1887

Abstract

In spite of the large number of reports on the aerobic respiratory chain of , from gene transcription regulation to enzyme kinetics and structural studies, an integrative perspective of this pathway is yet to be produced. Here, a multi-level analysis of the aerobic respiratory chain of was performed to find correlations between gene transcription, enzyme activity, growth dynamics, and supercomplex formation and composition. The transcription level of all genes encoding the aerobic respiratory chain of varied significantly in response to bacterial growth. Coordinated expression patterns were observed between the genes encoding NADH : quinone oxidoreductase and complex I (NDH-1), alternative NADH : quinone oxidoreductase (NDH-2) and cytochrome I, and also between and , encoding succinate dehydrogenase and cytochrome II, respectively. In general, the rates of the respiratory chain activities increased from mid-exponential to late-stationary phase, with no significant further variation occurring until the mid-stationary phase. Multi-level correlations between gene transcription, enzyme activity and growth dynamics were also found in this study. The previously reported NADH dehydrogenase and formate : oxygen oxidoreductase supercomplexes of were already assembled at mid-exponential phase and remained throughout growth. A new succinate oxidase supercomplex composed of succinate dehydrogenase and cytochrome II was identified, in agreement with the suggestion provided by the coordinated transcription of and .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.056531-0
2012-09-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/9/2408.html?itemId=/content/journal/micro/10.1099/mic.0.056531-0&mimeType=html&fmt=ahah

