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Structure, Function and Formation of Bacterial Intracytoplasmic Membranes

  • Robert A. Niederman
Chapter
Part of the Microbiology Monographs book series (MICROMONO, volume 2)

Abstract

A variety of prokaryotes increase their membrane surface area for energy transduction processesby developing an intracytoplasmic membrane (ICM), in the form of tubules, interconnected vesicles, and single,paired or stacked lamellae. Recent images of the ICM of the photosynthetic bacterium Rhodobactersphaeroides, obtained by atomic force microscopy, have provided the first submolecular surfaceviews of any complex multi-component membrane. These topographs revealed rows of dimeric core light-harvesting1 (LH1) (RC) complexes, interconnected by the peripheral light-harvesting 2 (LH2) complex, which also existedin separate clusters. In addition, polarized light spectroscopy demonstrated that this optimal functionalarrangement is extended into a long-range pattern of membrane organization. Functional insights providedby the detailed structures of the light-harvesting, RC and cytochrome bc 1complexes are also discussed, including how LH1 is organized to facilitate ubiquinone exchange. It wasshown that LH1-RC core structures are inserted initially into the cytoplasmic membrane, which upon additionof LH2, invaginates to form the ICM, with LH2 packing between rows of dimeric core complexes, and ultimatelyforming separate bulk LH2 clusters. The ICM of the ecologically important methanotrophs, and chemolithotrophicnitrifying bacteria that convert ammonia to nitrite, is also discussed. The recent determination of thecrystal structure of the major ICM protein, methane monooxygenase, and the complete genome sequence of Methylococcus capsulatus, are providing further insights into the molecular detailsof both methane oxidation and utilization of the resulting methanol as a sole source of carbon andenergy.

Keywords

Rhodobacter Sphaeroides Linear Dichroism Methane Monooxygenase Anoxygenic Phototrophic Bacterium Methanol Dehydrogenase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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Notes

Acknowledgments

The author thanks Chris Chen and Riyesh Menon for conducting the searches of the Rba. sphaeroides genome and Rps. palustris proteomics data. Profs. Xiche Hu, Mary Lynne Perille Collins, Alan A. Despirito, George Georgiou and Amy C. Rosenzweig are gratefully acknowledged for permission to use figures from their publications.

