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 .

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2012-09-01
2020-07-15
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References

  1. Abdi H.. ( 2007;). Kendall Rank Correlation. Encyclopedia of Measurement and Statistics508–510 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 Microbiol80:1148–1154 [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 Prog89:213–242 [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 Bacteriol191:5510–5517 [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 Bacteriol192:746–754 [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 Bacteriol180:6625–6634[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 A108:17320–17324 [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 Biophys119:202–208 [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 Lett545:31–38 [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 A102:3225–3229 [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 Acta1797:664–670 [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 Microbiol10:273–282 [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 Bacteriol170:961–966[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 Microbiol38:1061–1073 [CrossRef][PubMed]
    [Google Scholar]
  15. Gunsalus R. P.. ( 1992;). Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J Bacteriol174:7069–7074[PubMed]
    [Google Scholar]
  16. Hatefi Y.. ( 1978a;). Resolution of complex II and isolation of succinate dehydrogenase (EC 1.3.99.1). Methods Enzymol53:27–35 [CrossRef][PubMed]
    [Google Scholar]
  17. Hatefi Y.. ( 1978b;). Preparation and properties of NADH: ubiquinone oxidoreductase (complexI), EC 1.6.5.3. Methods Enzymol53:11–14 [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 Biol55:266–281 [CrossRef][PubMed]
    [Google Scholar]
  19. Ingledew W. J., Poole R. K.. ( 1984;). The respiratory chains of Escherichia coli . Microbiol Rev48:222–271[PubMed]
    [Google Scholar]
  20. Jackson L., Blake T., Green J.. ( 2004;). Regulation of ndh expression in Escherichia coli by Fis. Microbiology150:407–413 [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 Softw33:1–21[PubMed]
    [Google Scholar]
  22. Kasahara M., Anraku Y.. ( 1974;). Succinate dehydrogenase of Escherichia coli membrane vesicles. Activation and properties of the enzyme. J Biochem76:959–966[PubMed]
    [Google Scholar]
  23. Kendall M.. ( 1938;). A new measure of rank correlation. Biometrika30:81–89[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 Res39:Database issueD583–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 Chem259:3375–3381[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 Proteomics9:2508–2516 [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 Sci51:14.11.1–14.11.36[PubMed]
    [Google Scholar]
  28. Laemmli U. K.. ( 1970;). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685 [CrossRef][PubMed]
    [Google Scholar]
  29. Lennox E. S.. ( 1955;). Transduction of linked genetic characters of the host by bacteriophage P1. Virology1:190–206 [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 Res10:1848–1859 [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 Rev68:603–616 [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 Chem267:2096–2104[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 Biomembr36:93–105 [CrossRef][PubMed]
    [Google Scholar]
  34. Pfaffl M. W.. ( 2001;). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res29:e45 [CrossRef][PubMed]
    [Google Scholar]
  35. Price C. E., Driessen A. J.. ( 2010;). Biogenesis of membrane bound respiratory complexes in Escherichia coli . Biochim Biophys Acta1803:748–766 [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 Chem285:41815–41826 [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 Lett249:163–167 [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 . Biochemistry30:3936–3942 [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 Chem286:10147–10154 [CrossRef][PubMed]
    [Google Scholar]
  40. Rozen S., Skaletsky H.. ( 2000;). Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols, Methods in Molecular Biology365–386 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 Biochem199:223–231 [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 Biochem150:76–85 [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 . Biochimie93:418–425 [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 Rev6:399–428 [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 Chem279:5000–5007 [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 Bacteriol178:1742–1749[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 A76:4350–4354 [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 Acta1320:217–234 [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 Bioeng20:1695–1709 [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 Biol3: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 Genet262:876–883 [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 Bacteriol183:545–556 [CrossRef][PubMed]
    [Google Scholar]
  53. Wittig I., Braun H. P., Schägger H.. ( 2006;). Blue native PAGE. Nat Protoc1:418–428 [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 Proteomics9:2149–2161 [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. Electrophoresis18:2059–2064 [CrossRef][PubMed]
    [Google Scholar]
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