References

  1. Abdi H. . ( 2007; ). Kendall Rank Correlation. . In Encyclopedia of Measurement and Statistics, pp. 508–510. Edited by Salkind N. J. . . Thousand Oaks, CA:: Sage;.
    [Google Scholar]
  2. Bastet L. , Dubé A. , Massé E. , Lafontaine D. A. . ( 2011; ). New insights into riboswitch regulation mechanisms. . Mol Microbiol 80:, 1148–1154. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bekker M. , Teixeira de Mattos M. J. , Hellingwerf K. J. . ( 2006; ). The role of two-component regulation systems in the physiology of the bacterial cell. . Sci Prog 89:, 213–242. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bekker M. , de Vries S. , Ter Beek A. , Hellingwerf K. J. , de Mattos M. J. . ( 2009; ). Respiration of Escherichia coli can be fully uncoupled via the nonelectrogenic terminal cytochrome bd-II oxidase. . J Bacteriol 191:, 5510–5517. [CrossRef] [PubMed]
    [Google Scholar]
  5. Bekker M. , Alexeeva S. , Laan W. , Sawers G. , Teixeira de Mattos J. , Hellingwerf K. . ( 2010; ). The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool. . J Bacteriol 192:, 746–754. [CrossRef] [PubMed]
    [Google Scholar]
  6. Benoit S. , Abaibou H. , Mandrand-Berthelot M. A. . ( 1998; ). Topological analysis of the aerobic membrane-bound formate dehydrogenase of Escherichia coli . . J Bacteriol 180:, 6625–6634.[PubMed]
    [Google Scholar]
  7. Borisov V. B. , Murali R. , Verkhovskaya M. L. , Bloch D. A. , Han H. , Gennis R. B. , Verkhovsky M. I. . ( 2011; ). Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode. . Proc Natl Acad Sci U S A 108:, 17320–17324. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bragg P. D. , Hou C. . ( 1967; ). Reduced nicotinamide adenine dinucleotide oxidation in Escherichia coli particles. II. NADH dehydrogenases. . Arch Biochem Biophys 119:, 202–208. [CrossRef] [PubMed]
    [Google Scholar]
  9. Cecchini G. , Maklashina E. , Yankovskaya V. , Iverson T. M. , Iwata S. . ( 2003; ). Variation in proton donor/acceptor pathways in succinate : quinone oxidoreductases. . FEBS Lett 545:, 31–38. [CrossRef] [PubMed]
    [Google Scholar]
  10. Dudkina N. V. , Eubel H. , Keegstra W. , Boekema E. J. , Braun H. P. . ( 2005; ). Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III. . Proc Natl Acad Sci U S A 102:, 3225–3229. [CrossRef] [PubMed]
    [Google Scholar]
  11. Dudkina N. V. , Kouril R. , Peters K. , Braun H. P. , Boekema E. J. . ( 2010; ). Structure and function of mitochondrial supercomplexes. . Biochim Biophys Acta 1797:, 664–670. [CrossRef] [PubMed]
    [Google Scholar]
  12. Falconi M. , Higgins N. P. , Spurio R. , Pon C. L. , Gualerzi C. O. . ( 1993; ). Expression of the gene encoding the major bacterial nucleotide protein H-NS is subject to transcriptional auto-repression. . Mol Microbiol 10:, 273–282. [CrossRef] [PubMed]
    [Google Scholar]
  13. Georgiou C. D. , Dueweke T. J. , Gennis R. B. . ( 1988; ). Regulation of expression of the cytochrome d terminal oxidase in Escherichia coli is transcriptional. . J Bacteriol 170:, 961–966.[PubMed]
    [Google Scholar]
  14. Govantes F. , Orjalo A. V. , Gunsalus R. P. . ( 2000; ). Interplay between three global regulatory proteins mediates oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon. . Mol Microbiol 38:, 1061–1073. [CrossRef] [PubMed]
    [Google Scholar]
  15. Gunsalus R. P. . ( 1992; ). Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. . J Bacteriol 174:, 7069–7074.[PubMed]
    [Google Scholar]
  16. Hatefi Y. . ( 1978a; ). Resolution of complex II and isolation of succinate dehydrogenase (EC 1.3.99.1). . Methods Enzymol 53:, 27–35. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hatefi Y. . ( 1978b; ). Preparation and properties of NADH: ubiquinone oxidoreductase (complexI), EC 1.6.5.3. . Methods Enzymol 53:, 11–14. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hendler R. W. , Burgess A. H. . ( 1972; ). Respiration and protein synthesis in Escherichia coli membrane-envelope fragments. VI. Solubilization and characterization of the electron transport chain. . J Cell Biol 55:, 266–281. [CrossRef] [PubMed]
    [Google Scholar]
  19. Ingledew W. J. , Poole R. K. . ( 1984; ). The respiratory chains of Escherichia coli . . Microbiol Rev 48:, 222–271.[PubMed]