References

  1. 1.
    Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987) Structure of the reaction center from Rhodobacter sphaeroides R26: The protein subunits. Proc Natl Acad Sci USA 84:6162–6166 PubMedCrossRefGoogle Scholar
  2. 2.
    Anthony C, Williams P (2003) The structure and mechanism of methanol dehydrogenase. Biochim Biophys Acta 1647:18–23 PubMedCrossRefGoogle Scholar
  3. 3.
    Arp DJ, Sayavedra-Soto LA, Hommes NG (2002) Molecular biology and biochemistry of ammonia oxidation by Nitrosomonas europaea. Arch Microbiol 178:250–255 PubMedCrossRefGoogle Scholar
  4. 4.
    Bahatyrova S, Frese RN, Siebert CA, van der Werf KO, van Grondelle R, Niederman RA, Bullough PA, Otto C, Olsen JD, Hunter CN (2004a) The native architecture of a photosynthetic membrane. Nature 430:1058–1062 PubMedCrossRefGoogle Scholar
  5. 5.
    Bahatyrova S, Frese RN, van der Werf KO, Otto C, Hunter CN, Olsen JD (2004b) Flexibility and size heterogeneity of the LH1 light harvesting complex revealed by atomic force microscopy: functional significance for bacterial photosynthesis. J Biol Chem 279:21327–21333 PubMedCrossRefGoogle Scholar
  6. 6.
    Barz WP, Vermeglio A, Francia F, Venturoli G, Melandri BA, Oesterhelt D (1995) Role of the PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 2. PufX is required for efficient ubiquinone/ubiquinol exchange between the reaction center QB site and the cytochrome bc 1 complex. Biochemistry 34:15248–15258 PubMedCrossRefGoogle Scholar
  7. 7.
    Berry EA, Huang LS, Saechao LK, Pon NG, Valkova-Valchanova M, Daldal F (2004) X-Ray structure of Rhodobacter capsulatus cytochrome bc 1: Comparison with its mitochondrial and chloroplast counterparts. Photosynth Res 81:251–275 PubMedCrossRefGoogle Scholar
  8. 8.
    Bowyer JR, Hunter CN, Ohnishi T, Niederman RA (1985) Photosynthetic membrane development in Rhodopseudomonas sphaeroides. Spectral and kinetic characterization of redox components of light-driven electron flow in apparent photosynthetic membrane growth initiation sites. J Biol Chem 260:3295–3304 PubMedGoogle Scholar
  9. 9.
    Braatsch S, Gomelsky M, Kuphal S, Klug G (2002) A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol Microbiol 45:827–836 PubMedCrossRefGoogle Scholar
  10. 10.
    Brantner CA, Buchholz LA, Remsen CC, Collins MLP (2000) Isolation of intracytoplasmic membrane from the methanotrophic bacterium Methylomicrobium album BG8. Curr Microbiol 40:132–134 PubMedCrossRefGoogle Scholar
  11. 11.
    Brantner CA, Remsen CC, Owen HA, Buchholz LA, Perille Collins ML (2002) Intracellular localization of the particulate methane monooxygenase and methanol dehydrogenase in Methylomicrobium album BG8. Arch Microbiol 178:59–64 PubMedCrossRefGoogle Scholar
  12. 12.
    Broglie RM, Hunter CN, Delepelaire P, Niederman RA, Chua N-H, Clayton RK (1980) Isolation and characterization of the pigment–protein complexes of Rhodopseudomonas sphaeroides by lithium dodecyl sulfate/polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 77:87–91 PubMedCrossRefGoogle Scholar
  13. 13.
    Chain P, Lamerdin J, Larimer F, Regala W, Lao V, Land M, Hauser L, Hooper A, Klotz M, Norton J, Sayavedra-Soto L, Arciero D, Hommes N, Whittaker M, Arp D (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185:2759–2773 PubMedCrossRefGoogle Scholar
  14. 14.
    Chistoserdova L, Laukel M, Portais JC, Vorholt JA, Lidstrom ME (2004) Multiple formate dehydrogenase enzymes in the facultative methylotroph Methylobacterium extorquens AM1 are dispensable for growth on methanol. J Bacteriol 186:22–28 PubMedCrossRefGoogle Scholar
  15. 15.
    Choi DW, Antholine WE, Do YS, Semrau JD, Kisting CJ, Kunz RC, Campbell D, Rao V, Hartsel SC, DiSpirito AA (2005) Effect of methanobactin on the activity and electron paramagnetic resonance spectra of the membrane-associated methane monooxygenase in Methylococcus capsulatus Bath. Microbiology 151:3417–3426 PubMedCrossRefGoogle Scholar
  16. 16.
