Chapter 11 : Global Responses of Bacteria to Oxygen Deprivation

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This chapter highlights some of the advances on both the molecular mechanisms of oxygen (O) sensing and the biological responses to O limitation. In the first part of the chapter, the major regulators that control expression of anaerobic respiratory pathways are described, with focus on the well studied examples from K-12. Many facultative bacteria have anaerobic lifestyles that depend on pathways not found in enteric bacteria. A section reviews the master regulators of these anaerobic lifestyles, describing how their activity responds to O deprivation, highlighting commonalities and differences to the responses described for enterobacteria, and placing them into a metabolic context of the systems they control. A recurring theme in the review is that multiple transcription factors collaborate in a given organism to control gene expression in response to changes in O. In , decreased expression of the genes encoding aerobic respiratory functions under anaerobic growth conditions is largely mediated by the aerobic respiration control (Arc) A and ArcB two-component system. Regulation of anaerobic respiration in the γ-proteobacterium has attracted great interest because of the broad diversity of electron acceptors (>14) that these bacteria can respire, including metal oxides. The use of cofactors such as flavins, heme, and [Fe-S] clusters generally sense O directly, using chemistry reflecting their well-described roles in biological reactions.

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11

Key Concept Ranking

Gene Expression and Regulation
Bacterial Proteins
Gene Expression
Cellular Processes
Anaerobic Respiration
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Image of Figure 1.
Figure 1.

Distribution of genes regulated by FNR in K-12. The percentage of genes belonging to relevant functional groups, whose expression changed in response to FNR as determined in the genome-wide transcription studies of Kang et al. ( ), are indicated.

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11
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Image of Figure 2.
Figure 2.

Cellular levels of FNR are calibrated to efficiently respond to O Regulation of FNR activity and synthesis under anaerobic (top panel) and aerobic (bottom panel) growth conditions (Mettert et al., ). The Isc pathway inserts [Fe-S] clusters into FNR under both aerobic and anaerobic conditions but the active [4Fe-4S]-FNR form accumulates only under anaerobic conditions because of the O instability of the [4Fe-4S] cluster. O promotes the degradation of the [4Fe-4S] cluster to the [2Fe-2S] cluster and superoxide promotes the loss of the [2Fe-2S] cluster to apoFNR. In addition, negative autoregulation of transcription occurs under anaerobic conditions, whereas a portion of FNR is degraded via the ClpXP protease under aerobic conditions.

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11
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Image of Figure 3.
Figure 3.

Regulation of ArcB by quinones. During aerobic respiration in , electrons flow from donors to produce reduced ubiquinone (UQH), which is then used to reduce O to HO via cytochrome oxidase (C.O.), generating a higher ratio of UQ to UQH. As previously proposed (Malpica et al., ), the excess UQ under aerobic conditions oxidizes the cytosolic thiols of ArcB Cys 180 and 241 to form intermolecular disulfide bonds, inactivating the ArcB kinase activity, which uses its cytosolic domain for a His-Asp-His phosphorelay. The model also predicts that, in the absence of an electron acceptor, UQ levels are too low to maintain this disulfide bond in dimeric ArcB. The question mark denotes that it is not known how the disulfide bond is reduced back to the thiol state. This figure is adapted from Malpica et al. ( ).

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11
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1. Arslan, E.,, A. Kannt,, L. Thony-Meyer, and, H. Hennecke. 2000. The symbiotically essential cbb3-type oxidase of Bradyrhizobium japonicum is a proton pump. FEBS Lett. 470:710.
2. Bartolini,, E., E. Frigimelica,, S. Giovinazzi,, G. Galli,, Y. Shaik,, C. Genco,, J. A. Welsch,, D. M. Granoff,, G. Grandi, and, R. Grifantini. 2006. Role of FNR and FNR-regulated, sugar fermentation genes in Neisseria meningitidis infection. Mol. Microbiol. 60:963972.
3. Bates,, D. M.,, C. V. Popescu,, N. Khoroshilova,, K. Vogt,, H. Beinert,, E. Münck, and, P. J. Kiley. 2000. Substitution of leucine 28 with histidine in the Escherichia coli transcription factor FNR results in increased stability of the [4Fe-4S]2+ cluster to oxygen. J. Biol. Chem. 275:62346240.
4. Bauer, C. E., and, T. H. Bird. 1996. Regulatory circuits controlling photosynthesis gene expression. Cell 85:58.
5. Bauer, E.,, T. Kaspar,, H. M. Fischer, and, H. Hennecke. 1998. Expression of the fixR-nifA operon in Bradyrhizobium japonicum depends on a new response regulator, RegR. J. Bacteriol. 180:38533863.
