Respiration and Respiratory Complexes

  • Davide Zannoni
  • Barbara Schoepp-Cothenet
  • Jonathan Hosler
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 28)

Summary

Respiration in facultative phototrophs is a flexible metabolic process that involves various electron donors and acceptors. A good example of such respiratory flexibility can be found in Rhodobacter species, most of them being equipped with genes that encode five distinct oxidases having different oxygen affinities. One of these, the cytochrome cbb 3 oxidase is prevalent at low oxygen tensions, and terminates a highly coupled electron transfer pathway which is formed by a ‘core’ of redox components, e.g., quinones, the cytochrome bc 1 complex and cytochrome c, in common with the photosynthetic apparatus. Thus, by modulating expression of different terminal oxido-reductases that lock onto a core electron transfer pathway, Rhodobacter species can survive in a range of oxic, micro-oxic, and anoxic environments either in the dark or in the light.

This chapter covers first the types and basic characteristics of the terminal oxidases in a few Rhodobacter species; then, respiratory substrates other than oxygen are examined. These substrates include orthodox anaerobic electron acceptors such as DMSO or TMAO but also arsenics as unconventional bioenergetics substrates. Finally, a synopsis of the data examining the functional interactions between photosynthetic and respiratory ETP is given along with a phylogenetic scenario suggesting that respiration is more ancient than both anoxygenic and oxygenic photosynthesis.

Keywords

Fermentation DMSO Selenium Nitrite Bacillus 

Abbreviations

C.

Chloroflexus

CcO

cytochrome c oxidase

DMS

dimethylsulfide

DMSO

dimethylsulfoxide

E.

Escherichia

HiPIP

high-potential iron-sulfur protein

Rba.

Rhodobacter

RC

photochemical reaction center

Rps.

Rhodopseudomonas

Rsb.

Roseobacter

Rvu.

