1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Energetics of Respiration and Oxidative Phosphorylation in Mycobacteria

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
    176.38 Kb
  • HTML
    182.12 Kb
  • PDF
    548.37 Kb
  • Authors: Gregory M. Cook1, Kiel Hards2, Catherine Vilchèze3, Travis Hartman4, Michael Berney5
  • Editors: Graham F. Hatfull6, William R. Jacobs Jr.7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: University of Otago, Department of Microbiology and Immunology, Dunedin, New Zealand; 2: University of Otago, Department of Microbiology and Immunology, Dunedin, New Zealand; 3: Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY 10461; 4: Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY 10461; 5: Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY 10461; 6: University of Pittsburgh, Pittsburgh, PA; 7: Howard Hughes Medical Institute, Albert Einstein College of Medicine, Bronx, NY
    • Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.MGM2-0015-2013
  • Received 26 April 2013 Accepted 06 August 2013 Published 06 June 2014
  • G.M. Cook, [email protected]
image of Energetics of Respiration and Oxidative Phosphorylation in Mycobacteria
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Energetics of Respiration and Oxidative Phosphorylation in Mycobacteria, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/2/3/MGM2-0015-2013-1.gif /docserver/preview/fulltext/microbiolspec/2/3/MGM2-0015-2013-2.gif

  • Abstract:

    Mycobacteria inhabit a wide range of intracellular and extracellular environments. Many of these environments are highly dynamic, and therefore mycobacteria are faced with the constant challenge of redirecting their metabolic activity to be commensurate with either replicative growth or a nonreplicative quiescence. A fundamental feature in this adaptation is the ability of mycobacteria to respire, regenerate reducing equivalents, and generate ATP via oxidative phosphorylation. Mycobacteria harbor multiple primary dehydrogenases to fuel the electron transport chain, and two terminal respiratory oxidases, an -type cytochrome oxidase and a cytochrome -type menaquinol oxidase, are present for dioxygen reduction coupled to the generation of a proton motive force (PMF). Hypoxia leads to the downregulation of key respiratory complexes, but the molecular mechanisms regulating this expression are 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, succinate dehydrogenase/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. ATP synthesis by the membrane-bound FF-ATP synthase is essential for growing and nongrowing mycobacteria, and the enzyme is able to function over a wide range of PMF values (aerobic to hypoxic). The discovery of lead compounds that target respiration and oxidative phosphorylation in highlights the importance of this area for the generation of new frontline drugs to combat tuberculosis.

  • Citation: Cook G, Hards K, Vilchèze C, Hartman T, Berney M. 2014. Energetics of Respiration and Oxidative Phosphorylation in Mycobacteria. Microbiol Spectrum 2(3):MGM2-0015-2013. doi:10.1128/microbiolspec.MGM2-0015-2013.

