The alternative oxidase (AOX) gene in Vibrio fischeri is controlled by NsrR and upregulated in response to nitric oxide

Molecular Microbiology

Volumn 77, Issue 1, 2010, Pages 44-55

  Dunn, Anne K ^a   Karr, Elizabeth A ^a   Wang, Yanling ^b   Batton, Aaron R ^a   Ruby, Edward G ^b   Stabb, Eric V ^c  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEROBIC RESPIRATION CONTROL PROTEIN A; ALTERNATIVE OXIDASE; BACTERIAL PROTEIN; NITRIC OXIDE; OXIDOREDUCTASE; PROTEIN NSRR; UNCLASSIFIED DRUG; BACTERIAL DNA; DUROQUINOL OXIDASE; MITOCHONDRIAL PROTEIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BIOINFORMATICS; GENE CONTROL; GENE EXPRESSION REGULATION; NONHUMAN; OXYGEN CONSUMPTION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VIBRIO FISCHERI; ALIIVIBRIO FISCHERI; BINDING SITE; CHEMISTRY; DNA RESPONSIVE ELEMENT; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REPORTER GENE; TOXICITY;

BACTERIA (MICROORGANISMS); EUKARYOTA; VIBRIO FISCHERI;

ALIIVIBRIO FISCHERI; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; DNA, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REPORTER; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; OXIDOREDUCTASES; OXYGEN CONSUMPTION; PLANT PROTEINS; POLYMERASE CHAIN REACTION; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS;

EID: 77954022304     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07194.x     Document Type: Article

References (57)

