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Respiration and Oxidative Phosphorylation in Mycobacteria

  • Michael BerneyEmail author
  • Gregory M. CookEmail author
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 39)

Summary

The genus Mycobacterium comprises a group of obligately aerobic bacteria that have adapted to inhabit a wide range of intracellular and extracellular environments. A fundamental feature in this adaptation is the ability of mycobacteria to respire and generate energy for growth or to sustain latency. Mycobacteria harbor multiple primary dehydrogenases to fuel the electron transport chain and two terminal respiratory oxidases, an aa 3 -type cytochrome c oxidase and cytochrome bd-type menaquinol oxidase, are present for dioxygen reduction coupled to the generation of a protonmotive force. In mycobacteria, Type II NADH dehydrogenases are favoured over complex I for NADH oxidation and menaquinone acts as the primary conduit between electron-donating and electron-accepting reactions. The molecular mechanisms regulating the expression of the electron transport chain components in mycobacteria remains unknown. Despite being obligate aerobes, mycobacteria have the ability to metabolize in the absence of oxygen and a number of reductases are present to facilitate the turnover of reducing equivalents under these conditions (e.g., nitrate reductase, fumarate reductase). Hydrogenases and ferredoxins are also present in the genomes of mycobacteria suggesting the ability of these bacteria to adapt to an anaerobic-type of metabolism in the absence of oxygen. The exact roles of reductases and hydrogenases is poorly understood. ATP synthesis by the membrane-bound F1FO-ATP synthase (see Chap.  6) is essential for growing and non-growing mycobacteria and the enzyme is able to function over a wide range of proton-motive force values (aerobic to hypoxic). Research into mycobacterial respiration and oxidative phosphorylation have been energized by the discovery of a new drug (TMC207) that targets the ATP synthase of mycobacteria, suggesting that inhibitors of respiration and ATP synthesis will provide the next generation of front line drugs to combat tuberculosis and nontuberculous mycobacterial disease.

Keywords

NADH Dehydrogenase Mycobacterial Species Fumarate Reductase Alternative Electron Acceptor Substrate Level Phosphorylation 
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.

Abbreviations:

CCCP

– Carbonyl cyanide m-chlorophenylhydrazone;

CO-DH

– Carbon-monoxide dehydrogenase;

DCCD

N,N’-dicyclohexylcarbodiimide;

FAD

– Flavin adenine dinucleotide;

G3P

– Glycerol 3-phosphate;

HYD

– Hydrogenase;

MDH

– Malate dehydrogenase;

MK

– Menaquinone (vitamine K);

MKH2

– Menaquinol;

MQO

– Malate quinone oxidoreductase;

NAD+

– Nicotinamide adenine dinucleotide;

NDH

– NADH dehydrogenase;

NRP

– Non-replicating persistence;

P5CDH

– Pyrroline-5-carboxylate dehydrogenase;

PMF

– Proton-motive force;

PRODH

– Proline dehydrogenase;

SDH

– Succinate dehydrogenase;

TCA

– Tricarboxylic acid;

TMC207

– Tibotec Medicinal Compound 207;

Z∆pH

– Transmembrane pH gradient expressed in mV;

ΔΨ

– Electrical or membrane potential expressed in mV

Notes

Acknowledgments

Research in the authors laboratory is funded by Health Research Council, Lottery Health, Marsden Fund, Royal Society New Zealand and the Maurice Wilkins Centre.