References

1. Segal W, Bloch H. 1956. Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J Bacteriol 72:132–141. [PubMed]
2. Brodie AF, Gutnik DL. 1972. Electron transport and oxidative phosphorylation in microbial systems, p 599–681. In King TE, Klingenberg M (ed), Electron and Coupled Energy Transfer Systems, vol. 1B. Marcel Dekker, New York.
3. Russell JB, Cook GM. 1995. Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59:48–62. [PubMed]
4. Rao M, Streur TL, Aldwell FE, Cook GM. 2001. Intracellular pH regulation by Mycobacterium smegmatis and Mycobacterium bovis BCG. Microbiology 147:1017–1024. [PubMed]
5. Ishaque M. 1992. Energy generation mechanisms in the in vitro-grown Mycobacterium lepraemurium. Int J Lepr Other Mycobact Dis 60:61–70. [PubMed]
6. 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 USA 105:11945–11950. [PubMed][CrossRef]
7. 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 84:664–681. [PubMed][CrossRef]
8. Dimroth P, Cook GM. 2004. Bacterial Na+ - or H+ -coupled ATP synthases operating at low electrochemical potential. Adv Microb Physiol 49:175–218. [PubMed][CrossRef]
9. 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 313:68–74. [PubMed][CrossRef]
10. 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 250:6541–6548. [PubMed]
11. Kerscher S, Drose S, Zickermann V, Brandt U. 2008. The three families of respiratory NADH dehydrogenases. Results Probl Cell Differ 45:185–222. [PubMed][CrossRef]
12. Weinstein EA, Yano T, Li LS, Avarbock D, Avarbock A, Helm D, McColm AA, Duncan K, Lonsdale JT, Rubin H. 2005. Inhibitors of type II NADH:menaquinone oxidoreductase represent a class of antitubercular drugs. Proc Natl Acad Sci USA 102:4548–4553. [PubMed][CrossRef]
13. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honore N, Garnier T, Churcher C, Harris D, Mungall K, Basham D, Brown D, Chillingworth T, Connor R, Davies RM, Devlin K, Duthoy S, Feltwell T, Fraser A, Hamlin N, Holroyd S, Hornsby T, Jagels K, Lacroix C, Maclean J, Moule S, Murphy L, Oliver K, Quail MA, Rajandream MA, Rutherford KM, Rutter S, Seeger K, Simon S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Taylor K, Whitehead S, Woodward JR, Barrell BG. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007–1011. [PubMed][CrossRef]
14. 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 180:2459–2467. [PubMed]
15. 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 49:708–720. [PubMed][CrossRef]
16. Berney M, Cook GM. 2010. Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 5:e8614. [PubMed][CrossRef]
17. Velmurugan K, Chen B, Miller JL, Azogue S, Gurses S, Hsu T, Glickman M, Jacobs WR Jr, Porcelli SA, Briken V. 2007. Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3:e110. [PubMed][CrossRef]
18. 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 USA 102:15629–15634. [PubMed][CrossRef]
19. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, Schoolnik GK. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198:693–704. [PubMed][CrossRef]
20. 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 43:717–731. [PubMed][CrossRef]
21. Unden G, Bongaerts J. 1997. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320:217–234. [CrossRef]
22. Iwata M, Lee Y, Yamashita T, Yagi T, Iwata S, Cameron AD, Maher MJ. 2012. The structure of the yeast NADH dehydrogenase (Ndi1) reveals overlapping binding sites for water- and lipid-soluble substrates. Proc Natl Acad Sci USA 109:15247–15252. [PubMed][CrossRef]
23. Feng Y, Li WF, Li J, Wang JW, Ge JP, Xu D, Liu YJ, Wu KQ, Zeng QY, Wu JW, Tian CL, Zhou B, Yang MJ. 2012. Structural insight into the type-II mitochondrial NADH dehydrogenases. Nature 491:478–482. [PubMed][CrossRef]
24. Melo AMP, Bandeiras TM, Teixeira M. 2004. New insights into type II NAD(P)H : quinone oxidoreductases. Microbiol Mol Biol Rev 68:603–616. [PubMed][CrossRef]
25. Lin SS, Gross U, Bohne W. 2011. Two internal type II NADH dehydrogenases of Toxoplasma gondii are both required for optimal tachyzoite growth. Mol Microbiol 82:209–221. [PubMed][CrossRef]
26. 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:e1002251. [PubMed][CrossRef]