1. Akhter, S., McDade, H.C., Gorlach, J.M., Heinrich, G., Cox, G.M. Perfect, J.R. (2003) Role of alternative oxidase gene in pathogenesis of Cryptococcus neoformans. Infect Immun 71 : 5794 5802.
2. Avissar, Y.J. Beale, S.I. (1989) Identification of the enzymatic basis for delta-aminolevulinic acid auxotrophy in a hemA mutant of Escherichia coli. J Bacteriol 171 : 2919 2924.
3. Berthold, D.A., Voevodskaya, N., Stenmark, P., Graslund, A. Nordlund, P. (2002) EPR studies of the mitochondrial alternative oxidase. Evidence for a diiron carboxylate center. J Biol Chem 277 : 43608 43614.
4. Bodenmiller, D.M. Spiro, S. (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J Bacteriol 188 : 874 881.
5. Boettcher, K.J. Ruby, E.G. (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol 172 : 3701 3706.
6. Borisov, V.B., Forte, E., Konstantinov, A.A., Poole, R.K., Sarti, P. Giuffre, A. (2004) Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide. FEBS Lett 576 : 201 204.
7. Bose, J.L., Rosenberg, C.S. Stabb, E.V. (2008) Effects of luxCDABEG induction in Vibrio fischeri: enhancement of symbiotic colonization and conditional attenuation of growth in culture. Arch Microbiol 190 : 169 183.
8. Castro-Guerrero, N.A., Krab, K. Moreno-Sanchez, R. (2004) The alternative respiratory pathway of euglena mitochondria. J Bioenerg Biomembr 36 : 459 469.
9. Chaudhuri, M., Ajayi, W. Hill, G.C. (1998) Biochemical and molecular properties of the Trypanosoma brucei alternative oxidase. Mol Biochem Parasitol 95 : 53 68.
10. Choi, P.S., Naal, Z., Moore, C., Casado-Rivera, E., Abruna, H.D., Helmann, J.D. Shapleigh, J.P. (2006) Assessing the impact of denitrifier-produced nitric oxide on other bacteria. Appl Environ Microbiol 72 : 2200 2205.
11. Clarkson, A.B., Jr., Bienen, E.J., Pollakis, G. Grady, R.W. (1989) Respiration of bloodstream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase. J Biol Chem 264 : 17770 17776.
12. Cosseau, C. Batut, J. (2004) Genomics of the ccoNOQP-encoded cbb3 oxidase complex in bacteria. Arch Microbiol 181 : 89 96.
13. Cotter, P.A., Chepuri, V., Gennis, R.B. Gunsalus, R.P. (1990) Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J Bacteriol 172 : 6333 6338.
14. Czarna, M. Jarmuszkiewicz, W. (2005) Activation of alternative oxidase and uncoupling protein lowers hydrogen peroxide formation in amoeba Acanthamoeba castellanii mitochondria. FEBS Lett 579 : 3136 3140.
15. Davidson, S.K., Koropatnick, T.A., Kossmehl, R., Sycuro, L. McFall-Ngai, M.J. (2004) NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6 : 1139 1151.
16. Delgado, M.J., Bedmar, E.J. Downie, J.A. (1998) Genes involved in the formation and assembly of rhizobial cytochromes and their role in symbiotic nitrogen fixation. Adv Microb Physiol 40 : 191 231.
17. Dunn, A.K. Stabb, E.V. (2008) The twin arginine translocation system contributes to symbiotic colonization of Euprymna scolopes by Vibrio fischeri. FEMS Microbiol Lett 279 : 251 258.
18. Dunn, A.K., Martin, M.O. Stabb, E.V. (2005) Characterization of pES213, a small mobilizable plasmid from Vibrio fischeri. Plasmid 54 : 114 134.
19. Dunn, A.K., Millikan, D.S., Adin, D.M., Bose, J.L. Stabb, E.V. (2006) New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Appl Environ Microbiol 72 : 802 810.
20. Gupta, K.J., Zabalza, A. van Dongen, J.T. (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137 : 383 391.
21. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166 : 557 580.
22. Hansen, L.D., Church, J.N., Matheson, S., McCarlie, V.W., Thygerson, T., Criddle, R.S. Smith, B.N. (2002) Kinetics of plant growth and metabolism. Thermochim Acta 388 : 415 425.
23. Hori, H., Tsubaki, M., Mogi, T. Anraku, Y. (1996) EPR study of NO complex of bd-type ubiquinol oxidase from Escherichia coli. J Biol Chem 271 : 9254 9258.
24. Imlay, J.A. (1995) A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli. J Biol Chem 270 : 19767 19777.
25. Isabella, V.M., Lapek, J.D., Jr., Kennedy, E.M. Clark, V.L. (2009) Functional analysis of NsrR, a nitric oxide-sensing Rrf2 repressor in Neisseria gonorrhoeae. Mol Microbiol 71 : 227 239.
26. Kelly, M.J., Poole, R.K., Yates, M.G. Kennedy, C. (1990) Cloning and mutagenesis of genes encoding the cytochrome bd terminal oxidase complex in Azotobacter vinelandii: mutants deficient in the cytochrome d complex are unable to fix nitrogen in air. J Bacteriol 172 : 6010 6019.
27. Kumar, A.M. Soll, D. (1992) Arabidopsis alternative oxidase sustains Escherichia coli respiration. Proc Natl Acad Sci USA 89 : 10842 10846.
28. Lambers, H. (1982) Cyanide-resistant respiration: a non-phosphorylating electron transport pathway acting as an energy over-flow. Physiol Plant 55 : 478 485.
