Crp-dependent cytochrome bd oxidase confers nitrite resistance to shewanella oneidensis

Environmental Microbiology

Volumn 15, Issue 8, 2013, Pages 2198-2212

  Fu, Huihui ^a   Chen, Haijiang ^a   Wang, Jixuan ^a   Zhou, Guangqi ^a   Zhang, Haiyan ^a,b   Zhang, Lili ^b   Gao, Haichun ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b Tarim University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

SHEWANELLA ONEIDENSIS;

EID: 84881257026     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12091     Document Type: Article

References (60)

1. Abramson, J., Riistama, S., Larsson, G., Jasaitis, A., Svensson-Ek, M., Laakkonen, L., etal. (2000) The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat Struct Mol Biol 7: 910-917.
2. Alexeyev, M.F., and Shokolenko, I.N. (1995) Mini-Tn10 transposon derivatives for insertion mutagenesis and gene delivery into the chromosome of Gram-negative bacteria. Gene 160: 59-62.
3. Alvarez, A.F., Malpica, R., Contreras, M., Escamilla, E., and Georgellis, D. (2010) Cytochrome d but not cytochrome o rescues the toluidine blue growth sensitivity of arc mutants of Escherichia coli. J Bacteriol 192: 391-399.
4. Blatny, J.M., Brautaset, T., Winther-Larsen, H.C., Haugan, K., and Valla, S. (1997) Construction and use of a versatile set of broad-host-range cloning and expression vectors based on the RK2 replicon. Appl Environ Microbiol 63: 370-379.
5. Borisov, V.B., Forte, E., Sarti, P., Brunori, M., Konstantinov, A.A., and Giuffrè, A. (2007) Redox control of fast ligand dissociation from Escherichia coli cytochrome bd. Biochem Biophys Res Commun 355: 97-102.
6. Borisov, V.B., Gennis, R.B., Hemp, J., and Verkhovsky, M.I. (2011) The cytochrome bd respiratory oxygen reductases. Biochim Biophys Acta 1807: 1398-1413.
7. Calhoun, M.W., Hill, J.J., Lemieux, L.J., Ingledew, W.J., Alben, J.O., and Gennis, R.B. (1993) Site-directed mutants of the cytochrome bo ubiquinol oxidase of Escherichia coli: amino acid substitutions for two histidines that are putative CuB ligands. Biochemistry 32: 11524-11529.
8. Charania, M., Brockman, K., Zhang, Y., Banerjee, A., Pinchuk, G., Fredrickson, J., etal. (2009) Involvement of a membrane-bound class III adenylate cyclase in regulation of anaerobic respiration in Shewanella oneidensis MR-1. J Bacteriol 191: 4298-4306.
9. Cotter, P.A., Melville, S.B., Albrecht, J.A., and Gunsalus, R.P. (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.
10. Cruz-Garcia, C., Murray, A.E., Klappenbach, J.A., Stewart, V., and Tiedje, J.M. (2007) Respiratory nitrate ammonification by Shewanella oneidensis MR-1. J Bacteriol 189: 656-662.
11. Cruz-Garcia, C., Murray, A., Rodrigues, J., Gralnick, J., McCue, L., Romine, M., etal. (2011) Fnr (EtrA) acts as a fine-tuning regulator of anaerobic metabolism in Shewanella oneidensis MR-1. BMC Microbiol 11: 64.
12. Das, S., Noe, J.C., Paik, S., and Kitten, T. (2005) An improved arbitrary primed PCR method for rapid characterization of transposon insertion sites. J Microbiol Methods 63: 89-94.
13. Dong, Y., Wang, J., Fu, H., Zhou, G., Shi, M., and Gao, H. (2012) A Crp-dependent two-component system regulates nitrate and nitrite respiration in Shewanella oneidensis. PLoS ONE 7: e51643.
14. Ford, P.C. (2010) Reactions of NO and nitrite with heme models and proteins. Inorg Chem 49: 6226-6239.
15. Fredrickson, J.K., Romine, M.F., Beliaev, A.S., Auchtung, J.M., Driscoll, M.E., Gardner, T.S., etal. (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6: 592-603.
16. Gao, H., Wang, X., Yang, Z., Palzkill, T., and Zhou, J. (2008a) Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses. BMC Genomics 9: 42.