27. Yano T, Li LS, Weinstein E, Teh JS, Rubin H. 2006. Steady-state kinetics and inhibitory action of antitubercular phenothiazines on Mycobacterium tuberculosis type-II NADH-menaquinone oxidoreductase (NDH-2). J Biol Chem 281:11456–11463. [PubMed][CrossRef]
28. 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, Duncan K. 2002. Characterization of a Mycobacterium tuberculosis H37Rv transposon library reveals insertions in 351 ORFs and mutants with altered virulence. Microbiology 148:2975–2986. [PubMed]
29. Sassetti CM, Boyd DH, Rubin EJ. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48:77–84. [PubMed][CrossRef]
30. Warman AJ, Rito TS, Fisher NE, Moss DM, Berry NG, O’Neill PM, Ward SA, Biagini GA. 2013. Antitubercular pharmacodynamics of phenothiazines. J Antimicrob Chemother 68:869–880. [PubMed][CrossRef]
31. Teh JS, Yano T, Rubin H. 2007. Type II NADH: menaquinone oxidoreductase of Mycobacterium tuberculosis. Infectious Disorders Drug Targets 7:169–181. [PubMed][CrossRef]
32. Biagini GA, Viriyavejakul P, O’Neill PM, Bray PG, Ward SA. 2006. Functional characterization and target validation of alternative complex I of Plasmodium falciparum mitochondria. Antimicrob Agents Chemother 50:1841–1851. [PubMed][CrossRef]
33. Shirude PS, Paul P, Choudhury NR, Kedari C, Bandodkar B, Ugarkar BG. 2012. Quinolinyl pyrimidines: potent inhibitors of NDH-2 as a novel class of anti-TB agents. ACS Med Chem Lett 3:736–740. [CrossRef]
34. Ordway D, Viveiros M, Leandro C, Bettencourt R, Almeida J, Martins M, Kristiansen JE, Molnar J, Amaral L. 2003. Clinical concentrations of thioridazine kill intracellular multidrug-resistant Mycobacterium tuberculosis. Antimicrob Agents Chemother 47:917–922. [PubMed][CrossRef]
35. Amaral L, Kristiansen JE, Abebe LS, Millett W. 1996. Inhibition of the respiration of multi-drug resistant clinical isolates of Mycobacterium tuberculosis by thioridazine: potential use for initial therapy of freshly diagnosed tuberculosis. J Antimicrob Chemother 38:1049–1053. [PubMed][CrossRef]
36. Mogi T, Matsushita K, Murase Y, Kawahara K, Miyoshi H, Ui H, Shiomi K, Omura S, Kita K. 2009. Identification of new inhibitors for alternative NADH dehydrogenase (NDH-II). FEMS Microbiol Lett 291:157–161. [PubMed][CrossRef]
37. 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 USA 102:10670–10675. [PubMed][CrossRef]
38. 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 71:565–570. [PubMed]
39. Cecchini G, Schroder I, Gunsalus RP, Maklashina E. 2002. Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochimica Biophysica Acta 1553:140–157. [CrossRef]
40. Baek SH, Li AH, Sassetti CM. 2011. Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biol 9:e1001065. [PubMed][CrossRef]
41. Unden G, Schirawski J. 1997. The oxygen-responsive transcriptional regulator FNR of Escherichia coli: the search for signals and reactions. Mol Microbiol 25:205–210. [CrossRef]
42. 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:e1002287. [PubMed][CrossRef]
43. Eoh H, Rhee KY. 2013. Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 110:6554–6559. [PubMed][CrossRef]
44. 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) 84:205–217. [PubMed][CrossRef]
45. 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 189:3969–3976. [PubMed][CrossRef]
46. Tanner JJ. 2008. Structural biology of proline catabolism. Amino Acids 35:719–730. [PubMed][CrossRef]
47. 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 256:9755–9761. [PubMed]
48. Weigoldt M, Meens J, Bange FC, Pich A, Gerlach GF, Goethe R. 2013. Metabolic adaptation of Mycobacterium avium subsp. paratuberculosis to the gut environment. Microbiology 159:380–391. [PubMed][CrossRef]
49. Smith DA, Parish T, Stoker NG, Bancroft GJ. 2001. Characterization of auxotrophic mutants of Mycobacterium tuberculosis and their potential as vaccine candidates. Infect Immun 69:1142–1150. [PubMed][CrossRef]
50. Vignais PM, Colbeau A. 2004. Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188. [PubMed]
51. Tamagnini P, Leitao E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P. 2007. Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31:692–720. [PubMed][CrossRef]
52. 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 77:6027–6035. [PubMed][CrossRef]
53. 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 12:821–829. [PubMed][CrossRef]