Rhodovulum

T

Thermus

TMAO

trimethylamine-N-oxide

TMPD

N,N,N′,N′-tetramethyl-p-phenylenediamine

UQ

ubiquinone

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References

  1. Ädelroth P and Brzezinski P (2004) Surface-mediated protontransfer reactions in membrane-bound proteins. Biochim Biophys Acta 1655: 102–115PubMedGoogle Scholar
  2. Ädelroth P and Hosler JP (2006) Surface proton donors for the D-pathway of cytochrome c oxidase in the absence of subunit III. Biochemistry 45: 8308–8318PubMedGoogle Scholar
  3. Ädelroth P, Gennis RB and Brzezinski P (1998) Role of the pathway through K(I-362) in proton transfer in cytochrome c oxidase from R. sphaeroides. Biochemistry 37: 2470–2476PubMedGoogle Scholar
  4. Afkar E, Lisak J, Saltikov C, Basu P, Oremland RS and Stolz JF (2003) The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiol Lett 226: 107–112PubMedGoogle Scholar
  5. Anderson G, Williams J and Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J Biol Chem 267: 23674–23682PubMedGoogle Scholar
  6. Arata H, Shimizu M and Takamiya K (1992) Purification and properties of trimethylamine-N-oxide reductase from the aerobic photosynthetic bacterium Roseobacter denitrificans. J Biochem 112: 470–475PubMedGoogle Scholar
  7. Babcock GT (1999) How oxygen is activated and reduced in respiration. Proc Natl Acad Sci USA 96: 12971–12973PubMedGoogle Scholar
  8. Baymann F, Brugna M, Muhlenhoff U and Nitschke W (2001) Daddy, where did (PS)I come from? Biochim Biophys Acta 1507: 291–310PubMedGoogle Scholar
  9. Baymann F, Lebrun E, Brugna M, Schoepp-Cothenet B, Giudici-Orticoni M-T and Nitschke W (2003) The redox protein construction kit: Pre-last universal common ancestor evolution of energy-conserving enzymes. Phil Trans Roy Soc Lond B 358: 267–274Google Scholar
  10. Bender KS, Shang C, Chakraborty R, Belchik SM, Coates JD and Achenbach LA (2005) Identification, characterization, and classification of genes encoding perchlorate reductase. J Bacteriol 187: 5090–5096PubMedGoogle Scholar
  11. Bertero MG, Rothery RA, Palak M, Hou C, Lim D, Blasco F, Weiner JH and Strynadka NCJ (2003) Insights into the respiratory electron transfer pathway from the structure of nitrate reductase A. Nature Struct Biol 10: 681–687PubMedGoogle Scholar
  12. Blankenship RE and Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23: 94–97PubMedGoogle Scholar
  13. Blasco G, Guigliarelli B, Magalon A, Asso M, Giordano G and Rothery RA (2001) The coordination and function of the redox centers of the membrane bound nitrate reductases. Cell Molec Life Sci 58: 179–193PubMedGoogle Scholar
  14. Bonora P, Principi I, Hochkoeppler A, Borghese R and Zannoni D (1998) The respiratory chain of the halophilic anoxygenic purple bacterium Rhodospirillum sodomense. Arch Microbiol 170: 435–441PubMedGoogle Scholar
  15. Borisov VB, Liebl U, Rappaport F, Martin JL, Zhang J, Gennis RB, Konstantinov AA and Vos MH (2002) Interactions between heme d and heme b 595 in quinol oxidase bd from Escherichia coli: A photoselection study using femtosecond spectroscopy. Biochemistry 41: 1654–1662PubMedGoogle Scholar
  16. Borsetti F, Francia F, Turner RJ and Zannoni D (2007) The thiol: disulfide oxidoreductase DsbB mediates the oxidizing effects of the toxic metalloid tellurite on the plasma membrane redox system of the facultative phototroph Rhodobacter capsulatus. J Bacteriol 189: 851–859PubMedGoogle Scholar
  17. Branden G, Gennis RB and Brzezinski P (2006a) Transmembrane proton translocation by cytochrome c oxidase. Biochim Biophys Acta 1757: 1052–1063PubMedGoogle Scholar
  18. Branden G, Pawate AS, Gennis RB and Brzezinski P (2006b) Controlled uncoupling and recoupling of proton pumping in cytochrome c oxidase. Proc Natl Acad Sci USA 103: 317–322PubMedGoogle Scholar
  19. Brasier MD, Green OR, Jephcoat AP, Kleppe AK, Van Kranendonk MJ, Lindsay JF, Steele A and Grassineau NV (2002) Questioning the evidence for Earth’s oldest fossils. Nature 616: 76–81Google Scholar
  20. Bratton MR, Pressler MA and Hosier JP (1999) Suicide inactivation of cytochrome c oxidase: Catalytic turnover in the absence of subunit III alters the active site. Biochemistry 38: 16236–16245PubMedGoogle Scholar
  21. Bratton MR, Hiser L, Antholine WE, Hoganson C and Hosier JP (2000) Identification of the structural subunits required for formation of the metal centers in subunit I of cytochrome c oxidase of Rhodobacter sphaeroides. Biochemistry 39: 12989–12995PubMedGoogle Scholar
  22. Brochier C and Philippe H (2002) Phylogeny: A non hyperthermophilic ancestor for bacteria. Nature 417: 244PubMedGoogle Scholar
  23. Candela M, Zaccherini E and Zannoni D (2001) Respiratory electron transport and light induced energy transduction in membranes from the photosynthetic bacterium Roseobacter denitrificans. Arch Microbiol 175: 169–177Google Scholar
  24. Castresana J (2001) Comparative genomics and bioenergetics. Biochim Biophys Acta 1506: 147–162PubMedGoogle Scholar
  25. Cavalier-Smith T (2001) Obcells as proto-organisms: Membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cell, and photosynthesis. J Mol Evol 53: 555–595PubMedGoogle Scholar
  26. Ciurli S and Musiani F (2005) High potential iron-sulfur proteins and their role as soluble electron carriers in bacterial photosynthesis: Tale of a discovery. Photosynth Res 85: 115–131PubMedGoogle Scholar
  27. Cotton NJP, Clark AJ and Jackson JB (1983) Interaction between the respiratory and photosynthetic electron transport chains of intact cells of Rhodopseudomonas capsulata mediated by membrane potential. Eur J Biochem 130: 581–587PubMedGoogle Scholar
  28. Cox RL, Patterson C and Donohue T.I (2001) Roles for the Rhodobacter sphaeroides CcmA and CcmG proteins. J Bacteriol 183: 4643–4647PubMedGoogle Scholar
  29. Cramer WA and Knaff DB (1990) Energy Transduction in Biological Membranes. A Textbook of Bioenergetics. Springer-Verlag, New YorkGoogle Scholar