6. Bekker,, M., S. Alexeeva,, W. Laan,, G. Sawers,, J. Teixeira de Mattos, and, K. Hellingwerf. 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. 192:746754.
7. Beliaev,, A. S.,, D. K. Thompson,, M. W. Fields,, L. Wu,, D. P. Lies,, K. H. Nealson, and, J. Zhou. 2002. Microarray transcription profiling of a Shewanella oneidensis etrA mutant. J. Bacteriol. 184:46124616.
8. Bowman, W. C.,, S. Du,, C. E. Bauer, and, R. G. Kranz. 1999. In vitro activation and repression of photosynthesis gene transcription in Rhodobacter capsulatus. Mol. Microbiol. 33:429437.
9. Braatsch, S.,, M. Gomelsky,, S. Kuphal, and, G. Klug. 2002. A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides. Mol. Microbiol. 45:827836.
10. Bruscella, P.,, J. M. Eraso,, J. H. Roh, and, S. Kaplan. 2008. The use of chromatin immunoprecipitation to define PpsR binding activity in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 190:68176828.
11. Charania,, M. A.,, K. L. Brockman,, Y. Zhang,, A. Banerjee,, G. E. Pinchuk,, J. K. Fredrickson,, A. S. Beliaev, and, D. A. Saffarini. 2009. Involvement of a membrane-bound class III adenylate cyclase in regulation of anaerobic respiration in Shewanella oneidensis MR-1. J. Bacteriol. 191:42984306.
12. Cohen-Bazire, G. W.,, W. R. Sistrom, and, R. Y. Stanier. 1957. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J. Cell. Comp. Physiol. 49:2568.
13. Comolli,, J., A. Carl,, C. Hall, and, T. J. Donohue. 2002. Transcriptional activation of the Rhodobacter sphaeroides cytochrome c2 gene P2 promoter by the response regulator PrrA. J. Bacteriol. 184:390399.
14. Comolli, J. C., and, T. J. Donohue. 2004. Differences in two Pseudomonas aeruginosa cbb3 oxidases. Mol. Microbiol. 51:11931203.
15. Constantinidou,, C.,, J. L. Hobman,, L. Griffiths,, M. D. Patel,, C. W. Penn,, J. A. Cole, and, T. W. Overton. 2006. A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J. Biol. Chem. 281:48024815.
16. Crack, J., J. Green, and, A. J. Thomson. 2004. Mechanism of oxygen sensing by the bacterial transcription factor fumaratenitrate reduction (FNR). J. Biol. Chem. 279:92789286.
17. Crack,, J. C.,, A. A. Gaskell,, J. Green,, M. R. Cheesman,, N. E. Le Brun, and, A. J. Thomson. 2008a. Influence of the environment on the [4Fe-4S]2+ to [2Fe-2S]2+ cluster switch in the transcriptional regulator FNR. J. Am. Chem. Soc. 130:17491758.
18. Crack,, J. C.,, A. J. Jervis,, A. A. Gaskell,, G. F. White,, J. Green,, A. J. Thomson, and, N. E. Le Brun. 2008b. Signal perception by FNR: the role of the iron-sulfur cluster. Biochem. Soc. Trans. 36:11441148.
19. Crack,, J. C.,, J. Green,, M. R. Cheesman,, N. E. Le Brun, and, A. J. Thomson. 2007. Superoxide-mediated amplification of the oxygen-induced switch from [4Fe-4S] to [2Fe-2S] clusters in the transcriptional regulator FNR. Proc. Natl. Acad. Sci. USA 104:20922097.
20. Crack, J. C.,, J. Green,, N. E. Le Brun, and, A. J. Thomson. 2006. Detection of sulfide release from the oxygen-sensing [4Fe-4S] cluster of FNR. J. Biol. Chem. 281:1890918913.
21. Daldal,, F., M. Deshmukh, and, R. Prince. 2003. Membrane-anchored cytochrome c as an electron carrier in photosynthesis and respiration: past, present and future of an unexpected discovery. Photosynth. Res. 76:127134.
22. Dixon, R., and, D. Kahn. 2004. Genetic regulation of biological nitrogen fixation. Nat. Rev. Microbiol. 2:621631.
23. Dong,, C., S. Elsen,, L. R. Swem, and, C. E. Bauer. 2002. AerR, a second aerobic repressor of photosynthesis gene expression in Rhodobacter capsulatus. J. Bacteriol. 184:28052814.