54. King GM. 2003. Uptake of carbon monoxide and hydrogen at environmentally relevant concentrations by mycobacteria. Appl Environ Microbiol 69:7266–7272. [PubMed][CrossRef]
55. Kim YM, Hegeman GD. 1983. Oxidation of carbon monoxide by bacteria. Int Rev Cytol 81:1–32. [PubMed][CrossRef]
56. Park SW, Hwang EH, Park H, Kim JA, Heo J, Lee KH, Song T, Kim E, Ro YT, Kim SW, Kim YM. 2003. Growth of mycobacteria on carbon monoxide and methanol. J Bacteriol 185:142–147. [PubMed][CrossRef]
57. 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 253:783–788. [PubMed]
58. Boos W. 1998. Binding protein-dependent ABC transport system for glycerol 3-phosphate of Escherichia coli. Methods Enzymol 292:40–51. [PubMed][CrossRef]
59. Molenaar D, van der Rest ME, Drysch A, Yucel R. 2000. Functions of the membrane-associated and cytoplasmic malate dehydrogenases in the citric acid cycle of Corynebacterium glutamicum. J Bacteriol 182:6884–6891. [PubMed][CrossRef]
60. 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 254:395–403. [PubMed][CrossRef]
61. Prasada Reddy TL, Suryanarayana Murthy P, Venkitasubramanian TA. 1975. Respiratory chains of Mycobacterium smegmatis. Indian J Biochem Biophys 12:255–259. [PubMed]
62. 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 376:210–218. [PubMed][CrossRef]
63. 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 177:867–870. [PubMed]
64. 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 142:755–763. [PubMed][CrossRef]
65. 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 25:605–615. [PubMed][CrossRef]
66. 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 176:6599–6605. [PubMed]
67. 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 183:7076–7086. [PubMed][CrossRef]
68. Voskuil MI, Visconti KC, Schoolnik GK. 2004. Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb) 84:218–227. [PubMed][CrossRef]
69. Boshoff HI, Barry CE 3rd. 2005. Tuberculosis: metabolism and respiration in the absence of growth. Nat Rev Microbiol 3:70–80. [PubMed][CrossRef]
70. 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 bc 1-aa 3 branch of the respiratory network in mycobacteria and network adaptation occurring in response to its disruption. J Bacteriol 187:6300–6308. [PubMed][CrossRef]
71. Megehee JA, Hosler JP, Lundrigan MD. 2006. Evidence for a cytochrome bcc-aa 3 interaction in the respiratory chain of Mycobacterium smegmatis. Microbiology 152:823–829. [PubMed][CrossRef]
72. Niebisch A, Bott M. 2001. Molecular analysis of the cytochrome bc 1-aa 3 branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c 1. Arch Microbiol 175:282–294. [CrossRef]
73. Abrahams KA, Cox JA, Spivey VL, Loman NJ, Pallen MJ, Constantinidou C, Fernandez R, Alemparte C, Remuinan MJ, Barros D, Ballell L, Besra GS. 2012. Identification of novel imidazo[1,2-a]pyridine inhibitors targeting M. tuberculosis QcrB. PLoS One 7:e52951. [PubMed][CrossRef]
74. Niebisch A, Bott M. 2003. Purification of a cytochrome bc-aa 3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum. Identification of a fourth subunity of cytochrome aa 3 oxidase and mutational analysis of diheme cytochrome c 1. J Biol Chem 278:4339–4346. [PubMed][CrossRef]
75. Berry EA, Trumpower BL. 1985. Isolation of ubiquinol oxidase from Paracoccus denitrificans and resolution into cytochrome bc1 and cytochrome c-aa 3 complexes. J Biol Chem 260:2458–2467. [PubMed]
76. Sone N, Sekimachi M, Kutoh E. 1987. Identification and properties of a quinol oxidase super-complex composed of a bc 1 complex and cytochrome oxidase in the thermophilic bacterium PS3. J Biol Chem 262:15386–15391. [PubMed]
77. Poole RK, Cook GM. 2000. Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv Microb Physiol 43:165–224. [PubMed][CrossRef]
78. Borisov VB, Murali R, Verkhovskaya ML, Bloch DA, Han H, Gennis RB, Verkhovsky MI. 2011. Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode. Proc Natl Acad Sci USA 108:17320–17324. [PubMed][CrossRef]
79. Goldman BS, Gabbert KK, Kranz RG. 1996. 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 178:6348–6351. [PubMed]
80. Pittman MS, Robinson HC, Poole RK. 2005. A bacterial glutathione transporter ( Escherichia coli CydDC) exports reductant to the periplasm. J Biol Chem 280:32254–32261. [PubMed][CrossRef]