  30. Daldal F, Mandaci S, Winterstein C, Myllykallio H, Duyck K and Zannoni D (2001) Mobile cytochrome c 2 and membrane-anchored cytochrome c y are both efficient electron donors to the cbb 3- and aa 3-type cytochrome c oxidases during respiratory growth of Rhodobacter sphaeroides. J Bacteriol 183: 2013–2024PubMedGoogle Scholar
  31. Danielsson Thorell H, Beyer NH, Heegaard NH, Ohman M and Nilsson T (2004) Comparison of native and recombinant chlorite dismutase from Ideonella dechloratans. Eur J Biochem 271: 3539–3346PubMedGoogle Scholar
  32. D’Mello R, Hill S and Poole RK (1994) Determination of the oxygen affinities of terminal oxidases in Azotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin: Cytochrome bd is a low affinity oxidase. Microbiology 140: 1395–1402Google Scholar
  33. D’Mello R, Hill S and Poole RK (1996) The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: Implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142: 755–763PubMedGoogle Scholar
  34. Drosou V, Reincke B, Schneider M and Ludwig B (2002) Specificity of the interaction between the Paracoccus denitrificans oxidase and its substrate cytochrome c: Comparing the mitochondrial to the homologous bacterial cytochrome c 552, and its truncated and site-directed mutants. Biochemistry 41: 10629–10634PubMedGoogle Scholar
  35. Dueweke TJ and Gennis RB (1991) Proteolysis of the cytochrome d complex with trypsin and chymotrypsin localizes a quinol oxidase domain. Biochemistry 30: 3401–3406PubMedGoogle Scholar
  36. Dupuis A, Prieur I and Lunardi J (2001) Toward a characterization of the connecting module of complex I. J Bioenerg Biomembr 33: 159–168PubMedGoogle Scholar
  37. Ellis PT, Conrads T, Hille R and Kuhn P (2001) Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.6 Å and 2.03 Å. Structure 9: 125–132PubMedGoogle Scholar
  38. Ferguson SJ and Richardson DJ (2004) The enzymes and bioenergetics of bacterial nitrate, nitrite, nitric oxide and nitrous oxide respiration. In: Zannoni D (ed) Respiration in Archaea and Bacteria. Diversity of Prokaryotic Respiratory Systems (Advances in Photosynthesis and Respiration, Vol 16), pp 169–206 Springer, DordrechtGoogle Scholar
  39. Fetter JR, Qian J, Shapleigh J, Thomas JW, Garcia-Horsman A, Schmidt E, Hosier J, Babcock GT, Gennis RB and Ferguson-Miller S (1995) Possible proton relay pathways in cytochrome c oxidase. Proc Natl Acad Sci USA 92: 1604–1608PubMedGoogle Scholar
  40. Finel M (1996) Genetic inactivation of the H+-translocating NADH:ubiquinone oxidoreductase of Paracoccus denitrificans is facilitated by insertion of the ndh gene fromEscherichia coli. FEBS Lett 393: 81–85PubMedGoogle Scholar
  41. Friedrich T and Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479: 1–5PubMedGoogle Scholar
  42. García-Horsman JA, Barquera B and Escamilla JE (1991) Two different aa 3-type cytochromes can be purified from the bacterium Bacillus cereus. Eur J Biochem 199: 761–768PubMedGoogle Scholar
  43. García-Horsman JA, Barquera B, Rumbley J, Ma J and Gennis R (1994) The superfamily of heme-copper respiratory oxidases. J Bacteriol. 176: 5587–5600PubMedGoogle Scholar
  44. Gilderson G, Salomonsson L, Aagaard A, Gray J, Brzezinski P and Hosier J (2003) Subunit III of cytochrome c oxidase of Rhodobacter sphaeroides is required to maintain rapid proton uptake through the D pathway at physiologic pH. Biochemistry 42: 7400–7409PubMedGoogle Scholar
  45. Gon S, Giudici-Orticoni MT, Mejean V and Iobbi-Nivol C (2001) Electron transfer and binding of the c-type cytochrome TorC to the trimethylamine-N-oxide reductase of Escherichia coli. J Bacteriol 182: 5779–5786Google Scholar
  46. Hanlon SP, Holt RA, Moore GR and McEwan AG (1994) Isolation and characterization of a strain of Rhodobacter sulfidophilus: A bacterium which grows autotrophically with dimethylsulfide as electron donor. Microbiology 140: 1953–1958Google Scholar
  47. Hemp J, Christian C, Barquera B, Gennis RB and Martinez TJ (2005) Helix switching of akey active-site residue in the cytochrome cbb 3 oxidases. Biochemistry 44: 10766–10775PubMedGoogle Scholar
  48. Hemp J, Robinson DE, Ganesan KB, Martinez TJ, Kelleher NL and Gennis RB (2006) Evolutionary migration of a post-translationally modified active-site residue in the proton-pumping heme-copper oxygen reductases. Biochemistry 45: 15405–15410PubMedGoogle Scholar
  49. Herter SM, Kortlüle CM and Drews G (1998) Complex I of Rhodobacter capsulatus and its role in reverted electron transport. Arch Microbiol 169: 98–105PubMedGoogle Scholar
  50. Hill BC (1994) Modeling the sequence of electron transfer reactions in the single turnover of reduced, mammalian cytochrome c oxidase with oxygen. J Biol Chem 269: 2419–2425PubMedGoogle Scholar
  51. Hiser L, Di Valentin M, Hamer AG and Hosier JP (2000) Cox 11p is required for stable formation of the CuB and magnesium centers of cytochrome c oxidase. J Biol Chem 275: 619–623PubMedGoogle Scholar
  52. Hochkoeppler A, Ciurli S, Venturoli G and Zannoni D (1995a) The high potential iron-sulphur protein (HiPIP) from Rhodoferax fermentons is competent in photosynthetic electron transfer. FEBS Lett 357: 70–74PubMedGoogle Scholar
  53. Hochkoeppler A, Jenney FE, Jr., Lang SE, Zannoni D and Daldal F (1995b) Membrane-associated cytochrome c y of Rhodobacter capsulatus is an electron carrier from the cytochrome bc 1 complex to the cytochrome c oxidase during respiration. J Bacteriol 177: 608–613PubMedGoogle Scholar
  54. Hochkoeppler A, Moschettini G and Zannoni D (1995c) The electron transport system of the facultative phototrophic bacterium Rhodoferax fermentans. I. A functional, thermodynamic and spectroscopic study of the membrane bound respiratory chain of dark- and light-grown cells. Biochim Biophys Acta 1229: 73–80Google Scholar
  55. Hochkoeppler A, Principi I, Bonora P, Ciurli S and Zannoni D (1999) On the role of soluble redox carriers alternative to cytochrome c 2 as donors to tetraheme-type reaction centers and cytochrome oxidases. In: Peschek GA, Loffelhardt W and Schmetterer G (eds) The Phototrophic Prokaryotes, pp 293–302. Kluwer Academic / Plenum Publishers, New YorkGoogle Scholar
