marko. 2006. Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections. J. Struct. Biol. 153:1-13.
17. Hsieh, C. E., M. Marko, J. Frank, and C. A. Mannella. 2002. Electron tomographic analysis of frozen-hydrated tissue sections. J. Struct. Biol. 138: 63-73.
18. Johnson, Z. I., E. R. Zinser, A. Coe, N. P. McNulty, E. M. S. Woodward, and S. W. Chisholm. 2006. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737-1740.
19. Kerfeld, C. A., M. R. Sawaya, S. Tanaka, C. V. Nguyen, M. Phillips, M. Beeby, and T. O. Yeates. 2005. Protein structures forming the shell of primitive bacterial organelles. Science 309:936-938.
20. Koch, A. L. 1988. Biophysics of bacterial walls viewed as stress-bearing fabric. Microbiol. Rev. 52:337-353.
21. Kramer, D. M., J. A. Cruz, and A. Kanazawa. 2003. Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci. 8:27-32.
22. Kurner, J., A. S. Frangakis, and W. Baumeister. 2005. Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307:436-438.
23. Liberton, M., H. Berg, J. Heuser, R. Roth, and H. B. Pakrasi. 2006. Ultrastructure of the membrane systems in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Protoplasma 227:129-138.
24. Lichtle, C., J. C. Thomas, and A. Spilar. 1995. Immunological and ultrastructural characterization of the photosynthetic complexes of the prochlorophyte Prochlorococcus (Oxychlorobacteria). J. Phycol. 31:934-941.
25. Mannella, C. A. 2006. Structure and dynamics of the mitochondrial inner membrane cristae. Biochim. Biophys. Acta 1763:542-548.
26. Matias, V. R. F., A. Al-Amoudi, J. Dubochet, and T. J. Beveridge. 2003. Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J. Bacteriol. 185:6112-6118.
27. Medalia, O., I. Weber, A. S. Frangakis, D. Nicastro, G. Gerisch, and W. Baumeister. 2002. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298:1209-1213.
28. Miller, K. R., J. S. Jacob, T. Burger-Wiersma, and H. C. Matthijs. 1988. Supramolecular structure of the thylakoid membrane of Prochlorothrix hollandica: a chlorophyll b-containing prokaryote. J. Cell Sci. 91:577-586.
29. Moore, L. R., and S. W. Chisholm. 1999. Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol. Oceanogr. 44:628-638.
30. Morel, A., Y. H. Ahn, F. Partensky, D. Vaulot, and H. Claustre. 1993. Prochlorococcus and Synechococcus: A comparative study of their optical properties in relation to their size and pigmentation. J. Mar. Res. 51:617-649.
31. Mullineaux, C. W. 1999. The thylakoid membranes of cyanobacteria: structure, dynamics and function. Aust. J. Plant Physiol. 26:671-677.
32. Nicastro, D., A. S. Frangakis, D. Typke, and W. Baumeister. 2000. Cryoelectron tomography of neurospora mitochondria. J. Struct. Biol. 129:48-56.
33. Nicastro, D., J. R. McIntosh, and W. Baumeister. 2005. 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102:15889-15894.
34. Niklas, K. J. 1997. The evolutionary biology of plants, p. 219-244. University of Chicago Press, Chicago, IL.
35. Partensky, F., W. R. Hess, and D. Vaulot. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63:106-127.
36. Penczek, P., M. Marko, K. Buttle, and J. Frank. 1995. Double-title electron tomography. Ultramicroscopy 60:393-410.
37. Radermacher, M., and W. Hoppe. 1980. Properties of three-dimensionally reconstructed objects from projections by conical tilting compared to single axis tilting. Proc. 7th Eur. Congr. Electron Microsc. Den Haag 1:132-133.
38. Rappe, M. S., and S. J. Giovannoni. 2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369-394.
39. Rocap, G., F. W. Larimer, J. Lamerdin, S. Malfatti, P. Chain, N. A. Ahlgren, A. Arellano, M. Coleman, L. Hauser, W. R. Hess, Z. I. Johnson, M. Land, D. Lindell, A. F. Post, W. Regala, M. Shah, S. L. Shaw, C. Steglich, M. B. Sullivan, C. S. Ting, A. Tolonen, E. A. Webb, E. R. Zinser, and S. W. Chisholm. 2003. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042-1047.
40. Rogers, H. J., H. R. Perkins, and J. B. Ward. 1980. Microbial cell walls and membranes. Chapman & Hall, London, United Kingdom.
41. Schmid, M. F., A. M. Paredes, H. A. Khant, F. Soyer, H. C. Aldrich, W. Chiu, and J. M. Shively. 2006. Structure of Halothiobacillus neapolitanus carboxysomes by cryo-electron tomography. J. Mol. Biol. 364:526-535.
42. Shimada, A, S. Kanai, and T. Maruyama. 1995. Partial sequence of ribulose-1,5-bisphosphate carboxylase/oxygenase and the phytogeny of Prochloron and Prochlorococcus (Prochlorales). J. Mol. Evol. 40:671-677.
43. Shimoni, E., O. Rav-Hon, I. Ohad, V. Brumfeld, and Z. Reich. 2005. The three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17:2580-2586.
44. Stanier, G. 1988. Fine structure of cyanobacteria. Methods Enzymol. 167: 157-172.
45. Stanier, R. Y., and G. Cohen-Bazire. 1977. Photosynthetic prokaryotes: the cyanobacteria. Annu. Rev. Microbiol. 31:225-274.
46. Steven, A. C., and U. Aebi. 2003. The next ice age: cryo-electron tomography of intact cells. Trends Cell Biol. 13:107-110.
47. Sui, H., and K. H. Downing. 2006. Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography. Nature 442: 475-478.
48. Thompson, J. R., S. Pacocha, C. Pharino, V. Klepac-Ceraj, D. E. Hunt, J. Benoit, R. Sarma-Rupavtarm, D. Distel, and M. F. Polz. 2005. Genotypic diversity within a natural coastal bacterioplankton population. Science 307: 1311-1313.
49. Ting, C. S., E. Westly, and E. Russell-Roy. 2005. Genome diversification in marine cyanobacteria: implications for photosynthetic physiology and environmental stress response mechanisms, p. 614-616. In A. van der Est and D. Bruce (ed.), Photosynthesis: fundamental aspects to global perspectives. Alliance Communications Group, Lawrence, KS.
50. Ting, C. S., G. Rocap, J. King, and S. W. Chisholm. 2002. Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol. 10:134-142.
51. van de Meene, A. M. L., M. F. Hohmann-Marriott, W. F. Vermaas, and R. W. Roberson. 2006. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch. Microbiol. 184:259-270.
52. Vaulot, D., D. Marie, R. J. Olson, and S. W. Chisholm. 1995. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific Ocean. Science 268:1480-1482.
53. Wagenknecht, T., C. E. Hsieh, B. K. Rath, S. Fleischer, and M. Marko. 2002. Electron tomography of frozen-hydrated isolated triad junctions. Biophys. J. 83:2491-2501.
54. Young, K. D. 2003. Bacterial shape. Mol. Microbiol. 49:571-580.