    Choi DW, Kunz RC, Boyd ES, Semrau JD, Antholine WE, Han JI, Zahn JA, Boyd JM, de la Mora AM, DiSpirito AA (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH:quinone oxidoreductase complex from Methylococcus capsulatus. Bath J Bacteriol 185:5755–5764 CrossRefGoogle Scholar
  17. 17.
    Cogdell RJ, Gardiner AT, Roszak AW, Law CJ, Southall J, Isaacs NW (2004) Rings, ellipses and horseshoes: how purple bacteria harvest solar energy. Photosynth Res 81:207–214 PubMedCrossRefGoogle Scholar
  18. 18.
    Collins MLP, Buchholz LA, Remsen CC (1991) Effect of copper on Methylomonas albus BG8. Appl Environ Microbiol 57:1261–1264 PubMedGoogle Scholar
  19. 19.
    Csáki R, Bodrossy L, Klem J, Murrell JC, Kovacs KL (2003) Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath): cloning, sequencing and mutational analysis. Microbiology 149:1785–1795 PubMedCrossRefGoogle Scholar
  20. 20.
    Dalton H (1991) Structure and mechanism of action of the enzymes involved in methane oxidation. In: Kelley JW (ed) Applications of Enzyme Biotechnology. Plenum Press, New York, pp 55–68 Google Scholar
  21. 21.
    Deisenhofer J, Michel H (1989) The photosynthetic reaction center from the purple bacterium Rhodopseudomonas vridis. Science 245:1463–1473 PubMedCrossRefGoogle Scholar
  22. 22.
    Drews G (1996) Formation of the light-harvesting complex I (B870) of anoxygenic phototrophic purple bacteria. Arch Microbiol 166:151–159 PubMedCrossRefGoogle Scholar
  23. 23.
    Drews G, Golecki JR (1995) Structure, molecular organization, and biosynthesis of membranes of purple bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 231–257 Google Scholar
  24. 24.
    Drews G, Niederman RA (2002) Membrane biogenesis in anoxygenic photosynthetic prokaryotes. Historical minireview for History of photosynthesis: A celebration of the millennium. Photosynth Res 73:87–94 PubMedCrossRefGoogle Scholar
  25. 25.
    Eraso JM, Kaplan S (1994) prrA, A putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J Bacteriol 176:32–43 PubMedGoogle Scholar
  26. 26.
    Fassel TA, Buchholz LA, Collins MLP, Remsen CC (1992) Localization of methanol dehydrogenase in two strains of methylotrophic bacteria detected by immunogold labeling. Appl Environ Microbiol 58:2302–2307 PubMedGoogle Scholar
  27. 27.
    Fejes AP, Yi EC, Goodlett DR, Beatty JT (2003) Shotgun proteomic analysis of a chromatophore-enriched preparation from the purple phototrophic bacterium Rhodopseudomonas palustris. Photosynth Res 78:195–203 PubMedCrossRefGoogle Scholar
  28. 28.
    Fitch MW, Graham DW, Arnold RG, Agarwal SK, Phelps R, Speitel GE, Georgiou G (1993) Phenotypic characterization of cooper-resistant mutants of Methylosinus trichosporium OB3b. Appl Envirort Microbiol 159:2771–2776 Google Scholar
  29. 29.
    Fotiadis D, Qian P, Philippsen A, Bullough PA, Engel A, Hunter CN (2004) Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy. J Biol Chem 279:2063–2068 PubMedCrossRefGoogle Scholar
  30. 30.
    Francia F, Dezi M, Rebecchi A, Mallardi A, Palazzo G, Melandri BA, Venturoli G (2004) Light-harvesting complex 1 stabilizes P+QB charge separation in reaction centers of Rhodobacter sphaeroides. Biochemistry 43:14199–14210 PubMedCrossRefGoogle Scholar
  31. 31.
    Frese RN, Siebert CA, Niederman RA, Hunter CN, Otto C, van Grondelle R (2004) The long-range organization of a native photosynthetic membrane. Proc Natl Acad Sci USA 101:17994–17999 PubMedCrossRefGoogle Scholar
  32. 32.
    Frese RN, Olsen JD, Branvall R, Westerhuis WH, Hunter CN, van Grondelle R (2000) The long-range supraorganization of the bacterial photosynthetic unit: A key role for PufX. Proc Natl Acad Sci USA 97:5197–5202 PubMedCrossRefGoogle Scholar
  33. 33.
    Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, Richardson PM, DeLong EF (2004) Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305:1457–1462 PubMedCrossRefGoogle Scholar
  34. 34.
    Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471 PubMedGoogle Scholar
  35. 35.
