The evolution of respiratory O2/NO reductases: An out-of-the-phylogenetic-box perspective

Journal of the Royal Society Interface

Volumn 11, Issue 98, 2014, Pages

  Ducluzeau, Anne Lise ^c   Schoepp Cothenet, Barbara ^a   Van Lis, Robert ^a   Baymann, Frauke ^a   Russell, Michael J ^b   Nitschke, Wolfgang ^a  

^a CNRS and Aix Marseille University   (France)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Haem copper oxidase; NO reductase; Origin and evolution of respiration; Palaeogeochemistry

Indexed keywords

ENZYME ACTIVITY; NITRIC OXIDE;

EVOLUTIONARY INNOVATION; GREAT OXIDATION EVENT; HAEM-COPPER OXIDASE; NITRIC OXIDE REDUCTASE; NO-REDUCTASE; ORIGIN AND EVOLUTION OF RESPIRATION; PALAEOGEOCHEMISTRY; THERMODYNAMIC INFORMATION;

BIOLOGY;

CYTOCHROME; CYTOCHROME B; NITRATE REDUCTASE; NITRIC OXIDE; NITRIC OXIDE REDUCTASE; NITRITE REDUCTASE; NITROUS OXIDE REDUCTASE; OXIDOREDUCTASE; OXYGEN; POLYPEPTIDE; POTASSIUM CHANNEL; PROTON; BACTERIAL PROTEIN; NITRIC-OXIDE REDUCTASE;

ANAEROBIC METABOLISM; BINDING SITE; BIOENERGY; BIOGEOCHEMISTRY; CATALYSIS; CONVERGENT EVOLUTION; DENITRIFICATION; ELECTRON; ELECTRON TRANSPORT; ENERGY CONVERSION; ENZYME ACTIVE SITE; GLOBAL CLIMATE; GREENHOUSE; MITOCHONDRION; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXYGEN TENSION; PHOTOSYNTHESIS; PHYLOGENETIC TREE; PROTEIN DOMAIN; PROTON TRANSPORT; REVIEW; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS; ARCHAEON; ATMOSPHERE; BACTERIA; CHEMICAL STRUCTURE; CHEMISTRY; CLUSTER ANALYSIS; ENVIRONMENT; EVOLUTION; OXIDATION REDUCTION REACTION; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

ARCHAEA; ATMOSPHERE; BACTERIA; BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; CLUSTER ANALYSIS; ENVIRONMENT; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84904975677     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.0196     Document Type: Review

References (118)

1. Han H, Hemp J, Pace LA, Ouyang H, Ganesan K, Roh JH, Daldal F, Blanke SR, Gennis RB. 2011 Adaptation of aerobic respiration to low O2 environments. Proc. Natl Acad. Sci. USA 108, 14 109-14 114. (doi:10.1073/pnas.1018958108)
2. Rauhamäki V, Wikström M. 2014 The causes of reduced proton-pumping efficiency in type B and C respiratory heme-copper oxidases, and in some mutated variants of type A. Biochim. Biophys. Acta Bioenerg. 1837, 999-1003. (doi:10.1016/j.bbabio.2014.02.020)
3. Castresana J, Lübben M, Saraste M, Higgins DG. 1994 Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J. 13, 2516-2525.
4. Castresana J, Saraste M. 1995 Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biochem. Sci. 20, 443-448. (doi:10.1016/S0968-0004(00)89098-2)
5. Castresana J, Lübben M, Saraste M. 1995 New archaebacterial genes coding for redox proteins: implications for the evolution of aerobic metabolism. J. Mol. Biol. 250, 202-210. (doi:10.1006/jmbi.1995.0371)
6. Saraste M et al. 1996 Evolution of cytochrome oxidase. In Origin and evolution of biological energy conservation (ed. H Baltscheffsky), pp. 255-289. New York, NY: VCH Publ.