References

  1. Andries K, Verhasselt P, Guillemont J, Göhlmann HW, Neefs JM, Winkler H, Van Gestel J, Timmerman P, Zhu M, Lee E, Williams P, de Chaffoy D, Huitric E, Hoffner S, Cambau E, Truffot-Pernot C, Lounis N, Jarlier V (2005) A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307:223–227PubMedCrossRefGoogle Scholar
  2. Bacon J, James BW, Wernisch L, Williams A, Morley KA, Hatch GJ, Mangan JA, Hinds J, Stoker NG, Butcher PD, Marsh PD (2004) The influence of reduced oxygen availability on pathogenicity and gene expression in Mycobacterium tuberculosis. Tuberculosis (Edinb) 84:205–217CrossRefGoogle Scholar
  3. Baughn AD, Garforth SJ, Vilcheze C, Jacobs WR (2009) An anaerobic-type alpha-ketoglutarate ferredoxin oxidoreductase completes the oxidative tricarboxylic acid cycle of Mycobacterium tuberculosis. PloS Pathog 5:e1000662PubMedCentralPubMedCrossRefGoogle Scholar
  4. Berney M, Cook GM (2010) Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS ONE 5:e8614PubMedCentralPubMedCrossRefGoogle Scholar
  5. Berney M, Weimar MR, Heikal A, Cook GM (2012) Regulation of proline metabolism in mycobacteria and its role in carbon metabolism under hypoxia. Mol Microbiol 84:664–681PubMedCrossRefGoogle Scholar
  6. Beste DJ, Peters J, Hooper T, Avignone-Rossa C, Bushell ME, McFadden J (2005) Compiling a molecular inventory for Mycobacterium bovis BCG at two growth rates: evidence for growth rate-mediated regulation of ribosome biosynthesis and lipid metabolism. J Bacteriol 187:1677–1684PubMedCentralPubMedCrossRefGoogle Scholar
  7. Beste DJ, Laing E, Bonde B, Avignone-Rossa C, Bushell ME, McFadden JJ (2007) Transcriptomic analysis identifies growth rate modulation as a component of the adaptation of mycobacteria to survival inside the macrophage. J Bacteriol 189:3969–3976PubMedCentralPubMedCrossRefGoogle Scholar
  8. Betts JC (2002) Transcriptomics and proteomics: tools for the identification of novel drug targets and vaccine candidates for tuberculosis. IUBMB Life 53:239–242PubMedCrossRefGoogle Scholar
  9. Betts JC, Lukey PT, Robb LC, McAdam RA, Duncan K (2002) Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol 43:717–731PubMedCrossRefGoogle Scholar
  10. Boos W (1998) Binding protein-dependent ABC transport system for glycerol 3-phosphate of Escherichia coli. Methods Enzymol 292:40–51PubMedCrossRefGoogle Scholar
  11. Borisov VB, Murali R et al (2011) Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode. Proc Natl Acad Sci U S A 108(42):17320–17324PubMedCentralPubMedCrossRefGoogle Scholar
  12. Boshoff HI, Barry CE 3rd (2005) Tuberculosis: metabolism and respiration in the absence of growth. Nat Rev Microbiol 3:70–80PubMedCrossRefGoogle Scholar
  13. Cecchini G, Schroder I, Gunsalus RP, Maklashina E (2002) Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim Biophys Acta 1553:140–157PubMedCrossRefGoogle Scholar
  14. Cole ST, Brosch R et al (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685):537–544PubMedCrossRefGoogle Scholar
  15. Cole ST, Supply P, Honore N (2001) Repetitive sequences in Mycobacterium leprae and their impact on genome plasticity. Lepr Rev 72:449–461PubMedGoogle Scholar
  16. Constant P, Poissant L, Villemur R (2008) Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2. ISME J 2:1066–1076PubMedCrossRefGoogle Scholar
  17. Constant P, Chowdhury SP, Pratscher J, Conrad R (2010) Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ Microbiol 12:821–829PubMedCrossRefGoogle Scholar
  18. Constant P, Chowdhury SP, Hesse L, Pratscher J, Conrad R (2011) Genome data mining and soil survey for the novel group 5 [NiFe]-hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H(2)-oxidizing bacteria. Appl Environ Microbiol 77:6027–6035PubMedCentralPubMedCrossRefGoogle Scholar