  56. Holland HD (1994) Early proterozoic atmospheric change. In: Bengtson S (ed) Early Life on Earth, pp 237–244. Columbia University Press, New YorkGoogle Scholar
  57. Hosler JP (2004) The influence of subunit III of cytochrome c oxidase on the D pathway, the proton exit pathway and mechanism-based inactivation in subunit I. Biochim Biophys Acta 1655: 332–339PubMedGoogle Scholar
  58. Hosier JP, Ferguson-Miller S, Calhoun MW, Thomas JW, Hill J, Lemieux L, Ma J, Georgiou C, Fetter J, Shapleigh J, Teklenburg MMJ, Babcock GT and Gennis RB (1993) Insight into the active-site structure and function of cytochrome oxidase by analysis of site-directed mutants of bacterial cytochrome aa 3 and cytochrome bo. J Bioenerg Biomembr 25: 121–136Google Scholar
  59. Hosier JP, Ferguson-Miller S and Mills DA (2006) Energy transduction: Proton transfer through the respiratory complexes. Annu Rev Biochem 75: 165–187Google Scholar
  60. Imhoff JF, Petri R and Suling J (1998) Reclassification of species of the spiral-shaped phototrophic purple non-sufur bacteria of the alpha-Proteobacteria: Description of the new genera Paeospirillum gen. nov., Rhodovibrio gen. nov., Rhodothalassium gen. nov. and Roseospira gen. nov. as well as transfer of Rhodospirillum fulvum to Phaeospirillum fulvum comb. nov., of Rhodospirillum molischianum to Paeospirillum molischianum com. nov, of Rhodospirillum salinarum to Rhodovibrio salexigens. Int J Syst Bacteriol 48: 793–798PubMedCrossRefGoogle Scholar
  61. Iobbi-Nivol C, Pommier J, Simala-Grant J, Mejean V and Giordano G (1996) High substrate specificity and induction characteristics of trimethylamine-N-oxide reductase of Escherichia coli. Biochim Biophys Acta 1294: 157–162Google Scholar
  62. Jenney Jr. FE and Daldal F (1993) A novel membrane-associated c-type cytochrome Cyt c y, can mediate the photosynthetic growth of Rhodobacter capsuatus and Rhodobacter sphaeroides. EMBO J 12: 1283–1292PubMedGoogle Scholar
  63. Johnson KE and Rajagopalan KV (2001) An active site tyrosine influences the ability of the dimethylsulfoxide reductase family of molybdopterin enzymes to reduce S-oxides. J Biol Chem 276: 13178–13185PubMedGoogle Scholar
  64. Jormakka M, Richardson D, Byrne B and Iwata S (2004) Architecture of NarGH reveals a structural classification of Mo-bisMGD enzymes. Structure 12: 95–104PubMedGoogle Scholar
  65. Junemann S (1997) Cytochrome bd terminal oxidase. Biochim Biophys Acta 1321: 107–127PubMedGoogle Scholar
  66. Jungst A, Wakabayashi S, Matsubara H and Zunft WG (1991) The nirSTBM region coding for cytochrome cd 1-dependent nitrite respiration in Pseudomonas stutzeri consists of a cluster of mono-, di-, and tetraheme proteins. FEBS Lett 279: 205–209PubMedGoogle Scholar
  67. Kelly DP and Smith NA (1990) Organic sulphur compounds in the environment-biogeochemistry, microbiology, and ecological aspects. Adv Microb Ecol 11: 345–385Google Scholar
  68. Kloer DP, Hagel C, Heider J and Schulz GE (2006) Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14: 1377–1388PubMedGoogle Scholar
  69. Kniemeyer O and Heider J (2001) Ethylbenzene dehydrogenase, anovel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 276: 21381–21386PubMedGoogle Scholar
  70. Koch HG, Hwang O and Daldal F (1998) Isolation and characterization of Rhodobacter capsulatus mutants affected in cytochrome cbb 3 oxidase activity. J Bacteriol 180: 969–978PubMedGoogle Scholar
  71. Krafft T and Macy JM (1998) Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. Eur J Biochem 255: 647–653PubMedGoogle Scholar
  72. Krafft T, Bokranz M, Klimmer O, Schröder I, Fahrenholz F, Kojro E and Kröger A (1992) Cloning and nucleodide sequence of the psrA gene of Wolinella succinogenes polysulphide reductase. Eur J Biochem 206: 503–510PubMedGoogle Scholar
  73. Lebrun E, Brugna M, Baymann F, Muller D, Lievremont D, Lett M-C and Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20: 686–693PubMedGoogle Scholar
  74. Lebrun E, Santini JM, Brugna M, Ducluzeau AL, Ouchane S, Schoepp-Cothenet B, Baymann F and Nitschke W (2006) The Rieske-protein: A case study on the pitfalls of multiple sequence alignments and phylogenetic reconstruction. Mol Biol Evol 23: 1180–1191PubMedGoogle Scholar
  75. Lemon DD, Calhoun MW, Gennis RB and Woodruff WH (1993) The gateway to the active site of heme-copper oxidases. Biochemistry 32: 11953–11956PubMedGoogle Scholar
  76. Madigan MT, Martinko JM and Parker J (1997) Brock. Biology of Microorganisms. 10th Edition. Printice Hall, Upper Saddle RiverGoogle Scholar
  77. 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 and Kaplan S (2001) The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth Res 70: 19–41PubMedGoogle Scholar
  78. McDevitt CA, Hugenholtz P, Hanson GR and McEwan AG (2002a) Molecular analysis of dimethylsulfide dehydrogenase from Rhodovulum sulfidophilum; its place in the DMSO reductase family of microbial molybdenum-containing enzymes. Mol Microbiol 44: 1576–1587Google Scholar
  79. McDevitt CA, Hanson GR, Noble CJ, Cheesman MR and McEwan AG (2002b) Characterization of the redox centers in dimethyl sulfide dehydrogenase from Rhodovulum sulfidophilum. Biochemistry 41: 15234–15244PubMedGoogle Scholar
  80. McEwan AG, Cotton NPJ, Ferguson SJ and Jackson JB (1985) The role of auxiliary oxidants in the maintenance of balanced redox poise for photosynthesis in bacteria. Biochim Biophys Acta 810: 140–147Google Scholar
  81. McEwan AG, Ridge JP, McDevitt CA and Hugenholtz P (2002) The DMSO reductase family of microbial molybdenum enzymes; molecular properties and role in the dissimilatory reduction of toxic elements. Geomicrobiol J 19: 3–21Google Scholar
  82. McEwan AG, Kappler U and McDevitt CA (2004) Microbial molybdenum-containing enzymes in respiration: structural and functional aspects. In: Zannoni D (ed) Respiration in Archaea and Bacteria. Diversity of Prokaryotic Electron Transport Carriers (Advances in Photosynthesis and Respiration, Vol 15), pp 175–202. Kluwer Academic Publishers, DordrechtGoogle Scholar