7. Hendriks J, Gohlke U, Saraste M. 1998 From NO to OO: nitric oxide and dioxygen in bacterial respiration. J. Bioenerg. Biomembr. 30, 15-24. (doi:10.1023/A:1020547225398)
8. Pereira MM, Santana M, Teixeira M. 2001 A novel scenario for the evolution of haem-copper oxygen reductases. Biochim. Biophys. Acta Bioenergetics 1505, 185-208. (doi:10.1016/S0005-2728(01)00169-4)
9. Hemp J, Gennis RB. 2008 Diversity of the heme-copper superfamily in archaea: insights from genomics and structural modeling. Results Probl. Cell Differ. 45, 1-31. (doi:10.1007/400-2007-046)
10. Ducluzeau A-L, Ouchane S, Nitschke W. 2008 cbb3 oxidases are an ancient innovation of the domain bacteria. Mol. Biol. Evol. 25, 1158-1166. (doi:10.1093/molbev/msn062)
11. Ducluzeau A-L, van Lis R, Duval S, Schoepp-Cothenet B, Russell MJ, Nitschke W. 2009 Was nitric oxide the first strongly oxidizing terminal electron sink? Trends Biochem. Sci. 34, 9-15. (doi:10.1016/j.tibs.2008.10.005)
12. Brochier-Armanet C, Talla E, Gribaldo S. 2009 The multiple evolutionary histories of dioxygen reductases: implications for the origin and evolution of aerobic respiration. Mol. Biol. Evol. 26, 285-297. (doi:10.1093/molbev/msn246)
13. Gribaldo S, Talla E, Brochier-Armanet C. 2009 Evolution of the haem copper oxidases superfamily: a rooting tale. Trends Biochem. Sci. 34, 375-381. (doi:10.1016/j.tibs.2009.04.002)
14. Sousa FL, Alves RJ, Pereira-Leal JB, Teixeira M, Pereira MM. 2011 A bioinformatic classifier and database for heme-copper oxygen reductases. PLoS ONE 6, e19117. (doi:10.1371/journal.pone.0019117)
15. Sousa FL, Alves RJ, Ribeiro MA, Pereira-Leal JB, Teixeira M, Pereira MM. 2012 The superfamily of heme-copper oxygen reductases: types and evolutionary considerations. Biochim. Biophys. Acta Bioenergetics 1817, 629-637. (doi:10.1016/j.bbabio.2011.09.020)
16. Pereira MM, Teixeira M. 2004 Proton pathways, ligand binding and dynamics of the catalytic site in haem-copper oxygen reductases: a comparison between the three families. Biochim. Biophys. Acta Bioenergetics 1655, 340-346. (doi:10.1016/j.bbabio.2003.06.003)
17. Nitschke W, Kramer DM, Riedel A, Liebl U. 1995 From naphtho- to benzoquinones - (r)evolutionary reorganisations of electron transfer chains. In Photosynthesis: from light to biosphere, vol. I (ed. P Mathis), pp. 945-950. Dordrecht, The Netherlands: Kluwer Academic Publishers.
18. Schoepp-Cothenet B, Lieutaud C, Baymann F, Vermeglio A, Friedrich T, Kramer DM, Nitschke W. 2009 Menaquinone as pool quinone in a purple bacterium. Proc. Natl Acad. Sci. USA 106, 8549-8554. (doi:10.1073/pnas.0813173106)
19. Hiraishi A, Shin YK, Sugiyama J. 1995 Brachymonas denitrificans gen. sp. nov., an aerobic chemoorganotropphic bacterium which contains rhodoquninones, and evolutionary relationships of rhodoquinone producers to bacterial species with various quinone classes. J. Gen. Appl. Microbiol. 41, 99-117. (doi:10.2323/jgam.41.99)
20. Wikström MK, Berden JA. 1972 Oxidoreduction of cytochrome b in the presence of antimycin. Biochim. Biophys. Acta 283, 403-420. (doi:10.1016/0005- 2728(72)90258-7)
21. Mitchell P. 1975 Protonmotive redox mechanism of the cytochrome bc1 complex in the respiratory chain: protonmotive ubiquinone cycle. FEBS Lett. 56, 1-6. (doi:10.1016/0014-5793(75)80098-6)
22. Crofts AR, Hong S, Wilson C, Burton R, Victoria D, Harrison C, Schulten K. 2013 The mechanism of ubihydroquinone oxidation at the Qo site of the cytochrome bc1 complex. Biochim. Biophys. Acta Bioenergetics 1827, 1362-1377. (doi:10.1016/j.bbabio.2013.01.009)
23. Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G, Brugna M, Giudici-Orticoni MT. 2008 A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J. Biol. Chem. 283, 25 803-25 811. (doi:10.1074/jbc.M802496200)
24. Bird LJ, Bonnefoy V, Newman DK. 2011 Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol. 19, 330-340. (doi:10.1016/j.tim.2011.05. 001)
25. vanden Hoven RN, 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, 148-155. (doi:10.1016/j.bbabio. 2004.03.001)
26. Abramson J, Riistama S, Larsson G, Jasaitis A, Svensson-Ek M, Laakonen L, Puustinen A, Iwata S, Wikström M. 2000 The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat. Struct. Biol. 7, 910-917. (doi:10.1038/82824)
27. Alefounder PR, Greenfield AJ, McCarthy JEG, Ferguson SJ. 1983 Selection and organization of denitrifying electron-transfer pathways in Paracoccus denitrificans. Biochim. Biophys. Acta 724, 20-39. (doi:10.1016/0005-2728(83) 90022-1)
28. Ferguson SJ. 1994 Denitrification and its control. Antonie van Leeuwenhoek 66, 89-110. (doi:10.1007/BF00871634)
29. Kukimoto M, Nishiyama M, Murphy ME, Turley S, Adman ET, Horinouchi S, Beppu T. 1994 X-ray structure and site-directed mutagenesis of a nitrite reductase from Alcaligenes faecalis S-6: roles of two copper atoms in nitrite reduction. Biochemistry 33, 5246-5252. (doi:10.1021/bi00183a030)
30. Baker SC, Saunders NF, Willis AC, Ferguson SJ, Hajdu J, Fülöp V. 1997 Cytochrome cd1 structure: unusual haem environments in a nitrite reductase and analysis of factors contributing to beta-propeller folds. J. Mol. Biol. 269, 440-455. (doi:10.1006/jmbi.1997.1070)
31. Yoshimatsu K, Iwasaki T, Fujiwara T. 2002 Sequence and paramagnetic resonance analysis of nitrate reductase Nar GH from a denitrifying halophilic euryarchaeote Haloarcula marismortui. FEBS Lett. 516, 145-150. (doi:10.1016/S0014-5793(02)02524-3)
32. Lledó B, Martínez-Espinosa RM, Marhuenda-Egea FC, Bonete MJ. 2004 Respiratory nitrate reductase from haloarchaeon Haloferax mediterranei: biochemical and genetic analysis. Biochim. Biophys. Acta 1674, 50-59. (doi:10.1016/j.bbagen.2004.05.007)
33. Martinez-Espinosa RM, Dridge EJ, Bonete MJ, Butt JN, Butler CS, Sargent F, Richardson DJ. 2007 Look on the positive side! The orientation, identification and bioenergetics of 'Archaeal' membrane-bound nitrate reductases. FEMS Microbiol. Lett. 276, 129-139. (doi:10.1111/j.1574-6968.2007. 00887.x)
34. de Vries S, Momcilovic M, Strampraad MJ, Whitelegge JP, Baghai A, Schröder I. 2010 Adaptation to a high-tungsten environment: Pyrobaculum aerophilum contains an active tungsten nitrate reductase. Biochemistry 49, 9911-9921. (doi:10.1021/bi100974v)
35. Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInerney JO, Deppenmeier U, Martin WF. 2012 Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc. Natl Acad. Sci. USA 109, 20 537-20 542. (doi:10.1073/pnas.1209119109)
36. Baymann F, Schoepp-Cothenet B, Lebrun E, van Lis R, Nitschke W. 2012 Phylogeny of Rieske/cytb complexes with a special focus on the haloarchaeal enzymes. Genome Biol. Evol. 4, 720-729. (doi:10.1093/gbe/evs056)
37. Ettwig KF, Speth DR, Reimann J, Wu ML, Jetten MSM, Keltjens JT. 2012 Bacterial oxygen production in the dark. Front. Microbiol. 3, 273. (doi:10.3389/fmicb.2012.00273)
38. Wikström M, Verkhovsky MI. 2007 Mechanism and energetic of proton translocation by the respiratory heme-copper oxidases. Biochim. Biophys. Acta Bioenergetics 1767, 1200-1214. (doi:10.1016/j.bbabio.2007.06.008)