17. Gao, H., Pattison, D., Yan, T., Klingeman, D.M., Wang, X., Petrosino, J., etal. (2008b) Generation and validation of a Shewanella oneidensis MR-1 clone set for protein expression and phage display. PLoS ONE 3: e2983.
18. Gao, H., Yang, Z.K., Barua, S., Reed, S.B., Romine, M.F., Nealson, K.H., etal. (2009) Reduction of nitrate in Shewanella oneidensis depends on atypical NAP and NRF systems with NapB as a preferred electron transport protein from CymA to NapA. ISME J 3: 966-976.
19. Gao, H., Wang, X., Yang, Z.K., Chen, J., Liang, Y., Chen, H., etal. (2010a) Physiological roles of ArcA, Crp, and EtrA and their interactive control on aerobic and anaerobic respiration in Shewanella oneidensis. PLoS ONE 5: e15295.
20. Gao, H., Barua, S., Liang, Y., Wu, L., Dong, Y., Reed, S., etal. (2010b) Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration. Microb Biotechnol 3: 455-466.
21. Giuffrè, A., Borisov, V.B., Mastronicola, D., Sarti, P., and Forte, E. (2012) Cytochrome bd oxidase and nitric oxide: from reaction mechanisms to bacterial physiology. FEBS Lett 586: 622-629.
22. Gladwin, M.T., Grubina, R., and Doyle, M.P. (2008) The new chemical biology of nitrite reactions with hemoglobin: R-state catalysis, oxidative denitrosylation, and nitrite reductase/anhydrase. Acc Chem Res 42: 157-167.
23. Govantes, F., Orjalo, A.V., and 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.
24. Gralnick, J.A., Brown, C.T., and Newman, D.K. (2005) Anaerobic regulation by an atypical Arc system in Shewanella oneidensis. Mol Microbiol 56: 1347-1357.
25. Hall, B. (1999) Transposable elements as activators of cryptic genes in E.coli. Genetica 107: 181-187.
26. Hassani, B.K., Steunou, A.-S., Liotenberg, S., Reiss-Husson, F., Astier, C., and Ouchane, S. (2010) Adaptation to oxygen. J Biol Chem 285: 19891-19899.
27. He, C., Ogata, H., and Knipp, M. (2010) Formation of the complex of nitrite with the ferriheme b β-barrel proteins nitrophorin 4 and nitrophorin 7. Biochemistry 49: 5841-5851.
28. Hyduke, D.R., Jarboe, L.R., Tran, L.M., Chou, K.J.Y., and Liao, J.C. (2007) Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli. Proc Natl Acad Sci USA 104: 8484-8489.
29. 2 fixation. J Bacteriol 178: 5989-5994.
30. Kovach, M.E., Elzer, P.H., Steven Hill, D., Robertson, G.T., Farris, M.A., Roop Ii, R.M., and Peterson, K.M. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
31. Lassak, J., Henche, A.-L., Binnenkade, L., and Thormann, K.M. (2010) ArcS, the cognate sensor kinase in an atypical arc system of Shewanella oneidensis MR-1. Appl Environ Microbiol 76: 3263-3274.
32. Liang, Y., Gao, H., Chen, J., Dong, Y., Wu, L., He, Z., etal. (2010) Pellicle formation in Shewanella oneidensis. BMC Microbiol 10: 291.
33. Lundberg, J.O., Weitzberg, E., Cole, J.A., and Benjamin, N. (2004) Nitrate, bacteria and human health. Nat Rev Microbiol 2: 593-602.
34. Lundberg, J.O., Weitzberg, E., and Gladwin, M.T. (2008) The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7: 156-167.
35. Maier, T.M., and Myers, C.R. (2001) Isolation and characterization of a Shewanella putrefaciens MR-1 electron transport regulator etrA mutant: reassessment of the role of EtrA. J Bacteriol 183: 4918-4926.
36. Marx, C.J., and Lidstrom, M.E. (2002) Broad-host-range cre-lox system for antibiotic marker recycling in Gram-negative bacteria. Biotechniques 33: 1062-1067.
37. Mason, M.G., Shepherd, M., Nicholls, P., Dobbin, P.S., Dodsworth, K.S., Poole, R.K., and Cooper, C.E. (2009) Cytochrome bd confers nitric oxide resistance to Escherichia coli. Nat Chem Biol 5: 94-96.
38. Newton, G., and Gennis, R.B. (1991) In vivo assembly of the cytochrome d terminal oxidase complex of Escherichia coli from genes encoding the two subunits expressed on separate plasmids. Biochim Biophys Acta 1089: 8-12.