  19. Cotter PA, Melville SB, Albrecht JA, Gunsalus RP (1997) Aerobic regulation of cytochrome d oxidase (cydAB) operon expression in Escherichia coli: roles of Fnr and ArcA in repression and activation. Mol Microbiol 25:605–615PubMedCrossRefGoogle Scholar
  20. Cox RA, Cook GM (2007) Growth regulation in the mycobacterial cell. Curr Mol Med 7:231–245PubMedCrossRefGoogle Scholar
  21. D’Mello R, Hill S, Poole RK (1995) The oxygen affinity of cytochrome bo’ in Escherichia coli determined by the deoxygenation of oxyleghemoglobin and oxymyoglobin: Km values for oxygen are in the submicromolar range. J Bacteriol 177:867–870PubMedCentralPubMedGoogle Scholar
  22. D’Mello R, Hill S, 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 142:755–763PubMedCrossRefGoogle Scholar
  23. de Jonge MR, Koymans LH, Guillemont JE, Koul A, Andries K (2007) A computational model of the inhibition of Mycobacterium tuberculosis ATPase by a new drug candidate R207910. Proteins 67:971–980PubMedCrossRefGoogle Scholar
  24. Dhar N, McKinney JD (2010) Mycobacterium tuberculosis persistence mutants identified by screening in isoniazid-treated mice. Proc Natl Acad Sci U S A 107:12275–12280PubMedCentralPubMedCrossRefGoogle Scholar
  25. Dhiman RK, Mahapatra S, Slayden RA, Boyne ME, Lenaerts A, Hinshaw JC, Angala SK, Chatterjee D, Biswas K, Narayanasamy P, Kurosu M, Crick DC (2009) Menaquinone synthesis is critical for maintaining mycobacterial viability during exponential growth and recovery from non-replicating persistence. Mol Microbiol 72:85–97PubMedCrossRefGoogle Scholar
  26. Dimroth P, Cook GM (2004) Bacterial Na+- or H+ -coupled ATP synthases operating at low electrochemical potential. Adv Microb Physiol 49:175–218PubMedCrossRefGoogle Scholar
  27. Fontan P, Aris V, Ghanny S, Soteropoulos P, Smith I (2008) Global transcriptional profile of Mycobacterium tuberculosis during THP-1 human macrophage infection. Infect Immun 76:717–725PubMedCentralPubMedCrossRefGoogle Scholar
  28. Frampton R, Aggio RB, Villas-Boas SG, Arcus VL, Cook GM (2012) Toxin-antitoxin systems of Mycobacterium smegmatis are essential for cell survival. J Biol Chem 287:5340–5356PubMedCentralPubMedCrossRefGoogle Scholar
  29. Friedl P, Hoppe J, Gunsalus RP, Michelsen O, von Meyenburg K, Schairer HU (1983) Membrane integration and function of the three F0 subunits of the ATP synthase of Escherichia coli K12. EMBO J 2:99–103PubMedCentralPubMedGoogle Scholar
  30. Goldman BS, Gabbert KK, Kranz RG (1996a) Use of heme reporters for studies of cytochrome biosynthesis and heme transport. J Bacteriol 178:6338–6347PubMedCentralPubMedGoogle Scholar
  31. Goldman BS, Gabbert KK, Kranz RG (1996b) The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents. J Bacteriol 178:6348–6351PubMedCentralPubMedGoogle Scholar
  32. Griffin JE, Gawronski JD, Dejesus MA, Ioerger TR, Akerley BJ, Sassetti CM (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7:e1002251PubMedCentralPubMedCrossRefGoogle Scholar
  33. Haagsma AC, Driessen NN, Hahn MM, Lill H, Bald D (2010) ATP synthase in slow- and fast-growing mycobacteria is active in ATP synthesis and blocked in ATP hydrolysis direction. FEMS Microbiol Lett 313:68–74PubMedCrossRefGoogle Scholar
  34. Haagsma AC, Podasca I, Koul A, Andrie K, Guillemont J, Lill H, Bald D (2011) Probing the interaction of the diarylquinoline TMC207 with its target mycobacterial ATP synthase. PLoS ONE 6:e23575PubMedCentralPubMedCrossRefGoogle Scholar
  35. Higashi T, Kalra VK, Lee SH, Bogin E, Brodie AF (1975) Energy-transducing membrane-bound coupling factor-ATPase from Mycobacterium phlei. I. Purification, homogeneity, and properties. J Biol Chem 250:6541–6548PubMedGoogle Scholar