39. Wang M, Jiang Y-Y, Kim KM, Qu G, Ji H-F, Mittenthal JE, Zhang H-Y, Caetano-Anollés G. 2011 A universal molecular clock of protein folds and its power in tracing the early history of aerobic metabolism and planet oxygenation. Mol. Biol. Evol. 28, 567-582. (doi:10.1093/molbev/msq232)
40. Kim KM, Qin T, Jiang Y-Y, Chen L-L, Xiong M, Caetano-Anollés D, Zhang H-Y, Caetano-Anollés G. 2012 Protein domain structure uncovers the origin of aerobic metabolism and the rise of planetary oxygen. Structure 20, 67-76. (doi:10.1016/j.str.2011.11.003)
41. Guex N, Peitsch MC. 1997 SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723. (doi:10.1002/elps.1150181505)
42. Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S, Saraste M. 2000 Nitric oxide reductases in bacteria. Biochim. Biophys. Acta 1459, 266-273. (doi:10.1016/S0005-2728(00)00161-4)
43. Lobo SA, Almeida CC, Carita JN, Teixeira M, Saraiva LM. 2008 The haem-copper oxygen reductase of Desulfovibrio vulgaris contains a dihaem cytochrome c in subunit II. Biochim. Biophys. Acta Bioenergetics 1777, 1528-1534. (doi:10.1016/j.bbabio.2008.09.007)
44. van der Oost J et al. 1992 Restoration of a lost metal-binding site: construction of two different copper sites into a subunit of the E. coli cytochrome o quinol oxidase complex. EMBO J. 11, 3209-3217.
45. Soulimane T, Buse G, Bourenkov GP, Bartunik HD, Huber R, Than ME. 2000 Structure and mechanism of the aberrant ba3-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19, 1766-1776. (doi:10.1093/emboj/19.8.1766)
46. Buschmann S, Warkentin E, Xie H, Langer JD, Ermler U, Michel H. 2010 The structure of cbb3 cytochrome oxidase provides insights into proton pumping. Science 329, 327-330. (doi:10.1126/science.1187303)
47. Hino T, Matsumoto Y, Nagano S, Sugimoto H, Fukumori Y, Murata T, Iwata S, Shiro Y. 2010 Structural basis of biological N2O generation by bacterial nitric oxide reductase. Science 330, 1666-1670. (doi:10.1126/science.1195591)
48. Tosha T, Shiro Y. 2013 Crystal structures of nitric oxide reductases provide key insights into functional conversion of respiratory enzymes. IUBMB Life 65, 217-226. (doi:10.10002/iub.1135)
49. Matsumoto Y, Tosha T, Pisliakov AV, Hino T, Sugimoto H, Nagano S, Sugita Y, Shiro Y. 2012 Crystal structure of quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus. Nat. Struc. Mol. Biol. 19, 238-248. (doi:10.1038/nsmb.2213)
50. Salomonsson L, Reimann J, Tosha T, Krause N, Gonska N, Shiro Y, Ädelroth P. 2012 Proton transfer in the quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus during reduction of oxygen. Biochim. Biophys. Acta Bioenergetics 1817, 1914-1920. (doi:10.1016/j.bbabio. 2012.04.007)
51. Shiro Y. 2012 Structure and function of bacterial nitric oxide reductases: nitric oxide reductase, anaerobic enzymes. Biochim. Biophys. Acta Bioenergetics 1817, 1907-1913. (doi:10.1016/j.bbabio.2012.03.001)
52. Schurig-Briccio LA, Venkatakrishnan P, Hemp J, Bricio C, Berenguer J, Gennis RB. 2013 Characterisation of the nitric oxide reductase from Thermus thermophilus. Proc. Natl Acad. Sci. USA 110, 12 613-12 618. (doi:10.1073/pnas. 1301731110)
53. Hemp J, Robinson DE, Ganesan KB, Martinez TJ, Kelleher NL, Gennis RB. 2006 Evolutionary migration of a post-translationally modified active-site residue in the proton-pumping heme-copper oxygen reductases. Biochemistry 45, 15 405-15 410. (doi:10.1021/bi062026u)