24. Dragnea,, V.,, A. I. Arunkumar,, H. Yuan,, D. P. Giedroc, and, C. E. Bauer. 2009. Spectroscopic studies of the AppA BLUF domain from Rhodobacter sphaeroides: addressing movement of tryptophan 104 in the signaling state. Biochemistry 48:99699979.
25. Dubbs, J. M., and, F. R. Tabita. 2004. Regulators of nonsulfur purple phototrophic bacteria and the interactive control of CO2 assimilation, nitrogen fixation, hydrogen metabolism and energy generation. FEMS Microbiol. Rev. 28:353376.
26. Dubbs,, J. M.,, T. H. Bird,, C. E. Bauer, and, F. R. Tabita. 2000. Interaction of CbbR and RegA* transcription regulators with the Rhodobacter sphaeroides cbbI promoter-operator region. J. Biol. Chem. 275:1922419230.
27. Ducluzeau, A. L.,, S. Ouchane, and, W. Nitschke. 2008. The cbb3 oxidases are an ancient innovation of the domain bacteria. Mol. Biol. Evol. 25:11581166.
28. Dufour,, Y.,, P. J. Kiley, and, T. J. Donohue. 2010. Reconstruction of the core and extended regulons of global transcription factors. PLOS Genet. 6:e1001027.
29. Einsle, O., and, P. M. Kroneck. 2004. Structural basis of denitrification. Biol. Chem. 385:875883.
30. Elsen,, S.,, L. R. Swem,, D. L. Swem, and, C. E. Bauer. 2004. RegB/RegA, a highly conserved redox-responding global regulatory system. Microbiol. Mol. Biol. Rev. 68:263279.
31. Emmerich,, R., H. Hennecke, and, H.-M. Fischer. 2000. Evidence for a functional similarity between the two-component regulatory systems RegSR, ActSR, and RegBA (PrrBA) in a-proteobacteria. Arch. Microbiol. 174:307313.
32. Emmerich,, R., K. Panglungtshang,, P. Strehler,, H. Hennecke, and, H. M. Fischer. 1999. Phosphorylation, dephosphorylation and DNA-binding of the Bradyrhizobium japonicum RegSR two-component regulatory proteins. Eur. J. Biochem. 263:455463.
33. Eraso, J. M., and, S. Kaplan. 1994. prrA, a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides. J. Bacteriol. 176:3243.
34. Eraso, J. M., and, S. Kaplan. 1996. Complex regulatory activities associated with the histidine kinase PrrB in expression of photosynthesis genes in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 178:70377046.
35. Fenner,, B. J.,, R. P. Tiwari,, W. G. Reeve,, M. J. Dilworth, and, A. R. Glenn. 2004. Sinorhizobium medicae genes whose regulation involves the ActS and/or ActR signal transduction proteins. FEMS Microbiol. Lett. 236:2131.
36. Fernandez-Pinar, R.,, J. L. Ramos,, J. J. Rodriguez-Herva, and, M. Espinosa-Urgel. 2008. A two-component regulatory system integrates redox state and population density sensing in Pseudomonas putida. J. Bacteriol. 190:76667674.
37. Gao,, H., X. Wang,, Z. K. Yang,, T. Palzkill, and, J. Zhou. 2008. Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses. BMC Genomics 9:42.
38. Gao, R., and, A. M. Stock. 2009. Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63:133154.
39. Gest, H., and, R. Blankenship. 2004. Time line of discoveries: anoxygenic bacterial photosynthesis. Photosynth. Res. 80:5970.
40. Giel,, J. L.,, D. Rodionov,, M. Liu,, F. R. Blattner, and, P. J. Kiley. 2006. IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol. Microbiol. 60:10581075.
41. Goh,, E. B.,, P. J. Bledsoe,, L. L. Chen,, P. Gyaneshwar,, V. Stewart, and, M. M. Igo. 2005. Hierarchical control of anaerobic gene expression in Escherichia coli K-12: the nitrate-responsive NarX-NarL regulatory system represses synthesis of the fumarate-responsive DcuS-DcuR regulatory system. J. Bacteriol. 187:48904899.
42. Gomelsky,, M.,, I. M. Horne,, H. J. Lee,, J. M. Pemberton,, A. G. McEwan, and, S. Kaplan. 2000. Domain structure, oligomeric state, and mutational analysis of PpsR, the Rhodobacter sphaeroides repressor of photosystem gene expression. J. Bacteriol. 182:22532261.