  36. Huitric E, Verhasselt P, Andries K, Hoffner SE (2007) In vitro antimycobacterial spectrum of a diarylquinoline ATP synthase inhibitor. Antimicrob Agents Chemother 51:4202–4204PubMedCentralPubMedCrossRefGoogle Scholar
  37. Huitric E, Verhasselt P, Koul A, Andries K, Hoffner S, Andersson DI (2010) Rates and mechanisms of resistance development in Mycobacterium tuberculosis to a novel diarylquinoline ATP synthase inhibitor. Antimicrob Agents Chemother 54:1022–1028PubMedCentralPubMedCrossRefGoogle Scholar
  38. Kana BD, Weinstein EA, Avarbock D, Dawes SS, Rubin H, Mizrahi V (2001) Characterization of the cydAB-encoded cytochrome bd oxidase from Mycobacterium smegmatis. J Bacteriol 183:7076–7086PubMedCentralPubMedCrossRefGoogle Scholar
  39. Kana BD, Machowski EE, Schechter N, Teh J-S, Rubin H, Mizrahi V (2009) Electron transport and respiration in mycobacteria. In: Parish, T, Brown A (eds) Mycobacterium: genomics and molecular biology, Horizon Scientific Press, Poole, UK. pp 35–64Google Scholar
  40. Kim YM, Hegeman GD (1983) Oxidation of carbon monoxide by bacteria. Int Rev Cytol 81:1–32PubMedCrossRefGoogle Scholar
  41. King GM (2003) Uptake of carbon monoxide and hydrogen at environmentally relevant concentrations by mycobacteria. Appl Environ Microbiol 69:7266–7272PubMedCentralPubMedCrossRefGoogle Scholar
  42. Koch-Koerfges A, Kabus A, Ochrombel I, Marin K, Bott M (2012) Physiology and global gene expression of a Corynebacterium glutamicum DeltaF(1)F(O)-ATP synthase mutant devoid of oxidative phosphorylation. Biochim Biophys Acta 1817:370–380PubMedCrossRefGoogle Scholar
  43. Koul A, Dendouga N, Vergauwen K, Molenberghs B, Vranckx L, Willebrords R, Ristic Z, Lill H, Dorange I, Guillemont J, Bald D, Andries K (2007) Diarylquinolines target subunit c of mycobacterial ATP synthase. Nat Chem Biol 3:323–324PubMedCrossRefGoogle Scholar
  44. Koul A, Vranckx L, Dendouga N et al (2008) Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J Biol Chem 283:25273–25280PubMedCrossRefGoogle Scholar
  45. Kuhn M, Steinbuchel A, Schlegel HG (1984) Hydrogen evolution by strictly aerobic hydrogen bacteria under anaerobic conditions. J Bacteriol 159:633–639PubMedCentralPubMedGoogle Scholar
  46. Lounis N, Gevers T, Van den Berg J, Vranckx L, Andries K (2009) ATP synthase inhibition of Mycobacterium avium is not bactericidal. Antimicrob Agents Chemother 53:4927–4929PubMedCentralPubMedCrossRefGoogle Scholar
  47. Matsoso LG, Kana BD, Crellin PK, Lea-Smith DJ, Pelosi A, Powell D, Dawes SS, Rubin H, Coppel RL, Mizrahi V (2005) Function of the cytochrome bc1-aa3 branch of the respiratory network in mycobacteria and network adaptation occurring in response to its disruption. J Bacteriol 187:6300–6308PubMedCentralPubMedCrossRefGoogle Scholar
  48. McAdam RA, Quan S, Smith DA, Bardarov S, Betts JC, Cook FC, Hooker EU, Lewis AP, Woollard P, Everett MJ, Lukey PT, Bancroft GJ, Jacobs WR Jr, K D Jr (2002) Characterization of a Mycobacterium tuberculosis H37Rv transposon library reveals insertions in 351 ORFs and mutants with altered virulence. Microbiology 148:2975–2986PubMedGoogle Scholar
  49. Megehee JA, Hosler JP, Lundrigan MD (2006) Evidence for a cytochrome bcc-aa3 interaction in the respiratory chain of Mycobacterium smegmatis. Microbiology 152:823–829PubMedCrossRefGoogle Scholar
  50. Menzel R, Roth J (1981) Purification of the putA gene product. A bifunctional membrane-bound protein from Salmonella typhimurium responsible for the two-step oxidation of proline to glutamate. J Biol Chem 256:9755–9761PubMedGoogle Scholar