81. Dhar N, McKinney JD. 2010. Mycobacterium tuberculosis persistence mutants identified by screening in isoniazid-treated mice. Proc Natl Acad Sci USA 107:12275–12280. [PubMed][CrossRef]
82. Rowe JJ, Ubbink-Kok T, Molenaar D, Konings WN, Driessen AJ. 1994. NarK is a nitrite-extrusion system involved in anaerobic nitrate respiration by Escherichia coli. Mol Microbiol 12:579–586. [PubMed][CrossRef]
83. Clegg S, Yu F, Griffiths L, Cole JA. 2002. The roles of the polytopic membrane proteins NarK, NarU and NirC in Escherichia coli K-12: two nitrate and three nitrite transporters. Mol Microbiol 44:143–155. [PubMed][CrossRef]
84. Jia W, Cole JA. 2005. Nitrate and nitrite transport in Escherichia coli. Biochem Soc Trans 33:159–161. [PubMed][CrossRef]
85. Sohaskey CD, Wayne LG. 2003. Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 185:7247–7256. [CrossRef]
86. Sohaskey CD. 2005. Regulation of nitrate reductase activity in Mycobacterium tuberculosis by oxygen and nitric oxide. Microbiology 151:3803–3810. [PubMed][CrossRef]
87. Moir JW, Wood NJ. 2001. Nitrate and nitrite transport in bacteria. Cell Mol Life Sci 58:215–224. [PubMed][CrossRef]
88. Kumar A, Deshane JS, Crossman DK, Bolisetty S, Yan BS, Kramnik I, Agarwal A, Steyn AJ. 2008. Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 283:18032–18039. [PubMed][CrossRef]
89. Ohno H, Zhu G, Mohan VP, Chu D, Kohno S, Jacobs WR Jr, Chan J. 2003. The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell Microbiol 5:637–648. [PubMed][CrossRef]
90. 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 198:705–713. [PubMed][CrossRef]
91. Sohaskey CD. 2008. Nitrate enhances the survival of Mycobacterium tuberculosis during inhibition of respiration. J Bacteriol 190:2981–2986. [PubMed][CrossRef]
92. Tan MP, Sequeira P, Lin WW, Phong WY, Cliff P, Ng SH, Lee BH, Camacho L, Schnappinger D, Ehrt S, Dick T, Pethe K, Alonso S. 2010. Nitrate respiration protects hypoxic Mycobacterium tuberculosis against acid- and reactive nitrogen species stresses. PLoS One 5:e13356. [PubMed][CrossRef]
93. Pinto R, Harrison JS, Hsu T, Jacobs WR Jr, Leyh TS. 2007. Sulfite reduction in mycobacteria. J Bacteriol 189:6714–6722. [PubMed][CrossRef]
94. Kuhn M, Steinbuchel A, Schlegel HG. 1984. Hydrogen evolution by strictly aerobic hydrogen bacteria under anaerobic conditions. J Bacteriol 159:633–639. [PubMed]
95. 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 76:717–725. [PubMed][CrossRef]
96. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR. 2003. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48:833–843. [PubMed][CrossRef]
97. 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 USA 98:7534–7539. [PubMed][CrossRef]
98. 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 41:357–366. [PubMed][CrossRef]
99. Coppi MV. 2005. The hydrogenases of Geobacter sulfurreducens: a comparative genomic perspective. Microbiology 151:1239–1254. [PubMed][CrossRef]
100. Marreiros BC, Batista AP, Duarte AM, Pereira MM. 2013. A missing link between complex I and group 4 membrane-bound [NiFe] hydrogenases. Biochimica Biophysica Acta 1827:198–209. [PubMed][CrossRef]
101. He H, Bretl DJ, Penoske RM, Anderson DM, Zahrt TC. 2011. Components of the Rv0081-Rv0088 locus, which encodes a predicted formate hydrogenlyase complex, are coregulated by Rv0081, MprA, and DosR in Mycobacterium tuberculosis. J Bacteriol 193:5105–5118. [PubMed][CrossRef]
102. von Ballmoos C, Cook GM, Dimroth P. 2008. Unique rotary ATP synthase and its biological diversity. Annu Rev Biophys 37:43–64. [PubMed][CrossRef]
103. Tran SL, Cook GM. 2005. The F 1F 0-ATP synthase of Mycobacterium smegmatis is essential for growth. J Bacteriol 187:5023–5028. [PubMed][CrossRef]
104. Friedl P, Hoppe J, Gunsalus RP, Michelsen O, von Meyenburg K, Schairer HU. 1983. Membrane integration and function of the three F 0 subunits of the ATP synthase of Escherichia coli K12. EMBO J 2:99–103. [PubMed]
105. Santana M, Ionescu MS, Vertes A, Longin R, Kunst F, Danchin A, Glaser P. 1994. Bacillus subtilis F 0F 1 ATPase: DNA sequence of the atp operon and characterization of atp mutants. J Bacteriol 176:6802–6811. [PubMed]