  83. Meyer TE and Cusanovich MA (1985) Soluble cytochrome composition of the purple phototrophic bacterium Rhodopseudomas sphaeroides ATCC 17023. Biochim Biophys Acta 807: 308–391PubMedGoogle Scholar
  84. Meyer TE and Donohue TJ (1995) Cytochromes, iron-sulfur, and copper proteins mediating electron transfer from Cyt bc 1 complex to photosynthetic reaction center complexes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria (Advances in Photosynthesis and Respiration, Vol 2), pp 725–745. Kluwer Academic Publishers, DordrechtGoogle Scholar
  85. Mills DA, Schmidt B, Hiser C, Westley E and Ferguson-Miller S (2002) Membrane potential-controlled inhibition of cytochrome c oxidase by zinc. J Biol Chem. 277: 14894–14901PubMedGoogle Scholar
  86. Mills DA and Hosier JP (2005) Slow proton transfer through the pathways for pumped protons in cytochrome c oxidase induces suicide inactivation of the enzyme. Biochemistry 44: 4656–4666PubMedGoogle Scholar
  87. Mills DA, Tan Z, Ferguson-Miller S and Hosler J (2003) A role for subunit III in proton uptake into the D pathway and a possible proton exit pathway in Rhodobacter sphaeroides cytochrome c oxidase. Biochemistry 42: 7410–7417PubMedGoogle Scholar
  88. Mills DA, Geren L, Hiser C, Schmidt B, Durham B, Millett F and Ferguson-Miller S (2005) An arginine to lysine mutation in the vicinity of the heme propionates affects the redox potentials of the hemes and associated electron and proton transfer in cytochrome c oxidase. Biochemistry 44: 10457–10465PubMedGoogle Scholar
  89. Mogi T, Akimoto S, Endou S, Watanabe-Nakayama T, Mizuochi-Asai E and Miyoshi H (2006) Probing the ubiquinol-binding site in cytochrome bd by site-directed mutagenesis. Biochemistry 45: 7924–7930PubMedGoogle Scholar
  90. Moore MD and Kaplan S (1992) Identification of intrinsic high-level resistance to rare-earth oxides and oxyanions in members of the class Proteobacteria: Characterization of tellurite, selenite, and rhodium sesquioxide reduction in Rhodobacter sphaeroides. J Bacteriol 174: 1505–1514PubMedGoogle Scholar
  91. Morgan JE, Verkhovsky MI, Palmer G and Wikström M (2001) Role of the Pr intermediate in the reaction of cytochrome c oxidase with O2. Biochemistry 40: 6882–6892PubMedGoogle Scholar
  92. Moschettini G, Bonora P, Zaccherini E, Hochkoeppler A, Principi I and Zannoni D (1999) The primary quinone acceptor and the membrane-bound c-type cytochromes of the halophilic purple nonsulfur bacterium Rhodospirillum salinarum: a spectroscopic and thermodynamic study. Photosynth Research 62: 43–53Google Scholar
  93. Mouncey NJ, Gak E, Choudhary M, Oh J and Kaplan S (2000) Respiratory pathways of Rhodobacter sphaeroides 2.4.1T: Identification and characterization of genes encoding quinol oxidases. FEMS Microbiol Lett 192: 205–210PubMedGoogle Scholar
  94. Mukhopadhyay R, Rosen BP, Phung LT and Silver S (2002) Microbial arsenic: From geocycles to genes and enzymes. FEMS Microbiol Rev 26: 311–325PubMedGoogle Scholar
  95. Muller D, Lièvremont D, Dancheva Simeonova D, Hubert J-C and Lett M-C (2003) Arsenite oxidase aox genes from a metal-resistant !-proteobacterium. J Bacteriol 185: 135–141PubMedGoogle Scholar
  96. Namslauer A and Brzezinski P (2004) Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase. FEBS Lett. 567: 103–110PubMedGoogle Scholar
  97. Nitschke W, Muhlenhoff U and Liebl U (1997) Evolution. In: Raghavendra A (ed) Photosynthesis: A Comprehensive Treatise, pp 285–304. Cambridge University Press, CambridgeGoogle Scholar
  98. Oh JI (2006) Effect of mutations of five conserved histidine residues in the catalytic subunit of the cbb 3 cytochrome c oxidase on its function. J Microbiol 44: 284–292PubMedGoogle Scholar
  99. Oh JI and Kaplan S (1999) The cbb 3 terminal oxidase of Rhodobacter sphaeroides 2.4.1: Structural andfunctional implications for the regulation of spectral complex formation. Biochemistry 38: 2688–2696PubMedGoogle Scholar
  100. Oh JI and Kaplan S (2002) Oxygen adaptation. The role of the CcoQ subunit of the cbb 3 cytochrome c oxidase of Rhodobacter sphaeroides 2.4.1. J Biol Chem 277: 16220–16228PubMedGoogle Scholar
  101. Oh JI, Ko IJ and Kaplan S (2004) Reconstitution of the Rhodobacter sphaeroides cbb 3-PrrBA signal transduction pathway in vitro. Biochemistry 43: 7915–7923PubMedGoogle Scholar
  102. Ohmoto H (1996) Evidence in pre-2.2 Gapaleosols for the early evolution of atmospheric oxygen and terrestrial biota. Geology 24: 1135–1138PubMedGoogle Scholar
  103. Ohmoto H (1997) When did the Earth’s atmosphere become oxic?. Geochemical News 93: 12–29Google Scholar
  104. Olson JM (1999) Early evolution in chlorophyll-basedphotosynthesis. Chemtracts 12: 468–482Google Scholar
  105. Oremland RS and Stolz JF (2003) The ecology of Arsenic. Science 300: 939–944PubMedGoogle Scholar
  106. Oremland RS and Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends in Microbiology 13: 45–49PubMedGoogle Scholar
  107. Oremland RS, Blum JS, Culbertson CW, Visscher PT, Miller LG, Dowdle P and Strohmaier FE (1994) Isolation, growth, and metabolism of an obligately anaerobic, selenate-respiring bacterium, strain SES-3. Appl Environ Microbiol 60: 3011–3019PubMedGoogle Scholar
  108. Oremland RS, Hoeft SE, Santini JM, Bano N, Hollibaugh RA and Hollibaugh RT (2002) Anaerobic oxidation of arsenite in Mono Lake water and by a facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Appl Environ Microbiol 68: 4795–4802PubMedGoogle Scholar
  109. Pappas CT, Sram J, Moskvin OV, Ivanov PS, Mackenzie RC, Choudhary M, Land ML, Larimer FW, Kaplan S and Gomelsky M (2004) Construction and validation of the Rhodobacter sphaeroides 2.4.1 DNA microarray: Transcriptome flexibility at diverse growth modes. J Bacteriol 186: 4748–4758PubMedGoogle Scholar
  110. Pawate AS, Morgan J, Namslauer A, Mills D, Brzezinski P, Ferguson-Miller S and Gennis RB (2002) A mutation in subunit I of cytochrome oxidase from Rhodobacter sphaeroides results in an increase in steady-state activity but completely eliminates proton pumping. Biochemistry 41: 13417–13423PubMedGoogle Scholar
