Effects of Limited Aeration and of the ArcAB System on Intermediary Pyruvate Catabolism in Escherichia coli

ABSTRACT The capacity of Escherichia coli to adapt its catabolism to prevailing redox conditions resides mainly in three catabolic branch points involving (i) pyruvate formate-lyase (PFL) and the pyruvate dehydrogenase complex (PDHc), (ii) the exclusively fermentative enzymes and those of the Krebs cycle, and (iii) the alternative terminal cytochrome bd and cytochrome bo oxidases. A quantitative analysis of the relative catabolic fluxes through these pathways is presented for steady-state glucose-limited chemostat cultures with controlled oxygen availability ranging from full aerobiosis to complete anaerobiosis. Remarkably, PFL contributed significantly to the catabolic flux under microaerobic conditions and was found to be active simultaneously with PDHc and cytochrome bdoxidase-dependent respiration. The synthesis of PFL and cytochromebd oxidase was found to be maximal in the lower microaerobic range but not in a ΔArcA mutant, and we conclude that the Arc system is more active with respect to regulation of these two positively regulated operons during microaerobiosis than during anaerobiosis.

[1]  R. K. Finn.  AGITATION-AERATION IN THE LABORATORY AND IN INDUSTRY , 1954, Bacteriological reviews.

[2]  T. W. James,et al.  Continuous Culture of Microorganisms , 1961 .

[3]  D. Tempest,et al.  Chapter XIII The Continuous Cultivation of Micro-organisms: 2. Construction of a Chemostat , 1970 .

[4]  U. Henning,et al.  Regulation of pyruvate dehydrogenase complex synthesis in Escherichia coli K 12. Identification of the inducing metabolite. , 1970, European journal of biochemistry.

[5]  U. Henning,et al.  Regulation of Pyruvate Dehydrogenase Complex Synthesis in Escherichia coli K12 , 1970 .

[6]  P. J. Phipps,et al.  Chapter III Chemical Analysis of Microbial Cells , 1971 .

[7]  J. Wimpenny,et al.  The redox environment and microbial physiology. I. The transition from anaerobiosis to aerobiosis in continuous cultures of facultative anaerobes. , 1971, Biochimica et biophysica acta.

[8]  Jeffrey H. Miller.  Experiments in molecular genetics , 1972 .

[9]  W. Hempfling,et al.  The 503-nm Pigment of Escherichia coli B: Characterization and Nutritional Conditions Affecting Its Accumulation , 1973, Journal of bacteriology.

[10]  O. Neijssel.  The effect of 2,4-dinitrophenol on the growth of Klebsiella aerogenes NCTC 418 in aerobic chemostat cultures , 1977 .

[11]  W. Hempfling,et al.  Oxygen-limited continuous culture and respiratory energy conservation in Escherichia coli , 1978, Journal of bacteriology.

[12]  E. R. Kashket.  Effects of aerobiosis and nitrogen source on the proton motive force in growing Escherichia coli and Klebsiella pneumoniae cells , 1981, Journal of bacteriology.

[13]  B. L. Taylor,et al.  Aerotaxis in Salmonella typhimurium: role of electron transport , 1981, Journal of bacteriology.

[14]  F. Neidhardt,et al.  2-Oxoacid dehydrogenase complexes of Escherichia coli: cellular amounts and patterns of synthesis , 1983, Journal of bacteriology.

[15]  Y. Anraku,et al.  Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. , 1984, The Journal of biological chemistry.

[16]  Y. Anraku,et al.  Terminal oxidases of Escherichia coli aerobic respiratory chain. I. Purification and properties of cytochrome b562-o complex from cells in the early exponential phase of aerobic growth. , 1984, The Journal of biological chemistry.

[17]  Michael J. Miller,et al.  The cytochrome d complex is a coupling site in the aerobic respiratory chain of Escherichia coli. , 1985, The Journal of biological chemistry.

[18]  H. Kaback,et al.  NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. , 1987, Biochemistry.

[19]  A. Böck,et al.  Anaerobic regulation of pyruvate formate-lyase from Escherichia coli K-12 , 1988, Journal of bacteriology.

[20]  E. Lin,et al.  arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[21]  S. Iuchi,et al.  arcA(dye),大腸菌において好気経路の酵素を抑える働きをする全体的な制御遺伝子 , 1988 .

[22]  D. Clark,et al.  The fermentation pathways of Escherichia coli. , 1989, FEMS microbiology reviews.

[23]  M. Hayashi,et al.  Purification of NADH-ferricyanide dehydrogenase and NADH-quinone reductase from Escherichia coli membranes and their roles in the respiratory chain. , 1989, Biochimica et biophysica acta.

[24]  E. Lin,et al.  A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli , 1989, Journal of bacteriology.

[25]  J. Guest,et al.  FNR and its role in oxygen-regulated gene expression in Escherichia coli. , 1990, FEMS microbiology reviews.

[26]  R. Gennis,et al.  Requirement for terminal cytochromes in generation of the aerobic signal for the arc regulatory system in Escherichia coli: study utilizing deletions and lac fusions of cyo and cyd , 1990, Journal of bacteriology.

[27]  E. Lin,et al.  The arcB gene of Escherichia coli encodes a sensor‐regulator protein for anaerobic repression of the arc modulon , 1990, Molecular microbiology.

[28]  R. Gennis,et al.  Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product , 1990, Journal of bacteriology.

[29]  R. Gennis,et al.  Properties of the two terminal oxidases of Escherichia coli. , 1991, Biochemistry.

[30]  J. Guest,et al.  Adaptive responses to oxygen limitation in Escherichia coli. , 1991, Trends in biochemical sciences.

[31]  G. Sawers,et al.  Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins , 1992, Journal of bacteriology.