43. Gomelsky, M., and, G. Klug. 2002. BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem. Sci. 27:497500.
44. Grabbe, R., A. Kuhn, and, R. A. Schmitz. 2001. Cloning, sequencing and characterization of Fnr from Klebsiella pneumoniae. Antonie Van Leeuwenhoek 79:319326.
45. Grainger,, D. C.,, H. Aiba,, D. Hurd,, D. F. Browning, and, S. J. Busby. 2007. Transcription factor distribution in Escherichia coli: studies with FNR protein. Nucleic Acids Res. 35:269278.
46. Green,, J.,, J. C. Crack,, A. J. Thomson, and, N. E. LeBrun. 2009. Bacterial sensors of oxygen. Curr. Opin. Microbiol. 12:145151.
47. Green, J., and, M. L. Baldwin. 1997. HlyX, the FNR homologue of Actinobacillus pleuropneumoniae, is a [4Fe-4S]-containing oxygen-responsive transcription regulator that anaerobically activates FNR-dependent class I promoters via an enhanced AR1 contact. Mol. Microbiol. 24:593605.
48. Gunsalus, R. P. 1992. Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J. Bacteriol. 174:70697074.
49. Hauser,, F., G. Pessi,, M. Friberg,, C. Weber,, N. Rusca,, A. Lindemann,, H. M. Fischer, and, H. Hennecke. 2007. Dissection of the Bradyrhizobium japonicum NifA+σ54 regulon, and identification of a ferredoxin gene (fdxN) for symbiotic nitrogen fixation. Mol. Genet. Genomics 278:255271.
50. Iuchi,, S.,, D. C. Cameron, and, E. C. Lin. 1989. A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli. J. Bacteriol. 171:868873.
51. Iuchi, S., and, E. C. Lin. 1988. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. USA 85:18881892.
52. Janausch,, I. G.,, I. Garcia-Moreno,, D. Lehnen,, Y. Zeuner, and, G. Unden. 2004. Phosphorylation and DNA binding of the regulator DcuR of the fumarate-responsive two-component system DcuSR of Escherichia coli. Microbiology 150:877883.
53. Jones, D. F.,, R. A. Stenzel, and, T. J. Donohue. 2005. Mutational analysis of the C-terminal domain of the Rhodobacter sphaeroides response regulator PrrA. Microbiology 151:41034110.
54. Jovanovic,, G., C. Engl, and, M. Buck. 2009. Physical, functional and conditional interactions between ArcAB and phage shock proteins upon secretin-induced stress in Escherichia coli. Mol. Microbiol. 74:1628.
55. Kang,, Y.,, K. D. Weber,, Y. Qiu,, P. J. Kiley, and, F. R. Blattner. 2005. Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J. Bacteriol. 187:11351160.
56. Karls, R. K.,, J. R. Wolf, and, T. J. Donohue. 1999. Activation of the cycA P2 promoter for the Rhodobacter sphaeroides cytochrome c2 gene by the photosynthesis response regulator. Mol. Microbiol. 34:822835.
57. Khoroshilova,, N., C. Popescu,, E. Münck,, H. Beinert, and, P. J. Kiley. 1997. Iron-sulfur cluster disassembly in the FNR protein of Escherichia coli by O2: [4Fe-4S] to [2Fe-2S] conversion with loss of biological activity. Proc. Natl. Acad. Sci. USA 94:60876092.
58. Kim,, S. K.,, J. T. Mason,, D. B. Knaff,, C. E. Bauer, and, A. T. Setterdahl. 2006. Redox properties of the Rhodobacter sphaeroides transcriptional regulatory proteins PpsR and AppA. Photosynth. Res. 89:8998.
59. Korner,, H.,, H. J. Sofia, and, W. G. Zumft. 2003. Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol. Rev. 27:559592.
60. Kraft,, B. J.,, S. Masuda,, J. Kikuchi,, V. Dragnea,, G. Tollin,, J. M. Zaleski, and, C. E. Bauer. 2003. Spectroscopic and mutational analysis of the blue-light photoreceptor AppA: a novel photocycle involving flavin stacking with an aromatic amino acid. Biochemistry 42:67266734.
61. Laguri,, C.,, M. K. Phillips-Jones, and, M. P. Williamson. 2003. Solution structure and DNA binding of the effector domain from the global regulator PrrA (RegA) from Rhodobacter sphaeroides: insights into DNA binding specificity. Nucleic Acids Res. 31:67786787.
62. Laguri,, C.,, R. A. Stenzel,, T. J. Donohue,, M. K. Phillips-Jones, and, M. P. Williamson. 2006. Activation of the global gene regulator PrrA (RegA) from Rhodobacter sphaeroides. Biochemistry 45:78727881.