  111. Pils D and Schmetterer G (2001) Characterization of three bioenergetically active respiratory terminal oxidases in the cyanobacterium Synechocystis sp. Strain PCC 6803. FEMS Microbiol Lett 203: 217–222PubMedGoogle Scholar
  112. Pitcher RS and Watmough NJ (2004) The bacterial cytochrome cbb 3 oxidases. Biochim Biophys Acta 1655: 388–399PubMedGoogle Scholar
  113. Poole RK, Lloyd D and Chance B (1979) The reaction of cytochrome oxidase with oxygen in the fission yeast Schizosac-charomyces pombe 972H-. Studies at subzero temperatures and measurement of apparent oxygen affinity. Biochem J 184: 555–563PubMedGoogle Scholar
  114. Preisig O, Zufferey R, Thoeny-Meyer L, Appleby CA and Hennecke H (1996) A high-affinity cbb 3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178: 1532–1538PubMedGoogle Scholar
  115. Proshlyakov DA (2004) UV optical absorption by protein radicals in cytochrome c oxidase. Biochim Biophys Acta 1655: 282–289PubMedGoogle Scholar
  116. Proshlyakov DA, Pressler MA and Babcock GT (1998) Dioxygen activation and bond cleavage by mixed-valence cytochrome c oxidase. Proc Natl Acad Sci USA 95: 8020–8025PubMedGoogle Scholar
  117. Proshlyakov DA, Pressler MA, DeMaso C, Leykam JF, DeWitt DL and Babcock GT (2000) Oxygen activation and reduction in respiration: Involvement of redox-active tyrosine 244. Science 290: 1588–1591PubMedGoogle Scholar
  118. Qin L, Hiser C, Mulichak A, Garavito RM and Ferguson-Miller S (2006) Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase. Proc Natl Acad Sci USA 103: 16117–16122PubMedGoogle Scholar
  119. Rauhamaki V, Baumann M, Soliymani R, Puustinen A and Wikström M (2006) Identification of ahistidine-tyrosine cross-link in the active site of the cbb 3-type cytochrome c oxidase from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 103: 16135–16140PubMedGoogle Scholar
  120. Reysenbach AL and Shock E (2002) Merging genomes with geochemistry in hydrothermal ecosystems. Science 296: 1077–1082PubMedGoogle Scholar
  121. Richardson DJ (2000) Bacterial respiration: a flexible process for a changing environment. Microbiology 146: 551–571PubMedGoogle Scholar
  122. Richardson DJ, Bell LC, McEwan AG, Jackson JB and Ferguson SJ (1991) Cytochrome c 2 is essential for electron transfer to nitrous oxide reductase from physiological substrates in Rhodobacter capsulatus and acts as electron donor to the reductase in vivo. Correlation with photoinhibition studies. Eur J Biochem 199: 677–683PubMedGoogle Scholar
  123. Richaud P, Marrs BL and Verméglio A (1986) Two modes of interaction between photosynthetic and respiratory electron chains in whole cells of Rhodopseudomonas capsulata. Biochim Biophys Acta 850: 256–263Google Scholar
  124. Richter OM and Ludwig B (2003) Cytochrome c oxidase-structure, function, and physiology of a redox-driven molecular machine. Rev Physiol Biochem Pharmacol 147: 47–74PubMedGoogle Scholar
  125. Riistama S, Puustinen A, Verkhovsky MI, Morgan JE and Wikström M (2000) Binding of O2 and its reduction are both retarded by replacement of valine 279 by isoleucine in cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39: 6365–6372PubMedGoogle Scholar
  126. Rott MA, Witthuhn VC, Schike BA, Soranno M, Ali A and Donohue TJ (1993) Genetic evidence for the role of isocytochrome c 2 in photosynthetic growth of Rhodobacter sphaeroides spd mutants. J Bacteriol 175: 358–366PubMedGoogle Scholar
  127. Rugolo M and Zannoni D (1983) Oxygen induced inhibition of light dependent uptake of tetraphenylphosphonium ions as a probe of a direct interaction between photosynthetic and respiratory components in cells of Rhodopseudomonas capsulata. Biochem Biophys Res Commun 113: 155–162PubMedGoogle Scholar
  128. Ruitenberg M, Kannt A, Bamberg E, Ludwig B, Michel H and Fendler K (2000) Single-electron reduction of the oxidized state is coupled to proton uptake via the K pathway in Paracoccus denitrificans cytochrome c oxidase. Proc Natl Acad Sci USA 97: 4632–4636PubMedGoogle Scholar
  129. Sabaty M, Gans P and Verméglio A (1993) Inhibition of nitrate reduction by light and oxygen in Rhodobacter sphaeroides forma sp. denitrificans. Arch Microbiol 159: 153–159Google Scholar
  130. Sabaty M, Jappé J, Olive J and Verméglio A (1994) Organization of electron transfer components in Rhodobacter sphaeroides forma sp. denitrificans. Biochim Biophys Acta 1187: 313–323Google Scholar
  131. Sabaty M, Avazéri C, Pignol D and Verméglio A (2001) Characterization of the reduction of selenate and tellurite by nitrate reductases. Appl Environ Microbiol 67: 5122–5126PubMedGoogle Scholar
  132. Saitou N and Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425PubMedGoogle Scholar
  133. Santini JM and vanden Hoven RN (2004) Molybdenum-containing arsenite oxidase of the chemolithoautotrophic arsenite oxidizer NT-26. J Bacteriol 186: 1614–1619PubMedGoogle Scholar
  134. Santini JM, Sly LI, Schnagl RD and Macy JM (2000) A new chemolithoautotropic arsenite-oxidizing bacterium isolated from a gold mine: Phylogenetic, physiological, and preliminary biochemical studies. App Env Microbiol 66: 92–97Google Scholar
  135. Santini JM, Kappler U, Ward SA, Honeychurch MJ, van den Hoven RN and Bernhard PV (2007) The NT-26 cytochrome c552 and its role in arsenite oxidation. Biochim Biophys Acta 1767: 189–196PubMedGoogle Scholar
  136. Sazanov LA and Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311: 1430–1436PubMedGoogle Scholar
  137. Shapleigh J, Hosier JP, Tecklenburg MJ, Ferguson-Miller S, Babcock GT and Gennis RB (1992) Identification of the heme axial ligands for the cytochrome a component of cytochrome c oxidase. Proc Natl Acad Sci USA 89: 4786–4790PubMedGoogle Scholar
  138. Sharma V, Puustinen A, Wikström M and Laakkonen L (2006) Sequence analysis of the cbb 3 oxidases and an atomic model for the Rhodobacter sphaeroides enzyme. Biochemistry 45: 5754–5765PubMedGoogle Scholar