    Helde R, Wiesler B, Wachter E, Neubuser A, Hoffschulte HK, Hengelage T, Schimz KL, Stuart RA, Muller M (1997) Comparative characterization of SecA from the alpha-subclass purple bacterium Rhodobacter capsulatus and Escherichia coli reveals differences in membrane and precursor specificity. J Bacteriol 179:4003–4012 PubMedGoogle Scholar
  36. 36.
    Hu X, Damjanovic A, Ritz T, Schulten K (1998) Architecture and mechanism of the light-harvestin g apparatus of purple bacteria. Proc Natl Acad Sci USA 95:5935–5941 PubMedCrossRefGoogle Scholar
  37. 37.
    Hunter CN, Tucker JD, Niederman RA (2005) The assembly and organisation of photosynthetic membranes in Rhodobacter sphaeroides. Photochem Photobiol Sci 4:1023–1027 PubMedCrossRefGoogle Scholar
  38. 38.
    Hunter CN, Pennoyer JD, Sturgis JN, Farrelly D, Niederman RA (1988) Oligomerization states and associations of light-harvesting pigment–protein complexes of Rhodobacter sphaeroides as analyzed by lithium dodecyl sulfate-polyacrylamide gel electrophoresis. Biochemistry 27:3459–3467 CrossRefGoogle Scholar
  39. 39.
    Karrasch S, Bullough PA, Ghosh R (1995) The 8.5 Å projection map of the light-harvesting complex I from Rhodospirillum rubrum reveals a ring composed of 16 subunits. EMBO J 14:631–638 PubMedGoogle Scholar
  40. 40.
    Keren N, Liberton M, Pakrasi HB (2005) Photochemical competence of assembled photosystem II core complex in cyanobacterial plasma membrane. J Biol Chem 280:6548–6553 PubMedCrossRefGoogle Scholar
  41. 41.
    Kiley PJ, Varga A, Kaplan S (1988) Physiological and structural analysis of light-harvesting mutants of Rhodobacter sphaeroides. J Bacteriol 170:1103–1115 PubMedGoogle Scholar
  42. 42.
    Kim HJ, Graham DW, DiSpirito AA, Alterman MA, Galeva N, Larive CK, Asunskis D, Sherwood PM (2004) Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305:1612–1615 PubMedCrossRefGoogle Scholar
  43. 43.
    Koblízek M, Shih JD, Breitbart SI, Ratcliffe EC, Kolber ZS, Hunter CN, Niederman RA (2005) Sequential assembly of photosynthetic units in Rhodobacter sphaeroides as revealed by fast repetition rate analysis of variable bacteriochlorophyll a fluorescence. Biochim Biophys Acta 1706:220–231 PubMedCrossRefGoogle Scholar
  44. 44.
    Koepke J, Hu X, Muenke C, Schulten K, Michel H (1996) The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4:581–597 PubMedCrossRefGoogle Scholar
  45. 45.
    Kramer HJM, Pennoyer JD, van Grondelle R, Westerhuis WHJ, Niederman RA, Amesz J (1984) Low-temperature optical properties and pigment organization of the B875 light-harvesting bacteriochlorophyll-protein complex of purple photosynthetic bacteria. Biochim Biophys Acta 767:335–344 CrossRefGoogle Scholar
  46. 46.
    Lieberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature 434:177–182 PubMedCrossRefGoogle Scholar
  47. 47.
    Lieberman RL, Rosenzweig AC (2004) Biological methane oxidation: regulation, biochemistry, and active site structure of particulate methane monooxygenase. Crit Rev Biochem Mol Biol 39:147–164 PubMedCrossRefGoogle Scholar
  48. 48.
    Lloyd JS, De Marco P, Dalton H, Murrell JC (1999) Heterologous expression of soluble methane monooxygenase genes in methanotrophs containing only particulate methane monooxygenase. Arch Microbiol 171:364–370 PubMedCrossRefGoogle Scholar
  49. 49.
    Mackenzie C, Choudhary M, Larimer FW, Predki PF, Stilwagen S, Armitage JP, Barber RD, Donohue TJ, Hosler JP, Newman JE, Shapleigh JP, Sockett RE, Zeilstra-Ryalls J, Kaplan S (2001) The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth Res 70:19–41 PubMedCrossRefGoogle Scholar
  50. 50.
    Masuda S, Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613–623 PubMedCrossRefGoogle Scholar
  51. 51.
    McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ, Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–521 CrossRefGoogle Scholar
  52. 52.
    Merkx M, Lippard SJ (2002) Why OrfY Characterization of mmoD, a long overlooked component of the soluble methane monooxygenase from Melhylococcus capsulatus (Bath). J Biol Chem 277:5858–5865 PubMedCrossRefGoogle Scholar
  53. 53.