63. Lambden, P. R., and, J. R. Guest. 1976. Mutants of Escherichia coli K12 unable to use fumarate as an anaerobic electron acceptor. J. Gen. Microbiol. 97:145160.
64. Lamberg, K. E.,, C. Luther,, K. D. Weber, and, P. J. Kiley. 2002. Characterization of activating region 3 from Escherichia coli FNR. J. Mol. Biol. 315:275283.
65. Lascelles, J. 1966. The accumulation of bacteriochlorophyll precursors by mutant and wild-type strains of Rhodopseudomonas spheroides. Biochem. J. 100:175183.
66. Lazazzera,, B. A.,, H. Beinert,, N. Khoroshilova,, M. C. Kennedy, and, P. J. Kiley. 1996. DNA binding and dimerization of the Fe-S-containing FNR protein from Escherichia coli are regulated by oxygen. J. Biol. Chem. 271:27622768.
67. Li,, B., H. Wing,, D. Lee,, H. C. Wu, and, S. Busby. 1998. Transcription activation by Escherichia coli FNR protein: similarities to, and differences from, the CRP paradigm. Nucleic Acids Res. 26:20752081.
68. Liu, X., and, P. De Wulf. 2004. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 279:1258812597.
69. Lloyd,, G., P. Landini, and, S. Busby. 2001. Activation and repression of transcription initiation in bacteria. Essays Biochem. 37:1731.
70. Loui, C.,, A. C. Chang, and, S. Lu. 2009. Role of the ArcAB two-component system in the resistance of Escherichia coli to reactive oxygen stress. BMC Microbiol. 9:183.
71. Mackenzie,, C.,, J. M. Eraso,, M. Choudhary,, J. H. Roh,, X. Zeng,, P. Bruscella,, A. Puskas, and, S. Kaplan. 2007. Postgenomic adventures with Rhodobacter sphaeroides. Ann. Rev. Microbiol. 61:283307.
72. Malpica, R.,, B. Franco,, C. Rodriguez,, O. Kwon, and, D. Georgellis. 2004. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc. Natl. Acad. Sci. USA 101:1331813323.
73. Mao,, L., C. Mackenzie,, J. H. Roh,, J. M. Eraso,, S. Kaplan, and, H. Resat. 2005. Combining microarray and genomic data to predict DNA binding motifs. Microbiology 151:31973213.
74. Masuda, S., and, C. Bauer. 2002. AppA Is a blue bight photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613623.
75. Masuda,, S., J. Berleman,, B. M. Hasselbring, and, C. E. Bauer. 2008. Regulation of aerobic photosystem synthesis in the purple bacterium Rhodospirillum centenum by CrtJ and AerR. Photochem. Photobiol. Sci. 7:12671272.
76. Matsubara, M., and, T. Mizuno. 2000. The SixA phospho-histidine phosphatase modulates the ArcB phosphorelay signal transduction in Escherichia coli. FEBS Lett. 470:118124.
77. Mettert, E. L., and, P. J. Kiley. 2005. ClpXP-dependent proteolysis of FNR upon loss of its O2-sensing [4Fe-4S] cluster. J. Mol. Biol. 354:220232.
78. Mettert, E. L., and, P. J. Kiley. 2007. Contributions of [4Fe-4S]-FNR and integration host factor to fnr transcriptional regulation. J. Bacteriol. 189:30363043.
79. Mettert,, E. L.,, F. W. Outten,, B. Wanta, and, P. J. Kiley. 2008. The impact of O2 on the Fe-S cluster biogenesis requirements of Escherichia coli FNR. J. Mol. Biol. 384:798811.
80. Meyer,, T. E., and, T. J. Donohue. 1995. Cytochromes, iron-sulfur and copper proteins mediating electron transfer from the cytochrome bc1 complex to photosynthetic reaction center complexes, P. 725–745. In R. E. Blankenship,, M. T. Madigan, and B. C. E (ed.), Anoxygenic Photosynthetic Bacteria: Advances in Photosynthesis. Kluwer Academic Publishers, Dordrecht, Netherlands.
81. Mika, F., and, R. Hengge. 2005. A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. Genes Dev. 19:27702781.
82. Moore, L. J., and, P. J. Kiley. 2001. Characterization of the dimerization domain in the FNR transcription factor. J. Biol. Chem. 276:4574445750.
83. Moore, L. J.,, E. L. Mettert, and, P. J. Kiley. 2006. Regulation of FNR dimerization by subunit charge repulsion. J. Biol. Chem. 281:3326833275.