54. Rauhamäki V, Baumann M, Soliymani R, Puustinen A, Wikström M. 2006 Identification of a histidine-tyrosine cross-link in the active site of the cbb3-type cytochrome c oxidase from Rhodobacter sphaeroides. Proc. Natl Acad. Sci. USA 103, 16 135-16 140. (doi:10.1073/pnas.0606254103)
55. Suharti, Strampraad MJ, Schröder I, de Vries S. 2001 A novel copper A containing menaquinol NO reductase from Bacillus azotoformans. Biochemistry 40, 2632-2639. (doi:10.1021/bi0020067)
56. Lu S, Suharti, de Vries S, Moënne-Loccoz P. 2004 Two CO molecules can bind concomitantly at the diiron site of NO reductase from Bacillus azotoformans. J. Am. Chem. Soc. 126, 15 332-15 333. (doi:10.1021/ja045233v)
57. Suharti, Heering HA, de Vries S. 2004 NO reductase from Bacillus azotoformans is a bifunctional enzyme accepting electrons from menaquinol and a specific endogenous membrane-bound cytochrome c551. Biochemistry 43, 13 487-13 495. (doi:10.1021/bi0488101)
58. Giuffrè A, Stubauer G, Sarti P, Brunori M, Zumft WG, Buse G, Soulimane T. 1999 The heme-copper oxidases of Thermus thermophilus catalyze the reduction of nitric oxide: evolutionary implications. Proc. Natl Acad. Sci. USA 96, 14 718-14 723. (doi:10.1073/pnas.96.26.14718)
59. Forte E, Urbani A, Saraste M, Sarti P, Brunori M, Giuffre A. 2001 The cytochrome cbb3 from Pseudomonas stutzeri displays nitric oxide reductase activity. Eur. J. Biochem. 268, 6486-6491. (doi:10.1046/j.0014-2956.2001.02597. x)
60. Butler CS, Forte E, Scandurra FM, Arese M, Giuffrè A, Greenwood C, Sarti P. 2002 Cytochrome bo3from Escherichia coli: the binding and turnover of nitric oxide. Biochem. Biophys. Res. Commun. 296, 1272-1278. (doi:10.1016/S0006-291X(02)02074-0)
61. Huang Y, Reimann J, Lepp H, Drici N, Ädelroth P. 2008 Vectorial proton transfer coupled to reduction of O2 and NO by a heme-copper oxidase. Proc. Natl Acad. Sci. USA 105, 20 257-20 262. (doi:10.1073/pnas.0805429106)
62. Kluwe WM, Hook JB, Bernstein J. 1982 Synergistic toxicity of carbon tetrachloride and several aromatic organohalide compounds. Toxicology 23, 321-336. (doi:10.1016/0300-483X(82)90070-1)
63. Prat L, Maillard J, Grimaud R, Holliger C. 2011 Physiological adaptation of Desulfitobacterium hafniense strain TCE1 to tetrachloroethene respiration. Appl. Environ. Microbiol. 77, 3853-3859. (doi:10.1128/AEM.02471-10)
64. Wagner A, Cooper M, Ferdi S, Seifert J, Adrian L. 2012 Growth of Dehalococcoides mccartyi strain CBDB1 by reductive dehalogenation of brominated benzenes to benzene. Environ. Sci. Technol. 46, 8960-8968. (doi:10.1021/ es3003519)
65. Leys D, Adrian L, Smidt H. 2013 Organohalide respiration: microbes breathing chlorinated molecules. Phil. Trans. R. Soc. B 368, 20120316. (doi:10.1098/rstb.2012.0316)
66. Schoepp-Cothenet B et al. 2013 On the universal core of bioenergetics. Biochim. Biophys. Acta Bioenergetics 1827, 79-93. (doi:10.1016/j.bbabio.2012.09. 005)
67. Nitschke W, Russell MJ. 2013 Beating the acetyl-CoA pathway to the origin of life. Phil. Trans. R. Soc. B 368, 20120258. (doi:10.1098/rstb.2012.0258)
68. Walker CB et al. 2010 Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl Acad. Sci. USA 107, 8818-8823. (doi:10.1073/pnas. 0913533107)
69. Farquhar J, Wing BA. 2003 Multiple sulfur isotopes and the evolution of the atmosphere. Earth Planet. Sci. Lett. 213, 1-13. (doi:10.1016/S0012-821X(03) 00296-6)
70. Holland HD. 2011 Discovering the history of atmospheric oxygen. In Frontiers in geochemistry: contribution of geochemistry to the study of the earth (eds RS Harmon, A Parker), pp. 43-60. Oxford, UK: Blackwell Publishing Ltd.