    Monger TG, Parson WW (1977) Singlet–triplet fusion in Rhodopseudomonas sphaeroides chromatophores. A probe of the organization of the photosynthetic apparatus. Biochim Biophys Acta 460:393–407 PubMedCrossRefGoogle Scholar
  54. 54.
    Murrell JC, Gilbert B, McDonald IR (2000) Molecular biology and regulation of methane monooxygenase. Arch Microbiol 173:325–332 PubMedCrossRefGoogle Scholar
  55. 55.
    Niederman RA, Mallon DE, Parks LC (1979) Membranes of Rhodopseudomonas sphaeroides. VI. Isolation of a fraction enriched in newly synthesized bacteriochlorophyll a-protein complexes. Biochim Biophys Acta 555:210–220 PubMedCrossRefGoogle Scholar
  56. 56.
    Niederman RA, Gibson KD (1978) Isolation and physicochemical properties of membranes from purple photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The Photosynthetic Bacteria. Plenum Publishing Corp, New York, NY, pp 79–118 Google Scholar
  57. 57.
    Oh J-I, Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39:1116–1123 PubMedCrossRefGoogle Scholar
  58. 58.
    Phelps PA, Agarwal SK, Speitel GE, Georgiou G (1992) Methylosinus trichosporium OB3b mutants having constitutive expression of soluble methane monooxygenase in the presence of high levels of copper. Appl Environ Microbiol 58:3701–3708 PubMedGoogle Scholar
  59. 59.
    Qian P, Hunter CN, Bullough PA (2005) The 8.5 Å projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides. J Mol Biol 349:948–960 PubMedCrossRefGoogle Scholar
  60. 60.
    Reilly PA, Niederman RA (1986) Role of apparent membrane growth initiation sites during photosynthetic membrane development in synchronously dividing Rhodopseudomonas sphaeroides. J Bacteriol 167:153–159 PubMedGoogle Scholar
  61. 61.
    Roh JH, Smith WE, Kaplan S (2004) Effects of oxygen and light intensity on transcriptome expression in Rhodobacter sphaeroides 2.4.1. Redox active gene expression profile. J Biol Chem 279:9146–9155 PubMedCrossRefGoogle Scholar
  62. 62.
    Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P (1993) Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane. Nature 366:537–543 PubMedCrossRefGoogle Scholar
  63. 63.
    Roszak AW, Howard TD, Southall J, Gardiner AT, Law CJ, Isaacs NW, Cogdell RJ (2003) Crystal structure of the RC-LH1 core complex from Rhodopseudomonas palustris. Science 302:1969–1972 PubMedCrossRefGoogle Scholar
  64. 64.
    Scheuring S, Levy D, Rigaud JL (2005) Watching the components of photosynthetic bacterial membranes and their in situ organisation by atomic force microscopy. Biochim Biophys Acta 1712:109–127 PubMedCrossRefGoogle Scholar
  65. 65.
    Scheuring S, Francia F, Busselez J, Melandri BA, Rigaud JL, Levy D (2004) Structural role of PufX in the dimerization of the photosynthetic core complex of Rhodobacter sphaeroides. J Biol Chem 279:3620–3626 PubMedCrossRefGoogle Scholar
  66. 66.
    Schmidt I, Zart D, Bock E (2001) Effects of gaseous NO2 on cells of Nitrosomonas eutropha previously incapable of using ammonia as an energy source. Antonie van Leeuwenhoek 79:39–47 PubMedCrossRefGoogle Scholar
  67. 67.
    Stafford GP, Scanlan J, McDonald IR, Murrell JC (2003) rpoN, mmoR and mmoG, genes involved in regulating the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b. Microbiology 149:1771–1784 PubMedCrossRefGoogle Scholar
  68. 68.
    Stolyar S, Costello AM, Peeples TL, Lidstrom ME (1999) Role of multiple gene copies in particulate methane monooxygenase activity in the methane-oxidizing bacterium Methylococcus capsulatus Bath. Microbiology 145:1235–1244 PubMedCrossRefGoogle Scholar
  69. 69.
    Stolyar S, Franke M, Lidstrom ME (2001) Expression of individual copies of Methylococcus capsulatus Bath particulate methane monooxygenase genes. J Bacteriol 183:1810–1812 PubMedCrossRefGoogle Scholar
  70. 70.
    Sturgis JN, Niederman RA (1996) The effect of different levels of the B800–850 light-harvesting complex on intracytoplasmic membrane development in Rhodobacter sphaeroides. Arch Microbiol 165:235–242 PubMedCrossRefGoogle Scholar
  71. 71.