84. Moskvin, O. V.,, S. Kaplan,, M. A. Gilles-Gonzalez, and, M. Gomelsky. 2007. Novel heme-based oxygen sensor with a revealing evolutionary history. J. Biol. Chem. 282:2874028748.
85. Nakano,, M. M.,, P. Zuber,, P. Glaser,, A. Danchin, and, F. M. Hulett. 1996. Two-component regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis. J. Bacteriol. 178:37963802.
86. Oh, J.-I., I.-J. Ko, and, S. Kaplan. 2001. The default state of the membrane-localized histidine kinase PrrB of Rhodobacter sphaeroides 2.4.1 is in the kinase-positive mode. J. Bacteriol. 183:68076814.
87. Oh, J.-I., I.-J. Ko, and, S. Kaplan. 2004. Reconstitution of the Rhodobacter sphaeroides cbb3-PrrBA signal transduction pathway in vitro. Biochemistry 43:79157923.
88. Oh, J.-I., and, S. Kaplan. 2000. Redox signaling: globalization of gene expression. EMBO J. 19:42374247.
89. Partridge,, J. D.,, C. Scott,, Y. Tang,, R. K. Poole, and, J. Green. 2006. Escherichia coli transcriptome dynamics during the transition from anaerobic to aerobic conditions. J. Biol. Chem. 281:2780627815.
90. Partridge,, J. D.,, G. Sanguinetti,, D. P. Dibden,, R. E. Roberts,, R. K. Poole, and, J. Green. 2007. Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components. J. Biol. Chem. 282:1123011237.
91. Patschkowski, T., A. Schluter, and, U. B. Priefer. 1996. Rhizobium leguminosarum bv. viciae contains a second fnr/fixK-like gene and an unusual fixL homologue. Mol. Microbiol. 21:267280.
92. Pena-Sandoval, G. R.,, O. Kwon, and, D. Georgellis. 2005. Requirement of the receiver and phosphotransfer domains of ArcB for efficient dephosphorylation of phosphorylated ArcA in vivo. J. Bacteriol. 187:32673272.
93. Pitcher, R. S., and, N. J. Watmough. 2004. The bacterial cytochrome cbb3 oxidases. Biochim. Biophys. Acta 1655:388399.
94. Popescu,, C. V.,, D. M. Bates,, H. Beinert,, E. Münck, and, P. J. Kiley. 1998. Mössbauer spectroscopy as a tool for the study of activation/inactivation of the transcription regulator FNR in whole cells of Escherichia coli. Proc. Natl. Acad. Sci. USA 95:1343113435.
95. Potter,, C. A.,, A. Ward,, C. Laguri,, M. P. Williamson,, P. J., F. Henderson, and, M. K. Phillips-Jones. 2002. Expression, purification and characterisation of full-length histidine protein kinase RegB from Rhodobacter sphaeroides. J. Mol. Biol. 320:201213.
96. Ranson-Olson,, B.,, D. F. Jones,, T. J. Donohue, and, J. H. Zeilstra-Ryalls. 2006. In vitro and in vivo analysis of the role of PrrA in Rhodobacter sphaeroides 2.4.1 hemA gene expression. J. Bacteriol. 188:32083218.
97. Ravcheev,, D. A.,, A. V. Gerasimova,, A. A. Mironov, and, M. S. Gelfand. 2007. Comparative genomic analysis of regulation of anaerobic respiration in ten genomes from three families of gamma-proteobacteria (Enterobacteriaceae, Pasteurellaceae, Vibrionaceae). BMC Genomics 8:54.
98. Reents,, H., I. Gruner,, U. Harmening,, L. H. Bottger,, G. Layer,, P. Heathcote,, A. X. Trautwein,, D. Jahn, and, E. Hartig. 2006. Bacillus subtilis Fnr senses oxygen via a [4Fe-4S] cluster coordinated by three cysteine residues without change in the oligomeric state. Mol. Microbiol. 60:14321445.
99. Reinhart, F.,, A. Huber,, R. Thiele, and, G. Unden. 2010. Response of the oxygen sensor NreB to air in vivo: Fe-S containing and apoNreB in aerobically and anaerobically growing Staphylococcus carnosus. J. Bacteriol. 192:8693.
100. Saffarini, D. A., and, K. H. Nealson. 1993. Sequence and genetic characterization of etrA, an fnr analog that regulates anaerobic respiration in Shewanella putrefaciens MR-1. J. Bacteriol. 175:79387944.