[32]  A. Squartini,et al.  Experimental conditions may affect reproducibility of the β-galactosidase assay , 1992 .

[33]  E. Lin,et al.  Purification and phosphorylation of the Arc regulatory components of Escherichia coli , 1992, Journal of bacteriology.

[34]  R P Gunsalus,et al.  Contribution of the fnr and arcA gene products in coordinate regulation of cytochrome o and d oxidase (cyoABCDE and cydAB) genes in Escherichia coli. , 1992, FEMS microbiology letters.

[35]  F. A. Neugebauer,et al.  The free radical in pyruvate formate-lyase is located on glycine-734. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[36]  E. Lin,et al.  Adaptation of Escherichia coli to redox environments by gene expression , 1993, Molecular microbiology.

[37]  S. Iuchi,et al.  Phosphorylation/dephosphorylation of the receiver module at the conserved aspartate residue controls transphosphorylation activity of histidine kinase in sensor protein ArcB of Escherichia coli. , 1993, The Journal of biological chemistry.

[38]  J. Snoep,et al.  Differences in sensitivity to NADH of purified pyruvate dehydrogenase complexes of Enterococcus faecalis, Lactococcus lactis, Azotobacter vinelandii and Escherichia coli: implications for their activity in vivo. , 1993, FEMS microbiology letters.

[39]  R. Gennis,et al.  Energetic efficiency of Escherichia coli: effects of mutations in components of the aerobic respiratory chain , 1993, Journal of bacteriology.

[40]  S. Park,et al.  Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons. , 1994, Research in microbiology.

[41]  G. Sawers,et al.  Isolation and characterization of hypophosphite‐resistant mutants of Escherichia coli: identification of the FocA protein, encoded by the pfl operon, as a putative formate transporter , 1994, Molecular microbiology.

[42]  H. Lawford,et al.  Effect of oxygen on ethanol production by a recombinant ethanologenicE. coli , 1994, Applied biochemistry and biotechnology.

[43]  V. Skulachev,et al.  Induction of the Escherichia coli cytochrome d by low delta mu H+ and by sodium ions. , 1995, European journal of biochemistry.

[44]  T. Mizuno,et al.  Phosphotransfer circuitry of the putative multi‐signal transducer, ArcB, of Escherichia coli: in vitro studies with mutants , 1995, Molecular microbiology.

[45]  E. Lin,et al.  Signal Transduction in the Arc System for Control of Operons Encoding Aerobic Respiratory Enzymes , 1995 .

[46]  S. Iuchi,et al.  Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments. , 1996, Journal of biochemistry.

[47]  H. Holms,et al.  Flux analysis and control of the central metabolic pathways in Escherichia coli. , 1996, FEMS microbiology reviews.

[48]  R. Gunsalus,et al.  Effect of microaerophilic cell growth conditions on expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHJI, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli , 1996, Journal of bacteriology.

[49]  R. Poole,et al.  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. , 1996, Microbiology.

[50]  A. S. Lynch,et al.  Regulation of Gene Expression in Escherichia coli , 1996, Springer US.

[51]  A. S. Lynch,et al.  Regulation of Aerobic and Anaerobic Metabolism by the Arc system , 1996 .

[52]  Jeffrey Green,et al.  The FNR Modulon and FNR-Regulated Gene Expression , 1996 .

[53]  Takeshi Mizuno,et al.  Insights into Multistep Phosphorelay from the Crystal Structure of the C-Terminal HPt Domain of ArcB , 1997, Cell.

[54]  R. Poole,et al.  Respiratory Protection of Nitrogenase Activity in Azotobacter vinelandii—Roles of the Terminal Oxidases , 1997, Bioscience reports.

[55]  A. S. Lynch,et al.  In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli , 1997, Journal of bacteriology.

[56]  Stefan Dipl.-Ing. Schuster,et al.  Regulatory O2 tensions for the synthesis of fermentation products in Escherichia coli and relation to aerobic respiration , 1997, Archives of Microbiology.

[57]  G. Sawers,et al.  A glycyl radical solution: oxygen‐dependent interconversion of pyruvate formate‐lyase , 1998, Molecular microbiology.

[58]  T. Mizuno,et al.  The structure and function of the histidine-containing phosphotransfer (HPt) signaling domain of the Escherichia coli ArcB sensor. , 1998, Journal of biochemistry.

[59]  M. M. Attwood,et al.  Environmental control of pyruvate dehydrogenase complex expression in Escherichia coli. , 1998, FEMS microbiology letters.

[60]  T. Mizuno,et al.  Mutational analysis of the histidine-containing phosphotransfer (HPt) signaling domain of the ArcB sensor in Escherichia coli. , 1998, Bioscience, biotechnology, and biochemistry.

[61]  T. Mizuno,et al.  A Dual-Signaling Mechanism Mediated by the ArcB Hybrid Sensor Kinase Containing the Histidine-Containing Phosphotransfer Domain in Escherichia coli , 1998, Journal of bacteriology.

[62]  E. Lin,et al.  Signal Decay through a Reverse Phosphorelay in the Arc Two-component Signal Transduction System* , 1998, The Journal of Biological Chemistry.

[63]  I. Zhulin,et al.  PAS Domains: Internal Sensors of Oxygen, Redox Potential, and Light , 1999, Microbiology and Molecular Biology Reviews.

[64]  Svetlana Alexeeva,et al.  The Steady-State Internal Redox State (NADH/NAD) Reflects the External Redox State and Is Correlated with Catabolic Adaptation in Escherichia coli , 1999, Journal of bacteriology.

[65]  Ann M Stock,et al.  Two-component signal transduction. , 2000, Annual review of biochemistry.