71. Anbar AD, Duan Y, Lyons TW, Arnold GL, Kendall B, Creaser RA, Kauffman AJ, Buick R. 2007 A whiff of oxygen before the great oxidation event? Science 317, 1903-1906. (doi:10.1126/science.1140325)
72. Partin CA, Lalonde SV, Planavsky NJ, Bekker A, Rouxel OJ, Lyons TW, Konhauser KO. 2013 Uranium in iron formations and the rise of atmospheric oxygen. Chem. Geol. 362, 82-90. (doi:10.1016/j.chemgeo.2013.09.005)
73. Crowe SA, Dossing LN, Beukes NJ, Bau M, Kruger SJ, Frei R, Canfield DE. 2013 Atmospheric oxygenation three billion years ago. Nature 501, 535-538. (doi:10.1038/nature12426)
74. Stolper DA, Revsbech NP, Canfield DE. 2010 Aerobic growth at nanomolar oxygen concentrations. Proc. Natl Acad. Sci. USA 107, 18 755-18 760. (doi:10.1073/pnas.1013435107)
75. Haqq-Misra J, Kasting JF, Lee S. 2011 Availability of O2 and H2O2 on pre-photosynthetic earth. Astrobiology 11, 293-302. (doi:10.1089/ast.2010.0572)
76. Pavlov AA, Kasting JF. 2002 Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2, 27-41. (doi:10.1089/153110702753621321)
77. Draganić ZD, Negron-Mendoza A, Sehested K, Vujošević SI, Navarro-Gonzales R, Albarran-Sanchez MG, Draganić IG. 1991 Radiolysis of aqueous solutions of ammonium bicarbonate over a large dose range. Int. J. Radiat. Appl. Instrum. C Radiat. Phys. Chem. 38, 317-321. (doi:10.1016/1359-0197(91)90100-G)
78. Draganić IG. 2005 Radiolysis of water: a look at its origin and occurrence in the nature. Radiat. Phys. Chem. 72, 181-186. (doi:10.1016/j. radphyschem.2004.09.012)
79. Farquhar J, Savarino J, Airieau S, Thiemens MH. 2001 Observation of wavelength-sensitive mass-independent sulfur isotope effects during SO2 photolysis: implications for the early atmosphere. J. Geophys. Res. 106, 32 829-32 839. (doi:10.1029/2000JE001437)
80. Canuto VM, Levine JS, Augustsson TR, Imhoff CL. 1982 UV radiation from the young Sun and oxygen and ozone levels in the prebiological palaeoatmosphere. Nature 296, 816-820. (doi:10.1038/296816a0)
81. Li W, Czaja AD, Van Kranendonk MJ, Beard BL, Roden EE, Johnson CM. 2013 An anoxic, Fe (II)-rich, U-poor ocean 3.46 billion years ago. Geochim. Cosmochim. Acta 120, 65-79. (doi:10.1016/j.gca.2013.06.033)
82. Johnson MJ. 1967 Aerobic microbial growth at low oxygen concentrations. J. Bacteriol. 94, 101-108.
83. Realini L, De Ridder K, Palomino J, Hirschel B, Portaels F. 1998 Microaerophilic conditions promote growth of Mycobacterium genavense. J. Clin. Microbiol. 36, 2565-2570. (Pubitemid 28380956)
84. Sabra W, Kim EJ, Zeng AP. 2002 Physiological responses of Pseudomonas aeruginosa PAO1 to oxidative stress in controlled microaerobic and aerobic cultures. Microbiology 148, 3195-3202. (Pubitemid 35243719)
85. Unden G, Becker S, Bongaerts J, Holighaus G, Schirawski J, Six S. 1995 O2-sensing and O2-dependent gene regulation in facultatively anaerobic bacteria. Arch. Microbiol. 164, 81-90.