101. Saffarini, D. A.,, R. Schultz, and, A. Beliaev. 2003. Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J. Bacteriol. 185:36683671.
102. Salmon,, K.,, S. P. Hung,, K. Mekjian,, P. Baldi,, G. W. Hatfield, and, R. P. Gunsalus. 2003. Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J. Biol. Chem. 278:2983729855.
103. Salmon,, K. A.,, S. P. Hung,, N. R. Steffen,, R. Krupp,, P. Baldi,, G. W. Hatfield, and, R. P. Gunsalus. 2005. Global gene expression profiling in Escherichia coli K12: effects of oxygen availability and ArcA. J. Biol. Chem. 280:1508415096.
104. Schluter,, A., S. Ruberg,, M. Kramer,, S. Weidner, and, U. B. Priefer. 1995. A homolog of the Rhizobium meliloti nitrogen fixation gene fixN is involved in the production of a microaerobically induced oxidase activity in the phytopathogenic bacterium Agrobacterium tumefaciens. Mol. Gen. Genet. 247:206215.
105. Schreiber,, K., R. Krieger,, B. Benkert,, M. Eschbach,, H. Arai,, M. Schobert, and, D. Jahn. 2007. The anaerobic regulatory network required for Pseudomonas aeruginosa nitrate respiration. J. Bacteriol. 189:43104314.
106. Sciotti, M. A.,, A. Chanfon,, H. Hennecke, and, H. M. Fischer. 2003. Disparate oxygen responsiveness of two regulatory cascades that control expression of symbiotic genes in Bradyrhizobium japonicum. J. Bacteriol. 185:56395642.
107. Sganga, M. W., and, C. E. Bauer. 1992. Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus. Cell 68:945954.
108. Smart, J. L., and, C. E. Bauer. 2006. Tetrapyrrole biosynthesis in Rhodobacter capsulatus is transcriptionally regulated by the heme-binding regulatory protein, HbrL. J. Bacteriol. 188:15671576.
109. Sousa, E. H.,, G. Gonzalez, and, M. A. Gilles-Gonzalez. 2005. Oxygen blocks the reaction of the FixL-FixJ complex with ATP but does not influence binding of FixJ or ATP to FixL. Biochemistry 44:1535915365.
110. Sousa,, E. H.,, J. R. Tuckerman,, G. Gonzalez, and, M. A. Gilles-Gonzalez. 2007. A memory of oxygen binding explains the dose response of the heme-based sensor FixL. Biochemistry 46:62496257.
111. Spiro, S. 1994. The FNR family of transcriptional regulators. Antonie Van Leeuwenhoek 66:2336.
112. Spiro, S., and, J. R. Guest. 1988. Inactivation of the FNR protein of Escherichia coli by targeted mutagenesis in the N-terminal region. Mol. Microbiol. 2:701707.
113. Spiro,, S.,, K. L. Gaston,, A. I. Bell,, R. E. Roberts,, S. J. Busby, and, J. R. Guest. 1990. Interconversion of the DNA-binding specificities of two related transcription regulators, CRP and FNR. Mol. Microbiol. 4:18311838.
114. Stewart, V. 2003. Biochemical Society Special Lecture. Nitrate- and nitrite-responsive sensors NarX and NarQ of proteobacteria. Biochem. Soc. Trans. 31:110.
115. Sturgis, J. N., and, R. A. Niederman. 2008. Atomic force microscopy reveals multiple patterns of antenna organization in purple bacteria: implications for energy transduction mechanisms and membrane modeling. Photosynth. Res. 95:269278.
116. Sutton,, V. R.,, A. Stubna,, T. Patschkowski,, E. Münck,, H. Beinert, and, P. J. Kiley. 2004a. Superoxide destroys the [2Fe-2S]2+ cluster of FNR from Escherichia coli. Biochemistry 43:791798.
117. Sutton,, V. R.,, E. L. Mettert,, H. Beinert, and, P. J. Kiley. 2004b. Kinetic analysis of the oxidative conversion of the [4Fe-4S]2+ cluster of FNR to a [2Fe-2S]2+ cluster. J. Bacteriol. 186:80188025.
118. Swem,, L. R.,, B. J. Kraft,, D. L. Swem,, A. T. Setterdahl,, S. Masuda,, D. B. Knaff,, J. M. Zaleski, and, C. E. Bauer. 2003. Signal transduction by the global regulator RegB is mediated by a redox-active cysteine. EMBO J. 22:46994708.
119. Swem,, L. R.,, S. Elsen,, T. H. Bird,, D. L. Swem,, H. G. Koch,, H. Myllykallio,, F. Daldal, and, C. E. Bauer. 2001. The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus. J. Mol. Biol. 309:121138.