39. Pereira, M.M., Santana, M., and Teixeira, M. (2001) A novel scenario for the evolution of haem-copper oxygen reductases. Biochim Biophys Acta 1505: 185-208.
40. Pinchuk, G.E., Rodionov, D.A., Yang, C., Li, X., Osterman, A.L., Dervyn, E., etal. (2009) Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization. Proc Natl Acad Sci USA 106: 2874-2879.
41. Poole, R.K. (2005) Nitric oxide and nitrosative stress tolerance in bacteria. Biochem Soc Trans 33: 176-180.
42. Price, M.S., Chao, L.Y., and Marletta, M.A. (2007) Shewanella oneidensis MR-1 H-NOX regulation of a histidine kinase by nitric oxide. Biochemistry 46: 13677-13683.
43. Reddy, D., Lancaster, J., and Cornforth, D. (1983) Nitrite inhibition of Clostridium botulinum: electron spin resonance detection of iron-nitric oxide complexes. Science 221: 769-770.
44. Reese, M.G. (2001) Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem 26: 51-56.
45. Richardson, A.R., Payne, E.C., Younger, N., Karlinsey, J.E., Thomas, V.C., Becker, L.A., etal. (2011) Multiple targets of nitric oxide in the tricarboxylic acid cycle of Salmonella enterica Serovar Typhimurium. Cell Host Microbe 10: 33-43.
46. Saffarini, D., Schultz, R., and Beliaev, A. (2003) Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J Bacteriol 185: 3668-3671.
47. Sarti, P., Giuffrè, A., Barone, M.C., Forte, E., Mastronicola, D., and Brunori, M. (2003) Nitric oxide and cytochrome oxidase: reaction mechanisms from the enzyme to the cell. Free Radic Biol Med 34: 509-520.
48. Schwalb, C., Chapman, S.K., and Reid, G.A. (2003) The tetraheme cytochrome CymA is required for anaerobic respiration with dimethyl sulfoxide and nitrite in Shewanella oneidensis. Biochemistry 42: 9491-9497.
49. Shroff, N.P., Charania, M.A., and Saffarini, D.A. (2010) ArcB1, a homolog of Escherichia coli ArcB, regulates dimethyl sulfoxide reduction in Shewanella oneidensis MR-1. J Bacteriol 192: 3227-3230.
50. Sindelar, J.J., and Milkowski, A.L. (2012) Human safety controversies surrounding nitrate and nitrite in the diet. Nitric Oxide 26: 259-266.
51. Tseng, C.P., Albrecht, J., and Gunsalus, R.P. (1996) 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. J Bacteriol 178: 1094-1098.
52. Wikström, M., and Verkhovsky, M.I. (2007) Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases. Biochim Biophys Acta 1767: 1200-1214.
53. Wong, S.M., and Mekalanos, J.J. (2000) Genetic footprinting with mariner-based transposition in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97: 10191-10196.
54. Wu, L., Wang, J., Tang, P., Chen, H., and Gao, H. (2011) Genetic and molecular characterization of flagellar assembly in Shewanella oneidensis. PLoS ONE 6: e21479.
55. Yan, X., Yu, H.-J., Hong, Q., and Li, S. (2008) Cre/lox system and PCR-based genome engineering in Bacillus subtilis. Appl Environ Microbiol 74: 5556-5562.
56. Yin, J., and Gao, H. (2011) Stress responses of Shewanella. Int J Microbiol. Art. No. 863623.
57. Yoshikawa, S., Muramoto, K., and Shinzawa-Itoh, K. (2011) Proton-pumping mechanism of cytochrome c oxidase. Annu Rev Biophys 40: 205-223.
58. Yuan, J., Wei, B., Shi, M., and Gao, H. (2011) Functional assessment of EnvZ/OmpR two-component system in Shewanella oneidensis. PLoS ONE 6: e23701.
59. Yuan, J., Wei, B., Lipton, M.S., and Gao, H. (2012) Impact of ArcA loss in Shewanella oneidensis revealed by comparative proteomics under aerobic and anaerobic conditions. Proteomics 12: 1957-1969.
60. Zomer, A.L., Buist, G., Larsen, R., Kok, J., and Kuipers, O.P. (2007) Time-resolved determination of the CcpA regulon of Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 189: 1366-1381.