86. Unden G, Becker S, Bongaerts J, Schirawski J, Six S. 1994 Oxygen regulated gene expression in facultatively anaerobic bacteria. Antonie van Leeuwenhoek 66, 3-23. (doi:10.1007/BF00871629)
87. Becker S, Holighaus G, Gabrielczyk T, Unden G. 1996 O2 as the regulatory signal for FNR-dependent gene regulation in Escherichia coli. J. Bacteriol. 178, 4515-4521. (Pubitemid 26262237)
88. Ozima M, Seki K, Terada N, Miura YN, Podosek FA, Shinagawa H. 2005 Terrestrial nitrogen and noble gases in lunar soils. Nature 436, 655-659. (doi:10.1038/nature03929)
89. Martin RS, Mather TA, Pyle DM. 2007 Volcanic emissions and the early Earth atmosphere. Geochim. Cosmochim. Acta 71, 3673-3685. (doi:10.1016/j.gca. 2007.04.035)
90. Walker JC. 1985 Carbon dioxide on the early Earth. Orig. Life Evol. Biosph. 16, 117-127. (doi:10.1007/BF01809466)
91. Mancinelli RL, McKay CP. 1988 The evolution of nitrogen cycling. Orig. Life Evol. Biosph. 18, 311-325. (doi:10.1007/BF01808213)
92. Yung YL, McElroy MB. 1979 Fixation of nitrogen in the prebiotic atmosphere. Science 203, 1002-1004. (doi:10.1126/science.203.4384.1002)
93. Chameides WL, Walker JC. 1981 Rates of fixation by lightning of carbon and nitrogen in possible primitive atmospheres. Origins Life 11, 291-302. (doi:10.1007/BF00931483)
94. Gurevich AV, Zybin KP, Roussel-Dupre RA. 1999 Lightning initiation by simultaneous effect of runaway breakdown and cosmic ray showers. Phys. Lett. A 254, 79-87. (doi:10.1016/S0375-9601(99) 00091-2)
95. Gurevich AV, Karashtin AN. 2013 Runaway Breakdown and Hydrometeors in Lightning Initiation. Phys. Rev. Lett. 110, 185005. (doi:10.1103/PhysRevLett. 110.185005)
96. Krasnopolsky VA. 2006 A sensitive search for nitric oxides in the lower atmospheres of Venus and Mars: detection on Venus and upper limit for Mars. Icarus 182, 80-91. (doi:10.1016/j.icarus.2005.12.003)
97. Grimaldi S, Schoepp-Cothenet B, Cécaldi P, Guigliarelli B, Magalon A. 2013 The prokaryotic Mo/W-bisPGD enzymes family: a catalytic workhorse in bioenergetics. Biochim. Biophys. Acta Bioenergetics 1827, 1048-1085. (doi:10.1016/j.bbabio.2013.01.011)
98. Schoepp-Cothenet B, van Lis R, Philippot P, Magalon A, Russell MJ, Nitschke W. 2012 The ineluctable requirement for the trans-iron elements molybdenum and/or tungsten in the origin of life. Sci. Rep. 2, 263. (doi:10.1038/srep00263)
99. van Lis R, Ducluzeau A-L, Nitschke W, Schoepp-Cothenet B. 2011 The nitrogen cycle in the Archaean; an intricate interplay of enzymatic and abiotic reactions. In Nitrogen cycling in bacteria: molecular analysis (ed. JWB Moir), pp. 1-21. Norwich, UK: Caister Academic Press.