120. Swem, L. R.,, X. Gong,, C.-A. Yu, and, C. E. Bauer. 2006. Identification of a ubiquinone-binding site that affects autophosphorylation of the sensor kinase RegB. J. Biol. Chem. 281:67686775.
121. Tomiki, T., and, N. Saitou. 2004. Phylogenetic analysis of proteins associated in the four major energy metabolism systems: photosynthesis, aerobic respiration, denitrification, and sulfur respiration. J. Mol. Evol. 59:158176.
122. Tolla, D. A., and, M. A. Savageau. 2010. Regulation of aerobic-to-anaerobic transitions by the FNR cycle in Escherichia coli. J. Mol. Biol. 397:893905.
123. Tuckerman,, J. R.,, G. Gonzalez,, E. H. Sousa,, X. Wan,, J. A. Saito,, M. Alam, and, M. A. Gilles-Gonzalez. 2009. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48:97649774.
124. Unden, G., and, J. Bongaerts. 1997. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim. Biophys. Acta 1320:217234.
125. Vichivanives,, P.,, T. H. Bird,, C. E. Bauer, and, F. R. Tabita. 2000. Multiple regulators and their interactions in vivo and in vitro with the cbb regulons of Rhodobacter capsulatus. J. Mol. Biol. 300:10791099.
126. Vollack, K. U.,, E. Hartig,, H. Korner, and, W. G. Zumft. 1999. Multiple transcription factors of the FNR family in denitrifying Pseudomonas stutzeri: characterization of four fnr-like genes, regulatory responses and cognate metabolic processes. Mol. Microbiol. 31:16811694.
127. Weber, K. D.,, O. D. Vincent, and, P. J. Kiley. 2005. Additional determinants within Escherichia coli FNR activating region 1 and RNA polymerase alpha subunit required for transcription activation. J. Bacteriol. 187:17241731.
128. Whitehead,, R. N.,, T. W. Overton,, L. A. Snyder,, S. J. McGowan,, H. Smith,, J. A. Cole, and, N. J. Saunders. 2007. The small FNR regulon of Neisseria gonorrhoeae: comparison with the larger Escherichia coli FNR regulon and interaction with the NarQNarP regulon. BMC Genomics 8:35.
129. Willett,, J.,, J. L. Smart, and, C. E. Bauer. 2007. RegA control of bacteriochlorophyll and carotenoid synthesis in Rhodobacter capsulatus. J. Bacteriol. 189:77657773.
130. Winteler, H. V., and, D. Haas. 1996. The homologous regulators ANR of Pseudomonas aeruginosa and FNR of Escherichia coli have overlapping but distinct specificities for anaerobically inducible promoters. Microbiology 142:685693.
131. Wu,, G., S. Hill,, M. J. Kelly,, G. Sawers, and, R. K. Poole. 1997. The cydR gene product, required for regulation of cytochrome bd expression in the obligate aerobe Azotobacter vinelandii, is an Fnr-like protein. Microbiology 143:21972207.
132. Wu, J., and, C. E. Bauer. 2008. RegB/RegA, a global redox-responding two-component system. Adv. Exp. Med. Biol. 631:131148.
133. Zeilstra-Ryalls,, J., M. Gomelsky,, J. M. Eraso,, A. Yeliseev,, J. O’Gara, and, S. Kaplan. 1998. Control of photosystem formation in Rhodobacter sphaeroides. J. Bacteriol. 180:28012809.
134. Zeilstra-Ryalls,, J. H.,, K. Gabbert,, N. J. Mouncey,, S. Kaplan, and, R. G. Kranz. 1997. Analysis of the fnrL gene and its function in Rhodobacter capsulatus. J. Bacteriol. 179:72647273.
135. Zeilstra-Ryalls, J. H., and, S. Kaplan. 2004. Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm. Cell. Mol. Life Sci. 61:417436.
136. Zigha, A.,, E. Rosenfeld,, P. Schmitt, and, C. Duport. 2007. The redox regulator Fnr is required for fermentative growth and enterotoxin synthesis in Bacillus cereus F4430/73. J. Bacteriol. 189:28132824.
137. Zumft, W. G., and, P. M. Kroneck. 2007. Respiratory transformation of nitrous oxide (N2O) to dinitrogen by Bacteria and Archaea. Adv. Microb. Physiol. 52:107227.


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Table 1.

Global transcriptional regulators of bacterial responses to O deprivation

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11

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