106. Cox RA, Cook GM. 2007. Growth regulation in the mycobacterial cell. Curr Mol Med 7:231–245. [PubMed][CrossRef]
107. 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 151:665–672. [PubMed][CrossRef]
108. Koch-Koerfges A, Kabus A, Ochrombel I, Marin K, Bott M. 2012. Physiology and global gene expression of a Corynebacterium glutamicum DeltaF 1F 0-ATP synthase mutant devoid of oxidative phosphorylation. Biochimica Biophysica Acta 1817:370–380. [PubMed][CrossRef]
109. Andries K, Verhasselt P, Guillemont J, Gohlmann 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 307:223–227. [PubMed][CrossRef]
110. 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 72:85–97. [PubMed][CrossRef]
111. 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 3:323–324. [PubMed][CrossRef]
112. Koul A, Vranckx L, Dendouga N, Balemans W, Van den Wyngaert I, Vergauwen K, Gohlmann HW, Willebrords R, Poncelet A, Guillemont J, Bald D, Andries K. 2008. Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J Biol Chem 283:25273–25280. [PubMed][CrossRef]
113. Huitric E, Verhasselt P, Andries K, Hoffner SE. 2007. In vitro antimycobacterial spectrum of a diarylquinoline ATP synthase inhibitor. Antimicrob Agents Chemother 51:4202–4204. [PubMed][CrossRef]
114. 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 54:1022–1028. [PubMed][CrossRef]
115. 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 67:971–980. [PubMed][CrossRef]
116. Haagsma AC, Podasca I, Koul A, Andries K, Guillemont J, Lill H, Bald D. 2011. Probing the interaction of the diarylquinoline TMC207 with its target mycobacterial ATP synthase. PLoS One 6:e23575. [PubMed][CrossRef]
117. 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 287:5340–5356. [PubMed][CrossRef]
118. 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 53:4927–4929. [PubMed][CrossRef]
119. Wayne LG, Sohaskey CD. 2001. Nonreplicating persistence of mycobacterium tuberculosis. Annu Rev Microbiol 55:139–163. [PubMed][CrossRef]
120. Shiloh MU, Manzanillo P, Cox JS. 2008. Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3:323–330. [PubMed][CrossRef]
121. Singh A, Guidry L, Narasimhulu KV, Mai D, Trombley J, Redding KE, Giles GI, Lancaster JR Jr, Steyn AJ. 2007. Mycobacterium tuberculosis WhiB3 responds to O 2 and nitric oxide via its [4Fe-4S] cluster and is essential for nutrient starvation survival. Proc Natl Acad Sci USA 104:11562–11567. [PubMed][CrossRef]
122. Crack J, Green J, Thomson AJ. 2004. Mechanism of oxygen sensing by the bacterial transcription factor fumarate-nitrate reduction (FNR). J Biol Chem 279:9278–9286. [PubMed][CrossRef]
123. Suhail Alam M, Agrawal P. 2008. Matrix-assisted refolding and redox properties of WhiB3/Rv3416 of Mycobacterium tuberculosis H37Rv. Protein Expr Purif 61:83–91. [PubMed][CrossRef]
124. Steyn AJ, Collins DM, Hondalus MK, Jacobs WR Jr, Kawakami RP, Bloom BR. 2002. Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host survival but is dispensable for in vivo growth. Proc Natl Acad Sci USA 99:3147–3152. [PubMed][CrossRef]
125. Rustad TR, Harrell MI, Liao R, Sherman DR. 2008. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One 3:e1502.
126. Gazdik MA, McDonough KA. 2005. Identification of cyclic AMP-regulated genes in Mycobacterium tuberculosis complex bacteria under low-oxygen conditions. J Bacteriol 187:2681–2692. [PubMed][CrossRef]
127. Roberts G, Vadrevu IS, Madiraju MV, Parish T. 2011. Control of CydB and GltA1 expression by the SenX3 RegX3 two component regulatory system of Mycobacterium tuberculosis. PLoS One 6:e21090. [PubMed][CrossRef]
128. Rickman L, Scott C, Hunt DM, Hutchinson T, Menendez MC, Whalan R, Hinds J, Colston MJ, Green J, Buxton RS. 2005. A member of the cAMP receptor protein family of transcription regulators in Mycobacterium tuberculosis is required for virulence in mice and controls transcription of the rpfA gene coding for a resuscitation promoting factor. Mol Microbiol 56:1274–1286. [PubMed][CrossRef]
129. Zhang YJ, Ioerger TR, Huttenhower C, Long JE, Sassetti CM, Sacchettini JC, Rubin EJ. 2012. Global assessment of genomic regions required for growth in Mycobacterium tuberculosis. PLoS Pathog 8:e1002946. [PubMed][CrossRef]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013
2014-06-06
2019-10-14