  51. Miesel L, Weisbrod TR, Marcinkeviciene JA, Bittman R, Jacobs WR Jr (1998) NADH dehydrogenase defects confer isoniazid resistance and conditional lethality in Mycobacterium smegmatis. J Bacteriol 180:2459–2467PubMedCentralPubMedGoogle Scholar
  52. Mnatsakanyan N, Bagramyan K, Trchounian A (2004) Hydrogenase 3 but not hydrogenase 4 is major in hydrogen gas production by Escherichia coli formate hydrogenlyase at acidic pH and in the presence of external formate. Cell Biochem Biophys 41:357–366PubMedCrossRefGoogle Scholar
  53. Molenaar D, van der Rest ME, Petrovic S (1998) Biochemical and genetic characterization of the membrane-associated malate dehydrogenase (acceptor) from Corynebacterium glutamicum. Eur J Biochem 254:395–403PubMedCrossRefGoogle Scholar
  54. Niebisch A, Bott M (2003) Purification of a cytochrome bc-aa3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum. Identification of a fourth subunity of cytochrome aa3 oxidase and mutational analysis of diheme cytochrome c1. J Biol Chem 278:4339–4346PubMedCrossRefGoogle Scholar
  55. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR (2003a) Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48:833–843PubMedCentralPubMedCrossRefGoogle Scholar
  56. Park SW, Hwang EH, Park H, Kim JA, Heo J, Lee KH, Song T, Kim E, Ro YT, Kim SW, Kim YM (2003b) Growth of mycobacteria on carbon monoxide and methanol. J Bacteriol 185:142–147PubMedCentralPubMedCrossRefGoogle Scholar
  57. Pfeiffer T, Schuster S, Bonhoeffer S (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292:504–507PubMedCrossRefGoogle Scholar
  58. Pittman MS, Robinson HC, Poole RK (2005) A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm. J Biol Chem 280:32254–32261PubMedCrossRefGoogle Scholar
  59. Poole RK, Cook GM (2000) Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv Microb Physiol 43:165–224PubMedCrossRefGoogle Scholar
  60. Prasada Reddy TL, Suryanarayana Murthy P, Venkitasubramanian TA (1975) Variations in the pathways of malate oxidation and phosphorylation in different species of Mycobacteria. Biochim Biophys Acta 376:210–218PubMedCrossRefGoogle Scholar
  61. Rao M, Streur TL, Aldwell FE, Cook GM (2001) Intracellular pH regulation by Mycobacterium smegmatis and Mycobacterium bovis BCG. Microbiology 147:1017–1024PubMedGoogle Scholar
  62. Rao SP, Alonso S, Rand L, Dick T, Pethe K (2008) The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 105:11945–11950PubMedCentralPubMedCrossRefGoogle Scholar
  63. Santana M, Ionescu MS, Vertes A, Longin R, Kunst F, Danchin A, Glaser P (1994) Bacillus subtilis F0F1 ATPase: DNA sequence of the atp operon and characterization of atp mutants. J Bacteriol 176:6802–6811PubMedCentralPubMedGoogle Scholar
  64. Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48:77–84PubMedCrossRefGoogle Scholar
  65. Schnappinger D, Ehrt S, Voskuil MI et al (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198:693–704PubMedCentralPubMedCrossRefGoogle Scholar
  66. Schryvers A, Lohmeier E, Weiner JH (1978) Chemical and functional properties of the native and reconstituted forms of the membrane-bound, aerobic glycerol-3-phosphate dehydrogenase of Escherichia coli. J Biol Chem 253:783–788PubMedGoogle Scholar
  67. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha -crystallin. Proc Natl Acad Sci U S A 98:7534–7539PubMedCentralPubMedCrossRefGoogle Scholar
  68. Shi L, Sohaskey CD, Kana BD, Dawes S, North RJ, Mizrahi V, Gennaro ML (2005) Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc Natl Acad Sci U S A 102:15629–15634PubMedCentralPubMedCrossRefGoogle Scholar
  69. Sohaskey CD (2005) Regulation of nitrate reductase activity in Mycobacterium tuberculosis by oxygen and nitric oxide. Microbiology 151(Pt 11):3803–3810PubMedCrossRefGoogle Scholar