  139. Sharpe M, Qin L and Ferguson-Miller S (2005) Proton entry, exit and pathways in cytochrome oxidase: Insight from ‘conserved’ water. In: Wikström M (ed) Biophysical and Structural Aspects of Bioenergetics, pp 26–54. RSC Publishing, CambridgeGoogle Scholar
  140. Shaw AL, Hanson GR and McEwan AG (1996) Cloning and sequence analysis of the dimethylsulfoxide reductase structural gene from Rhodobacter capsulatus. Biochim Biophys Acta 1276: 176–180PubMedGoogle Scholar
  141. Shaw AL, Hochkoeppler A, Bonora P, Zannoni D, Hanson GR and McEwan AG (1999a) Characterization of DorC from Rhodobacter capsulatus, a c-type cytochrome involved in electron transfer to dimethylsulfoxide reductase. J Biol Chem 274: 9911–9914PubMedGoogle Scholar
  142. Shaw AL, Leimkuehler S, Klipp W, Hanson GR and McEwan AG (1999b) Mutational analysis of the dimethylsulfoxide respiratory (dor) operon of Rhodobacter capsulatus. Microbiol 145: 1409–1420Google Scholar
  143. Schopf JW, Kudryavtsev AB, Agresti DG, Wdowiak TJ and Czaja AD (2002) Laser-Raman imagery of Earth’s earliest fossils. Nature 416: 73–76PubMedGoogle Scholar
  144. Schröder I, Rech S, Krafft T and Macy JM (1997) Purification and characterization of the selenate reductase from Thauera selenatis. J Biol Chem 272: 23765–23768PubMedGoogle Scholar
  145. Smith D, Gray J, Mitchell L, Antholine WE and Hosler JP (2005) Assembly of cytochrome c oxidase in the absence of assembly protein Surf lp leads to loss of the active site heme. J Biol Chem 280: 17652–17656PubMedGoogle Scholar
  146. Stiburek L, Vesela K, Hansikova H, Pecina P, Tesarova M, Cerna L, Houstek J and Zeman J (2005) Tissue-specific cytochrome c oxidase assembly defects due to mutations in Sco2 and Surf1. Biochem J 392: 625–632PubMedGoogle Scholar
  147. Stolz JF and Oremland RS (1999) Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev 23: 615–627PubMedGoogle Scholar
  148. Stolz JF, Basu P, Santini JM and Oremland RS (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60: 107–130PubMedGoogle Scholar
  149. Svensson-Ek M, Abramson J, Larsson G, Tornroth S, Brzezinski P and Iwata S (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J Mol Biol 321: 329–339PubMedGoogle Scholar
  150. Swem LR, Gong X, Yu CA and Bauer CE (2006) Identification of a ubiquinone-binding site that affects autophosphorylation of the sensor kinase RegB. J Biol Chem 281: 6768–6775PubMedGoogle Scholar
  151. Switzer Blum J, Burns Bindi A, Buzzeli J, Stolz JF and Oremland RS (1998) Bacillus arsenicoselenatis, sp. nov., and Bacillus selenitireducens, sp. nov.: Two haloalkaliphiles from Mono Lake, California that respire oxyanions of selenium and arsenic. Arch Microbiol 171: 19–30PubMedGoogle Scholar
  152. Takamiya K, Iba K and Okamura K (1987) Reaction center complex from an aerobic photosynthetic bacterium Erythrobacter species OCh114. Biochim Biophys Acta 890: 127–133Google Scholar
  153. Taylor BF and Kiene RP (1989) Microbial-metabolism of dimethylsulfide. ACS Symposium Series 393: 202–221CrossRefGoogle Scholar
  154. Thöny-Mayer L (1997) Biogenesis of respiratory cytochromes in bacteria. Microbiol Mol Biol Rev 61: 337–376Google Scholar
  155. Toledo-Cuevas M, Barquera B, Gennis RB, Wikström M and García-Horsman JA (1998) The cbb 3-type cytochrome c oxidase from Rhodobacter sphaeroides, a proton-pumping heme-copper oxidase. Biochim Biophys Acta 1365: 421–434PubMedGoogle Scholar
  156. Tomson FL, Morgan JE, Gu G, Barquera B, Vygodina TV and Gennis RB (2003) Substitutions for glutamate 101 in subunit II of cytochrome c oxidase from Rhodobacter sphaeroides result in blocking the proton-conducting K-channel. Biochemistry 42: 1711–1717PubMedGoogle Scholar
  157. Towe KM (1990) Aerobic respiration in the Archaean? Nature 348: 54–56PubMedGoogle Scholar
  158. Towe KM (1994) Earth’s early atmosphere: Constraints and opportunities for early evolution. In: Bengston S (ed) Early Life on Earth, pp. 36–47. Columbia University Press, New YorkGoogle Scholar
  159. Towe KM (1996) Environmental oxygen conditions during the origina and early evolution of life. Adv Space Res 18: 7–15Google Scholar
  160. Trieber CA, Rothery RA and Weiner JH (1996) Engineering a novel iron-sulfur cluster into the catalytic subunit of Escherichia coli dimethyl-sulfoxide reductase. J Biol Chem 271: 4620–4626PubMedGoogle Scholar
  161. Unemoto T and Hayashi M (1993) Na+-translocating NADH-quinone reductase of marine and halophilic bacteria. J Bioenerg Biomembr 25: 385–391PubMedGoogle Scholar
  162. vanden Hoven RN and Santini JM (2004) Arsenite oxidation by the heterotroph Hydrogenophaga sp. str. NT-14: the arsenite oxidase and its physiological electron acceptor. Biochim Biophys Acta 1656: 148–155Google Scholar
  163. Varanasi L, Mills D, Murphree A, Gray J, Purser C, Baker R and Hosier J (2006) Altering conserved lipid binding sites in cytochrome c oxidase of Rhodobacter sphaeroides perturbs the interaction between subunits I and III and promotes suicide inactivation of the enzyme. Biochemistry 45: 14896–14907PubMedGoogle Scholar
  164. Verméglio A (1977) Secondary electron transfer in reaction centers of Rhodopseudomonas sphaeroides: out-of-phase periodicity of two for the formation of ubisemiquinone and fully reduced ubiquinone. Biochim Biophys Acta 459: 516–524PubMedGoogle Scholar
  165. Visscher PT, Taylor BF and Kiene RP (1995) Microbial consumption of dimethyl sulfide and methanediol in coastal marine-sediments. FEMS Microbiol Ecol 18: 145–153Google Scholar
  166. Visscher PT and Taylor BF (1993) Organic thiols as organolithotrophic substrates for growth of phototrophic bacteria. Appl Environ Microbiol 59: 93–96PubMedGoogle Scholar
  167. Wang K, Zhen Y, Sadoski R, Grinnell S, Geren L, Ferguson-Miller S, Durham B and Millett F (1999) Definition of the interaction domain for cytochrome c on cytochrome c oxidase. I. Rapid kinetic analysis of electron transfer from cytochrome c to Rhodobacter sphaeroides cytochrome oxidase surface mutants. J Biol Chem 274: 38042–38050PubMedGoogle Scholar