Abstract:

Mycobacteria inhabit a wide range of intracellular and extracellular environments. Many of these environments are highly dynamic, and therefore mycobacteria are faced with the constant challenge of redirecting their metabolic activity to be commensurate with either replicative growth or a nonreplicative quiescence. A fundamental feature in this adaptation is the ability of mycobacteria to respire, regenerate reducing equivalents, and generate ATP via oxidative phosphorylation. Mycobacteria harbor multiple primary dehydrogenases to fuel the electron transport chain, and two terminal respiratory oxidases, an -type cytochrome oxidase and a cytochrome -type menaquinol oxidase, are present for dioxygen reduction coupled to the generation of a proton motive force (PMF). Hypoxia leads to the downregulation of key respiratory complexes, but the molecular mechanisms regulating this expression are 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, succinate dehydrogenase/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. ATP synthesis by the membrane-bound FF-ATP synthase is essential for growing and nongrowing mycobacteria, and the enzyme is able to function over a wide range of PMF values (aerobic to hypoxic). The discovery of lead compounds that target respiration and oxidative phosphorylation in highlights the importance of this area for the generation of new frontline drugs to combat tuberculosis.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/2/3/MGM2-0015-2013.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013&mimeType=html&fmt=ahah

Figures

Energetics of Respiration and Oxidative Phosphorylation in Mycobacteria
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-1,properties={foaf_givenname=Gregory M., foaf_name=Gregory M. Cook, foaf_surname=Cook, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-2,properties={foaf_givenname=Kiel, foaf_name=Kiel Hards, foaf_surname=Hards, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-3,properties={foaf_givenname=Catherine, foaf_name=Catherine Vilchèze, foaf_surname=Vilchèze, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-4,properties={foaf_givenname=Travis, foaf_name=Travis Hartman, foaf_surname=Hartman, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff4]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-5,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-5,properties={foaf_givenname=Michael, foaf_name=Michael Berney, foaf_surname=Berney, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff5]]}]]
Citation: Cook G, Hards K, Vilchèze C, Hartman T, Berney M. 2014. Energetics of respiration and oxidative phosphorylation in mycobacteria. microbiolspec 2(3): doi:10.1128/microbiolspec.MGM2-0015-2013
/content/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013.fig1
FIGURE 1
Organization and components of the electron transport chain in mycobacteria.
microbiolspec/2/3/MGM2-0015-2013-fig1_thmb.gif
microbiolspec/2/3/MGM2-0015-2013-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

Organization and components of the electron transport chain in mycobacteria.

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.MGM2-0015-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013.fig2
FIGURE 2
The core respiratory chain of mycobacteria and components upregulated under energy-limiting conditions. During exponential growth, mycobacteria use a classical respiratory chain composed of a type I NADH:menaquinone oxidoreductase (Nuo)succinate:menaquinone oxidoreductase 1 (SDH1), cytochrome supercomplex (Qcr-Cta), and FF ATPase. Menaquinone (MQ) is the only quinone present in mycobacterial membranes, and reverse electron transport driven by the PMF is proposed to facilitate the function of SDH1 and similar enzymes (see text). Components in light blue are upregulated in response to energy-limiting conditions ( 6 ). Catalysis and electron flow are indicated by arrows. Abbreviations: Cox, carbon monoxide dehydrogenase; Hyd, hydrogenase; DH, dehydrogenase; A, unidentified electron acceptor.
microbiolspec/2/3/MGM2-0015-2013-fig2_thmb.gif
microbiolspec/2/3/MGM2-0015-2013-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