    Toyama H, Inagaki H, Matsushita K, Anthony C, Adachi O (2003) The role of the MxaD protein in the respiratory chain of Methylobacterium extorquens during growth on methanol. Biochim Biophys Acta 1647:372–375 PubMedCrossRefGoogle Scholar
  72. 72.
    Tso SC, Shenoy SK, Quinn BN, Yu L (2000) Subunit IV of cytochrome bc 1 complex from Rhodobacter sphaeroides. Localization of regions essential for interaction with the three-subunit core complex. J Biol Chem 275:15287–15294 PubMedCrossRefGoogle Scholar
  73. 73.
    Varga AR, Staehelin LA (1985) Membrane adhesion in photosynthetic bacterial membranes. Light harvesting complex I (LHI) appears to be the main adhesion factor. Arch Microbiol 141:290–296 PubMedCrossRefGoogle Scholar
  74. 74.
    Vorholt JA (2002) Cofactor-dependent pathways of formaldehyde oxidation in methylotrophic bacteria. Arch Microbiol 178:239–249 PubMedCrossRefGoogle Scholar
  75. 75.
    Vorholt JA, Chistoserdova L, Stolyar SM, Thauer RK, Lidstrom ME (1999) Distribution of tetrahydromethanopterin-dependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases. J Bacteriol 181:5750–5757 PubMedGoogle Scholar
  76. 76.
    Vos M, van Grondelle R, van der Kooij FW, van de Poll D, Amesz J, Duysens LMN (1986) Singlet–singlet annihilation at low temperatures in the antenna of purple bacteria. Biochim Biophys Acta 850:501–512 CrossRefGoogle Scholar
  77. 77.
    Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541:91–101 PubMedCrossRefGoogle Scholar
  78. 78.
    Walz T, Jamieson SJ, Bowers CM, Bullough PA, Hunter CN (1998) Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 Å, LH1 and RC–LH1 at 25 Å. J Mol Biol 282:833–845 PubMedCrossRefGoogle Scholar
  79. 79.
    Ward N, Larsen Ø, Sakwa J, Bruseth L, Khouri H, Durkin AS, Dimitrov G, Jiang L, Scanlan D, Kang KH, Lewis M, Nelson KE, Methe B, Wu M, Heidelberg JF, Paulsen IT, Fouts D, Ravel J, Tettelin H, Ren Q, Read T, DeBoy RT, Seshadri R, Salzberg SL, Jensen HB, Birkeland NK, Nelson WC, Dodson RJ, Grindhaug SH, Holt I, Eidhammer I, Jonasen I, Vanaken S, Utterback T, Feldblyum TV, Fraser CM, Lillehaug JR, Eisen JA (2004) Genomic insights into methanotrophy: The complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2:e303 Google Scholar
  80. 80.
    Westerhuis WHJ, Sturgis JN, Ratcliffe EC, Hunter CN, Niederman RA (2002) Isolation, size estimates, and spectral heterogeneity of an oligomeric series of light-harvesting 1 complexes from Rhodobacter sphaeroides. Biochemistry 41:8698–8707 PubMedCrossRefGoogle Scholar
  81. 81.
    Westerhuis WHJ, Hunter CN, van Grondelle R, Niederman RA (1999) Modeling of oligomeric-state dependent spectral heterogeneity in the B875 light-harvesting complex of Rhodobacter sphaeroides by numerical simulation. J Phys Chem B 103:7733–7742 CrossRefGoogle Scholar
  82. 82.
    Whittaker M, Bergmann D, Arciero D, Hooper AB (2000) Electron transfer during the oxidation of ammonia by the chemolithotrophic bacterium Nitrosomonas europaea. Biochim Biophys Acta 1459:346–355 PubMedCrossRefGoogle Scholar
  83. 83.
    Young CS, Beatty JT (2003) Multi-level regulation of purple bacterial light-harvesting complexes. In: Green BR, Parson WW (eds) Light-harvesting Antennas in Photosynthesis. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 449–470 Google Scholar
  84. 84.
    Yuan H, Collins MLP, Antholine WE (1999) Type 2 Cu2+ in pMMO from Methylomicrobium album BG8. Biophys J 76:2223–2229 PubMedCrossRefGoogle Scholar
  85. 85.
    Zahn JA, Bergmann DJ, Boyd JM, Kunz RC, DiSpirito AA (2001) Membrane-associated quinoprotein formaldehyde dehydrogenase from Methylococcus capsulatus Bath. J Bacteriol 183:6832–6840 PubMedCrossRefGoogle Scholar
  86. 86.
    Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB (2001) The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci USA 98:13443–13448 PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2006

Authors and Affiliations

  1. 1.Rutgers University, Department of Molecular Biology and BiochemistryNelson Biological LaboratoriesPiscatawayUSA

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