    [Google Scholar]
  20. Jackson L. , Blake T. , Green J. . ( 2004; ). Regulation of ndh expression in Escherichia coli by Fis. . Microbiology 150:, 407–413. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kahm M. , Hasenbrink G. , Lichtenberg-Frate H. , Ludwig J. , Kschischo M. . ( 2010; ). grofit: fitting biological growth curves with R. . J Stat Softw 33:, 1–21.[PubMed]
    [Google Scholar]
  22. Kasahara M. , Anraku Y. . ( 1974; ). Succinate dehydrogenase of Escherichia coli membrane vesicles. Activation and properties of the enzyme. . J Biochem 76:, 959–966.[PubMed]
    [Google Scholar]
  23. Kendall M. . ( 1938; ). A new measure of rank correlation. . Biometrika 30:, 81–89.[CrossRef]
    [Google Scholar]
  24. Keseler I. M. , Collado-Vides J. , Santos-Zavaleta A. , Peralta-Gil M. , Gama-Castro S. , Muñiz-Rascado L. , Bonavides-Martinez C. , Paley S. , Krummenacker M. . & other authors ( 2011; ). EcoCyc: a comprehensive database of Escherichia coli biology. . Nucleic Acids Res 39: (Database issue), D583–D590. [CrossRef] [PubMed]
    [Google Scholar]
  25. Kita K. , Konishi K. , Anraku Y. . ( 1984; ). Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b 558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. . J Biol Chem 259:, 3375–3381.[PubMed]
    [Google Scholar]
  26. Kramer G. , Sprenger R. R. , Nessen M. A. , Roseboom W. , Speijer D. , de Jong L. , de Mattos M. J. , Back J. , de Koster C. G. . ( 2010; ). Proteome-wide alterations in Escherichia coli translation rates upon anaerobiosis. . Mol Cell Proteomics 9:, 2508–2516. [CrossRef] [PubMed]
    [Google Scholar]
  27. Krause F. , Seelert H. . ( 2008; ). Detection and analysis of protein-protein interactions of organellar and prokaryotic proteomes by blue native and colorless native gel electrophoresis. . Curr Protoc Protein Sci 51:, 14.11.1–14.11.36.[PubMed]
    [Google Scholar]
  28. Laemmli U. K. . ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef] [PubMed]
    [Google Scholar]
  29. Lennox E. S. . ( 1955; ). Transduction of linked genetic characters of the host by bacteriophage P1. . Virology 1:, 190–206. [CrossRef] [PubMed]
    [Google Scholar]
  30. Maddalo G. , Stenberg-Bruzell F. , Götzke H. , Toddo S. , Björkholm P. , Eriksson H. , Chovanec P. , Genevaux P. , Lehtiö J. . & other authors ( 2011; ). Systematic analysis of native membrane protein complexes in Escherichia coli . . J Proteome Res 10:, 1848–1859. [CrossRef] [PubMed]
    [Google Scholar]
  31. Melo A. M. P. , Bandeiras T. M. , Teixeira M. . ( 2004; ). New insights into type II NAD(P)H : quinone oxidoreductases. . Microbiol Mol Biol Rev 68:, 603–616. [CrossRef] [PubMed]
    [Google Scholar]
  32. Minagawa J. , Mogi T. , Gennis R. B. , Anraku Y. . ( 1992; ). Identification of heme and copper ligands in subunit I of the cytochrome bo complex in Escherichia coli . . J Biol Chem 267:, 2096–2104.[PubMed]
    [Google Scholar]
  33. Pereira M. M. , Bandeiras T. M. , Fernandes A. S. , Lemos R. S. , Melo A. M. P. , Teixeira M. . ( 2004; ). Respiratory chains from aerobic thermophilic prokaryotes. . J Bioenerg Biomembr 36:, 93–105. [CrossRef] [PubMed]
    [Google Scholar]
  34. Pfaffl M. W. . ( 2001; ). A new mathematical model for relative quantification in real-time RT-PCR. . Nucleic Acids Res 29:, e45. [CrossRef] [PubMed]
    [Google Scholar]
  35. Price C. E. , Driessen A. J. . ( 2010; ). Biogenesis of membrane bound respiratory complexes in Escherichia coli . . Biochim Biophys Acta 1803:, 748–766. [CrossRef] [PubMed]
    [Google Scholar]
  36. Prunetti L. , Infossi P. , Brugna M. , Ebel C. , Giudici-Orticoni M. T. , Guiral M. . ( 2010; ). New functional sulfide oxidase-oxygen reductase supercomplex in the membrane of the hyperthermophilic bacterium Aquifex aeolicus . . J Biol Chem 285:, 41815–41826. [CrossRef] [PubMed]
    [Google Scholar]
  37. Puustinen A. , Finel M. , Virkki M. , Wikström M. . ( 1989; ). Cytochrome o (bo) is a proton pump in Paracoccus denitrificans and Escherichia coli . . FEBS Lett 249:, 163–167. [CrossRef] [PubMed]
    [Google Scholar]
  38. Puustinen A. , Finel M. , Haltia T. , Gennis R. B. , Wikström M. . ( 1991; ). Properties of the two terminal oxidases of Escherichia coli . . Biochemistry 30:, 3936–3942. [CrossRef] [PubMed]