The core respiratory chain of mycobacteria and components upregulated under energy-limiting conditions. During exponential growth, mycobacteria use a classical respiratory chain composed of a type I NADH:menaquinone oxidoreductase (Nuo)succinate:menaquinone oxidoreductase 1 (SDH1), cytochrome supercomplex (Qcr-Cta), and FF ATPase. Menaquinone (MQ) is the only quinone present in mycobacterial membranes, and reverse electron transport driven by the PMF is proposed to facilitate the function of SDH1 and similar enzymes (see text). Components in light blue are upregulated in response to energy-limiting conditions ( 6 ). Catalysis and electron flow are indicated by arrows. Abbreviations: Cox, carbon monoxide dehydrogenase; Hyd, hydrogenase; DH, dehydrogenase; A, unidentified electron acceptor.

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.MGM2-0015-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013.fig3
FIGURE 3
The preferential respiratory chain of an oxygen-limited mycobacterial cell. Under low-oxygen conditions, a diverse response utilizing alternate electron donors and acceptors, energy-conserving enzymes, and a high-affinity terminal oxidase permits survival under hypoxic conditions. Components in red are upregulated under microaerobic conditions ( 6 ). Catalysis and electron flow are indicated by arrows. The possible PMF-driven reverse electron flow of Sdh2 is not shown, for clarity. Abbreviations: Mqo, malate:menaquinone oxidoreductase; Ndh, type II NADH:menaquinone oxidoreductase; Sdh2, succinate:menaquinone oxidoreductase 2; Nar, nitrate reductase; Cyd, cytochrome oxidase; Frd, FRD; Hyd, hydrogenase; MQ, menaquinone; A, unidentified electron acceptor.
microbiolspec/2/3/MGM2-0015-2013-fig3_thmb.gif
microbiolspec/2/3/MGM2-0015-2013-fig3.gif
Image of FIGURE 3

Click to view

FIGURE 3

The preferential respiratory chain of an oxygen-limited mycobacterial cell. Under low-oxygen conditions, a diverse response utilizing alternate electron donors and acceptors, energy-conserving enzymes, and a high-affinity terminal oxidase permits survival under hypoxic conditions. Components in red are upregulated under microaerobic conditions ( 6 ). Catalysis and electron flow are indicated by arrows. The possible PMF-driven reverse electron flow of Sdh2 is not shown, for clarity. Abbreviations: Mqo, malate:menaquinone oxidoreductase; Ndh, type II NADH:menaquinone oxidoreductase; Sdh2, succinate:menaquinone oxidoreductase 2; Nar, nitrate reductase; Cyd, cytochrome oxidase; Frd, FRD; Hyd, hydrogenase; MQ, menaquinone; A, unidentified electron acceptor.

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.MGM2-0015-2013
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Energetics of Respiration and Oxidative Phosphorylation in Mycobacteria
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-1,properties={foaf_givenname=Gregory M., foaf_name=Gregory M. Cook, foaf_surname=Cook, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-2,properties={foaf_givenname=Kiel, foaf_name=Kiel Hards, foaf_surname=Hards, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-3,properties={foaf_givenname=Catherine, foaf_name=Catherine Vilchèze, foaf_surname=Vilchèze, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-4,properties={foaf_givenname=Travis, foaf_name=Travis Hartman, foaf_surname=Hartman, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff4]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-5,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-5,properties={foaf_givenname=Michael, foaf_name=Michael Berney, foaf_surname=Berney, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013-aff5]]}]]
Citation: Cook G, Hards K, Vilchèze C, Hartman T, Berney M. 2014. Energetics of respiration and oxidative phosphorylation in mycobacteria. microbiolspec 2(3): doi:10.1128/microbiolspec.MGM2-0015-2013
/content/microbiolspec/10.1128/microbiolspec.MGM2-0015-2013.T1
TABLE 1
Electron transport chain components and energy-generating machinery of mycobacteria
Generic image for table

Click to view

TABLE 1

Electron transport chain components and energy-generating machinery of mycobacteria

Source: microbiolspec June 2014 vol. 2 no. 3 doi:10.1128/microbiolspec.MGM2-0015-2013

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error