29. Mason, M.G., Shepherd, M., Nicholls, P., Dobbin, P.S., Dodsworth, K.S., Poole, R.K. Cooper, C.E. (2009) Cytochrome bd confers nitric oxide resistance to Escherichia coli. Nat Chem Biol 5 : 94 96.
30. McDonald, A. Vanlerberghe, G. (2004) Branched mitochondrial electron transport in the Animalia: presence of alternative oxidase in several animal phyla. IUBMB Life 56 : 333 341.
31. McDonald, A.E. Vanlerberghe, G.C. (2005) Alternative oxidase and plastoquinol terminal oxidase in marine prokaryotes of the Sargasso Sea. Gene 349 : 15 24.
32. Meeuse, B.J.D. (1975) Thermogenic respiration in aroids. Annu Rev Plant Physiol 26 : 117 126.
33. Millar, A.H. Day, D.A. (1996) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 398 : 155 158.
34. Millar, H., Considine, M.J., Day, D.A. Whelan, J. (2001) Unraveling the role of mitochondria during oxidative stress in plants. IUBMB Life 51 : 201 205.
35. Miller, J.H. (1992) A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria.
36. Partridge, J.D., Bodenmiller, D.M., Humphrys, M.S. Spiro, S. (2009) NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility. Mol Microbiol 73 : 680 694.
37. Preisig, O., Zufferey, R., Thony-Meyer, L., Appleby, C.A. Hennecke, H. (1996) A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178 : 1532 1538.
38. Purvis, A.C. (1997) Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol Plant 100 : 165 170.
39. Rasmusson, A.G., Fernie, A.R. van Dongen, J.T. (2009) Alternative oxidase: a defence against metabolic fluctuations? Physiol Plant 137 : 371 382.
40. Rodionov, D.A., Dubchak, I.L., Arkin, A.P., Alm, E.J. Gelfand, M.S. (2005) Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput Biol 1 : e55.
41. Ruby, E.G., Urbanowski, M., Campbell, J., Dunn, A., Faini, M., Gunsalus, R., et al. (2005) Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA 102 : 3004 3009.
42. Stabb, E.V. Ruby, E.G. (2002) RP4-based plasmids for conjugation between Escherichia coli and members of the Vibrionaceae. Methods Enzymol 358 : 413 426.
43. Stabb, E.V., Reich, K.A. Ruby, E.G. (2001) Vibrio fischeri genes hvnA and hvnB encode secreted NAD(+)-glycohydrolases. J Bacteriol 183 : 309 317.
44. Stenmark, P. Nordlund, P. (2003) A prokaryotic alternative oxidase present in the bacterium Novosphingobium aromaticivorans. FEBS Lett 552 : 189 192.
45. Stevanin, T.M., Ioannidis, N., Mills, C.E., Kim, S.O., Hughes, M.N. Poole, R.K. (2000) Flavohemoglobin Hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo′ or bd, from nitric oxide. J Biol Chem 275 : 35868 35875.
46. Thony-Meyer, L., Beck, C., Preisig, O. Hennecke, H. (1994) The ccoNOQP gene cluster codes for a cb-type cytochrome oxidase that functions in aerobic respiration of Rhodobacter capsulatus. Mol Microbiol 14 : 705 716.
47. Tokuda, H. Unemoto, T. (1984) Na+ is translocated at NADH:quinone oxidoreductase segment in the respiratory chain of Vibrio alginolyticus. J Biol Chem 259 : 7785 7790.
48. Tucker, N.P., Hicks, M.G., Clarke, T.A., Crack, J.C., Chandra, G., Brun, N.E.Le, et al. (2008) The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. PloS ONE 3 : e3623.
49. Tucker, N.P., Le Brun, N.E., Dixon, R. Hutchings, M.I. (2010) There's NO stopping NsrR, a global regulator of the bacterial NO stress response. Trends Microbiol 18 : 149 156.
50. Umbach, A.L. Siedow, J.N. (2000) The cyanide-resistant alternative oxidases from the fungi Pichia stipitis and Neurospora crassa are monomeric and lack regulatory features of the plant enzyme. Arch Biochem Biophys 378 : 234 245.
51. Vanlerberghe, G.C. McIntosh, L. (1997) ALTERNATIVE OXIDASE: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 48 : 703 734.
52. Vanlerberghe, G.C., Cvetkovska, M. Wang, J. (2009) Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol Plant 137 : 392 406.
53. Visick, K.L. Ruby, E.G. (2006) Vibrio fischeri and its host: it takes two to tango. Curr Opin Microbiol 9 : 632 638.
54. Wagner, A.M. Moore, A.L. (1997) Structure and function of the plant alternative oxidase: its putative role in the oxygen defence mechanism. Biosci Rep 17 : 319 333.
55. Wang, Y., Dufour, Y.S., Carlson, H.K., Marletta, M.A. Ruby, E.G. (2010) H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri. Proc Natl Acad Sci USA (in press).
56. Yu, H., Sato, E.F., Nagata, K., Nishikawa, M., Kashiba, M., Arakawa, T., et al. (1997) Oxygen-dependent regulation of the respiration and growth of Escherichia coli by nitric oxide. FEBS Lett 409 : 161 165.
57. Yukl, E.T., Elbaz, M.A., Nakano, M.M. Moenne-Loccoz, P. (2008) Transcription Factor NsrR from Bacillus subtilis senses nitric oxide with a 4Fe-4S Cluster. Biochemistry 47 : 13084 13092.