    [Google Scholar]
  39. Rolfe M. D. , Ter Beek A. , Graham A. I. , Trotter E. W. , Asif H. M. , Sanguinetti G. , de Mattos J. T. , Poole R. K. , Green J. . ( 2011; ). Transcript profiling and inference of Escherichia coli K-12 ArcA activity across the range of physiologically relevant oxygen concentrations. . J Biol Chem 286:, 10147–10154. [CrossRef] [PubMed]
    [Google Scholar]
  40. Rozen S. , Skaletsky H. . ( 2000; ). Primer3 on the WWW for general users and for biologist programmers. . In Bioinformatics Methods and Protocols, Methods in Molecular Biology, pp. 365–386. Edited by Krawetz S. , Misener S. . . Totowa, NJ:: Humana Press;. [CrossRef]
    [Google Scholar]
  41. Schägger H. , von Jagow G. . ( 1991; ). Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. . Anal Biochem 199:, 223–231. [CrossRef] [PubMed]
    [Google Scholar]
  42. Smith P. K. , Krohn R. I. , Hermanson G. T. , Mallia A. K. , Gartner F. H. , Provenzano M. D. , Fujimoto E. K. , Goeke N. M. , Olson B. J. , Klenk D. C. . ( 1985; ). Measurement of protein using bicinchoninic acid. . Anal Biochem 150:, 76–85. [CrossRef] [PubMed]
    [Google Scholar]
  43. Sousa P. M. F. , Silva S. T. , Hood B. L. , Charro N. , Carita J. N. , Vaz F. , Penque D. , Conrads T. P. , Melo A. M. P. . ( 2011; ). Supramolecular organizations in the aerobic respiratory chain of Escherichia coli . . Biochimie 93:, 418–425. [CrossRef] [PubMed]
    [Google Scholar]
  44. Spiro S. , Guest J. R. . ( 1990; ). FNR and its role in oxygen-regulated gene expression in Escherichia coli . . FEMS Microbiol Rev 6:, 399–428. [CrossRef] [PubMed]
    [Google Scholar]
  45. Stroh A. , Anderka O. , Pfeiffer K. , Yagi T. , Finel M. , Ludwig B. , Schägger H. . ( 2004; ). Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans . . J Biol Chem 279:, 5000–5007. [CrossRef] [PubMed]
    [Google Scholar]
  46. Sturr M. G. , Krulwich T. A. , Hicks D. B. . ( 1996; ). Purification of a cytochrome bd terminal oxidase encoded by the Escherichia coli app locus from a Δcyo Δcyd strain complemented by genes from Bacillus firmus OF4. . J Bacteriol 178:, 1742–1749.[PubMed]
    [Google Scholar]
  47. Towbin H. , Staehelin T. , Gordon J. . ( 1979; ). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. . Proc Natl Acad Sci U S A 76:, 4350–4354. [CrossRef] [PubMed]
    [Google Scholar]
  48. 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] [PubMed]
    [Google Scholar]
  49. Van Suijdam J. C. , Kossen N. F. W. , Joha A. C. . ( 1978; ). Model for oxygen transfer in a shake flask. . Biotechnol Bioeng 20:, 1695–1709. [CrossRef]
    [Google Scholar]
  50. Vandesompele J. , De Preter K. , Pattyn F. , Poppe B. , Van Roy N. , De Paepe A. , Speleman F. . ( 2002; ). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. . Genome Biol 3:, RESEARCH0034. [CrossRef] [PubMed]
    [Google Scholar]
  51. Wackwitz B. , Bongaerts J. , Goodman S. D. , Unden G. . ( 1999; ). Growth phase-dependent regulation of nuoA-N expression in Escherichia coli K-12 by the Fis protein: upstream binding sites and bioenergetic significance. . Mol Gen Genet 262:, 876–883. [CrossRef] [PubMed]
    [Google Scholar]
  52. Wei Y. , Lee J. M. , Richmond C. , Blattner F. R. , Rafalski J. A. , LaRossa R. A. . ( 2001; ). High-density microarray-mediated gene expression profiling of Escherichia coli . . J Bacteriol 183:, 545–556. [CrossRef] [PubMed]
    [Google Scholar]
  53. Wittig I. , Braun H. P. , Schägger H. . ( 2006; ). Blue native PAGE. . Nat Protoc 1:, 418–428. [CrossRef] [PubMed]
    [Google Scholar]
  54. Wittig I. , Beckhaus T. , Wumaier Z. , Karas M. , Schägger H. . ( 2010; ). Mass estimation of native proteins by blue native electrophoresis: principles and practical hints. . Mol Cell Proteomics 9:, 2149–2161. [CrossRef] [PubMed]
    [Google Scholar]
  55. Zerbetto E. , Vergani L. , Dabbeni-Sala F. . ( 1997; ). Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. . Electrophoresis 18:, 2059–2064. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.056531-0
Loading
/content/journal/micro/10.1099/mic.0.056531-0
Loading

Data & Media loading...

Supplements

Table S2 

PDF

Table S1 

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error