  70. Sohaskey CD (2008) Nitrate enhances the survival of Mycobacterium tuberculosis during inhibition of respiration. J Bacteriol 190:2981–2986PubMedCentralPubMedCrossRefGoogle Scholar
  71. Sohaskey CD, Wayne LG (2003) Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 185:7247–7256PubMedCentralPubMedCrossRefGoogle Scholar
  72. Tamagnini P, Leitao E et al (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31(6):692–720PubMedCrossRefGoogle Scholar
  73. Tanner JJ (2008) Structural biology of proline catabolism. Amino Acids 35:719–730PubMedCentralPubMedCrossRefGoogle Scholar
  74. Tian J, Bryk R, Itoh M, Suematsu M, Nathan C (2005) Variant tricarboxylic acid cycle in Mycobacterium tuberculosis: identification of alpha-ketoglutarate decarboxylase. Proc Natl Acad Sci U S A 102:10670–10675PubMedCentralPubMedCrossRefGoogle Scholar
  75. Tran SL, Cook GM (2005) The F1Fo-ATP synthase of Mycobacterium smegmatis is essential for growth. J Bacteriol 187:5023–5028PubMedCentralPubMedCrossRefGoogle Scholar
  76. Tran SL, Rao M, Simmers C, Gebhard S, Olsson K, Cook GM (2005) Mutants of Mycobacterium smegmatis unable to grow at acidic pH in the presence of the protonophore carbonyl cyanide m-chlorophenylhydrazone. Microbiology 151:665–672PubMedCrossRefGoogle Scholar
  77. Tseng CP, Hansen AK, Cotter P, Gunsalus RP (1994) Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli. J Bacteriol 176:6599–6605PubMedCentralPubMedGoogle Scholar
  78. Unden G, Bongaerts J (1997) Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320:217–234PubMedCrossRefGoogle Scholar
  79. Velmurugan K, Chen B, Miller JL et al (2007) Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3:e110PubMedCentralPubMedCrossRefGoogle Scholar
  80. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501PubMedCrossRefGoogle Scholar
  81. Vilcheze C, Weisbrod TR, Chen B, Kremer L, Hazbon MH, Wang F, Alland D, Sacchettini JC, Jacobs WR Jr (2005) Altered NADH/NAD + ratio mediates coresistance to isoniazid and ethionamide in mycobacteria. Antimicrob Agents Chemother 49:708–720PubMedCentralPubMedCrossRefGoogle Scholar
  82. von Ballmoos C, Cook GM, Dimroth P (2008) Unique rotary ATP synthase and its biological diversity. Annu Rev Biophys 37:43–64CrossRefGoogle Scholar
  83. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, Sherman DR, Schoolnik GK (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198:705–713PubMedCentralPubMedCrossRefGoogle Scholar
  84. Voskuil MI, Visconti KC, Schoolnik GK (2004) Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84:218–227CrossRefGoogle Scholar
  85. Watanabe S, Zimmermann M, Goodwin MB, Sauer U, Barry CE 3rd, Boshoff HI (2011) Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS Pathog 7:e1002287PubMedCentralPubMedCrossRefGoogle Scholar
  86. Wayne LG, Hayes LG (1996) An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64:2062–2069PubMedCentralPubMedGoogle Scholar
  87. Weinstein EA, Yano T, Li LS et al (2005) Inhibitors of type II NADH: menaquinone oxidoreductase represent a class of antitubercular drugs. Proc Natl Acad Sci U S A 102:4548–4553PubMedCentralPubMedCrossRefGoogle Scholar
  88. Youmans AS, Millman I, Youmans GP (1956) The oxidation of compounds related to the tricarboxylic acid cycle by whole cells and enzyme preparations of Mycobacterium tuberculosis var. Hominis. J Bacteriol 71:565–570PubMedCentralPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Microbiology and ImmunologyAlbert Einstein College of MedicineBronxUSA
  2. 2.Department of Microbiology and ImmunologyUniversity of OtagoDunedinNew Zealand

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