  168. Watts CA, Ridley H, Condie KL, Leaver JT, Richardson DJ and Butler CS (2003) Selenate reduction by Enterobacter cloacae SDL 1a-1 is catalysed by a molybdenum-dependent membrane-bound enzyme that is distinct from the membrane-bound nitrate reductase. FEMS Microbiol Lett 228: 273–279PubMedGoogle Scholar
  169. Watts CA, Ridley H, Dridge EJ, Leaver JT, Reilly AJ, Richardson DJ and Butler CS (2005) Microbial reduction of selenate and nitrate: common themes and variations. Biochem Soc Trans 33: 173–175PubMedGoogle Scholar
  170. Wikström M (2004) Cytochrome c oxidase: 25 years of the elusive proton pump. Biochim Biophys Acta 1655: 241–247PubMedGoogle Scholar
  171. Wood PM (1981) The redox potential of dimethylsulfoxide reduction to dimethylsulfide-evaluation and biochemical implications. FEBS Lett 124: 11–14PubMedGoogle Scholar
  172. Wraight CA, Cogdell RJ and Chance B (1978) Ion transport and electrochemical gradients in photosynthetic bacteria. In: Clayton RK and Sistrom RW (eds) The Photosynthetic Bacteria, pp 471–502. Plenum Press, New YorkGoogle Scholar
  173. Xiong J and Bauer CE (2002) Complex evolution of photosynthesis. Annu Rev Plant Biol 53: 503–521PubMedGoogle Scholar
  174. Xu X and Yagi T (2001) Identification of the NADH binding subunit of energy transducing NADH-quinone oxidoreductase (NDH-1) of Thermus thermophilus HB-8. Biochem Biophys Res Commun 174: 667–672Google Scholar
  175. Xu X, Matsuno-Yagi A and Yagi T (1991a) Characterization of the 25-kilodalton subunit of the energy transducing NADH-ubiquinone oxidoreductase of Paracoccus denitrificans: Sequence similarity to the 24-kilodalton subunit of the flavoprotein fraction of mammalian complex I. Biochemistry 30: 8678–8684PubMedGoogle Scholar
  176. Xu X, Matsuno-Yagi A and Yagi T (1991b) The NADH-binding subunit of the energy transducing NADH-ubiquinone oxidoreductase of Paracoccus denitrificans: Gene cloning and deduced primary structure. Biochemistry 30: 6422–6428PubMedGoogle Scholar
  177. Xu X, Matsuno-Yagi A and Yagi T (1992a) Gene cluster of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans: Characterization of four structural gene products. Biochemistry 31: 6925–6932PubMedGoogle Scholar
  178. Xu X, Matsuno-Yagi A and Yagi T (1992b) Structural features of the 66 kilodalton subunit of the energy transducing NADH-ubiquinone oxidoreductase (NDH-1) of Paracoccus denitrificans. Arch Biochem Biophys 296: 40–48PubMedGoogle Scholar
  179. Xu X, Matsuno-Yagi A and Yagi T (1993) DNA sequencing of the seven remaining structural genes of the gene cluster encoding the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans. Arch Biochem Biophys 250: 302–311Google Scholar
  180. Yagi T (1993) The bacterial energy-transducing NADH-quinone oxidoreductases. Biochim Biophys Acta 1141: 1–17PubMedGoogle Scholar
  181. Yagi T and Matsuno-Yagi A (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: The secret unlocked. Biochemistry 42: 2266–2274PubMedGoogle Scholar
  182. Yagi T, Seo BB, Di Bernardo S, Nakamaru-Ogiso E, Kao MC and Matsuno-Yagi A (2001) NADH dehydrogenases: From basic science to biomedicine. J Bioenerg Biomembr 33: 233–242PubMedGoogle Scholar
  183. Yoshikawa S, Shinzawa-Itoh K,Nakashima R, Yaono R,Yamashita E, Inoue N, Yao M, Fei MJ, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T and Tsukihara T (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280: 1723–1729PubMedGoogle Scholar
  184. Yun CH, Beci R, Crofts AR, Kaplan S and Gennis RB (1990) Cloning and DNA sequencing of the fbc operon encoding the cytochrome bc 1 complex from Rhodobacter sphaeroides. Characterization of fbc deletion mutants and complementation by a site-specific mutational variant. Eur J Biochem 194: 399–411PubMedGoogle Scholar
  185. Zannoni D (1995) Aerobic and anaerobic electron transport chains in anoxygenic phototrophic bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria (Advances in Photosynthesis and Respiration, Vol 2), pp 449–971. Kluwer Academic Publishers, DordrechtGoogle Scholar
  186. Zannoni D and Ingledew JW (1985) A thermodynamic analysis of the plasma membrane electron transport components in phototrophically grown cells of Chloroflexus aurantiacus: An optical and electron paramagnetic resonance study. FEBS Letters 193: 93–98Google Scholar
  187. Zannoni D and Moore AL (1990) Measurement of the redox state of the ubiquinone pool in Rhodobacter capsulatus membrane fragments. FEBS Letters 271: 123–127PubMedGoogle Scholar
  188. Zannoni D, Jasper P and Marrs BL (1978) Light induced oxygen uptake as a probe of electron transport between respiratory and photosynthetic components in membranes of Rhodopseudomonas capsulata Arch Biochem Biophys 191: 625–631PubMedGoogle Scholar
  189. Zannoni D, Peterson S and Marrs BL (1986) Recovery of the alternative oxidase dependent electron flow by fusion of membrane vesicles from Rhodobacter capsulatus mutant strains. Arch Microbiol 144: 375–380Google Scholar
  190. Zeller T, Moskvin OV, Li K, Klug G and Gomelsky M (2005) Transcriptome and physiological responses to hydrogen peroxide of the facultatively photo trophic bacterium Rhodobacter sphaeroides. J Bacteriol 187: 7232–7242PubMedGoogle Scholar
  191. Zhang J, Barquera B and Gennis RB (2004) Gene fusions with beta-lactamase show that subunit I of the cytochrome bd quinol oxidase from E. coli has nine transmembrane helices with the O2 reactive site near the periplasmic surface. FEBS Lett 561: 58–62PubMedGoogle Scholar
  192. Zufferey R, Preisig O, Hennecke H and Thöny-Meyer L (1996) Assembly and function of the cytochrome cbb 3 oxidase subunits in Bradyrhizobium japonicum. J Biol Chem 271: 9114–9119PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2009

Authors and Affiliations

  • Davide Zannoni
    • 1
  • Barbara Schoepp-Cothenet
    • 2
  • Jonathan Hosler
    • 3
  1. 1.Department of BiologyUniversity of BolognaBolognaItaly
  2. 2.Laboratoire de Bioénergétique et Ingénierie des ProtéinesInstitut de Biologie Structurale et Microbiologie (IFR)Marseille Cedex 20France
  3. 3.Department of BiochemistryUniversity of Mississippi Medical CenterJacksonUSA

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