100. Wang WC, Yung YL, Lacis AA, Mo T, Hansen JE. 1976 Greenhouse effects due to man-made perturbations of trace gases. Science 194, 685-690. (doi:10.1126/science.194.4266.685)
101. Zumft WG, Kroneck PMH. 2007 Respiratory transformation of nitrous oxide (N2O) to dinitrogen by bacteria and archaea. Adv. Microbiol. Physiol. 52, 107-227. (doi:10.1016/S0065-2911(06)52003-X)
102. Wuebbles DJ. 2009 Nitrous oxide: no laughing matter. Science 326, 56-57. (doi:10.1126/science.1179571)
103. Ettwig KF et al. 2010 Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464, 543-548. (doi:10.1038/nature08883)
104. Wu ML, de Vries S, van Alen TA, Butler MK, Op den Camp HJM, Keltjens JT, Jetten MSM, Strous M. 2011 Physiological role of the respiratory quinol oxidase in the anaerobic nitrite-reducing methanotroph 'Candidatus Methylomirabilis oxyfera'. Microbiology 157, 890-898. (doi:10.1099/mic.0.045187-0)
105. Luesken FA, Wu ML, Op den Camp HJM, Keltjens JT, Stunnenberg H, Francoijs K-J, Strous M, Jetten MSM. 2012 Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis. Environ. Microbiol. 14, 1024-1034. (doi:10.1111/j.1462-2920.2011.02682.x)
106. Ferguson SJ, Ingledew WJ. 2008 Energetic problems faced by micro-organisms growing or surviving on parsimonious energy sources and at acidic pH: Acidithiobacillus ferrooxidans as a paradigm. Biochim. Biophys. Acta Bioenergetics 1777, 1471-1479. (doi:10.1016/j.bbabio.2008.02.012)
107. Bratsch SG. 1989 Standard electrode potentials and temperature coefficients in water at 298.15 K. J. Phys. Chem. Ref. Data 18, 1-21. (doi:10.1063/1.555839)
108. Steensma E, Heering HA, Hagen WR, van Mierlo CPM. 1996 Redox properties of wild-type, Cys69Ala, and Cys69Ser Azotobacter vinelandii flavodoxin II as measured by cyclic voltammetry and EPR spectroscopy. Eur. J. Biochem. 235, 167-172. (doi:10.1111/j.1432-1033.1996.00167.x)
109. Goretski J, Zafiriou OC, Hollocher TC. 1990 Steady-state nitric oxide concentrations during dentrification. J. Biol. Chem. 265, 11 535-11 538.
110. Kastrau DH, Heiss B, Kroneck PM, Zumft WG. 1994 Nitric oxide reductase from Pseudomonas stutzeri, a novel cytochrome bc complex. Phospholipid requirement, electron paramagnetic resonance and redox properties. Eur. J. Biochem. 222, 293-303. (doi:10.1111/j.1432-1033.1994.tb18868.x)
111. Margulis L, Lovelock JE. 1974 Biological modulation of the Earth's atmosphere. Icarus 21, 471-489. (doi:10.1016/0019-1035(74)90150-X)
112. Lovelock JE. 1988 The ages of Gaia. London, UK: WW Norton and Co.
113. Lane N, Martin WF. 2012 The origin of membrane bioenergetics. Cell 151, 1406-1416. (doi:10.1016/j.cell.2012.11.050)
114. Sousa FL, Thiergart T, Landan G, Nelson-Sathi S, Pereira IA, Allen JF, Lane N, Martin WF. 2013 Early bioenergetic evolution. Phil. Trans. R. Soc. B 368, 20130088. (doi:10.1098/rstb.2013.0088)
115. Ducluzeau A-L, Schoepp-Cothenet B, Baymann F, Russell MJ, Nitschke W. 2014 Free energy conversion in the LUCA: quo vadis? Biochim. Biophys. Acta Bioenergetics 1837, 982-988. (doi:10.1016/j.bbabio.2013.12.005)
116. Hodgson GW, Ponnamperuma C. 1968 Prebiotic porphyrin genesis: porphyrins from electric discharge in methane, ammonia and water vapor. Proc. Natl Acad. Sci. USA 59, 22-28. (doi:10.1073/pnas.59.1.22)
117. Simionescu CI, Simionescu BC, Mora R, Leancâ M. 1978 Porphyrin-like compounds genesis under simulated abiotic conditions. Origins Life 9, 103-114. (doi:10.1007/BF00931408)
118. Navarro-González R, McKay CP, Mvondo DN. 2001 A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning. Nature 412, 61-64. (doi:10.1038/35083537)