Characterization of an ntrX Mutant of Neisseria gonorrhoeae Reveals a Response Regulator That Controls Expression of Respiratory Enzymes in Oxidase-Positive Proteobacteria

Journal of Bacteriology

Volumn 195, Issue 11, 2013, Pages 2632-2641

  Atack, John M ^a,b   Srikhanta, Yogitha N ^a   Djoko, Karrera Y ^a   Welch, Jessica P ^a   Hasri, Norain H M ^a   Steichen, Christopher T ^c   Vanden Hoven, Rachel N ^a   Grimmond, S M ^a   Pg Othman, Dk Seti Maimonah ^a   Kappler, Ulrike ^a   Apicella, Michael A ^c   Jennings, Michael P ^a,b   Edwards, Jennifer L ^d   McEwan, Alastair G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c UNIVERSITY OF IOWA   (United States)

^d THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CYTOCHROME C OXIDASE; NITRIC OXIDE REDUCTASE; NITRITE REDUCTASE;

ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM MUTANT; BIOFILM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; EPITHELIUM CELL; FEMALE; GENE DISRUPTION; HUMAN; HUMAN CELL; INDEL MUTATION; MICROARRAY ANALYSIS; NEISSERIA GONORRHOEAE; NONHUMAN; NTRX GENE; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOBACTERIA; REGULATORY MECHANISM; RESPIRATORY CHAIN; RHODOBACTER CAPSULATUS; WILD TYPE;

BACTERIAL PROTEINS; BIOFILMS; CERVIX UTERI; ELECTRON TRANSPORT COMPLEX IV; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOME, BACTERIAL; GONORRHEA; HUMANS; MICROBIAL VIABILITY; NEISSERIA GONORRHOEAE; NITRITE REDUCTASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDOREDUCTASES; OXYGEN; PHYLOGENY; RHODOBACTER CAPSULATUS; RNA, BACTERIAL; SEQUENCE DELETION;

EID: 84877939990     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02062-12     Document Type: Article

References (69)

1. Poole RK, Cook GM. 2000. Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv. Microb. Physiol. 43:165-224.
2. Aspholm M, Aas FE, Harrison OB, Quinn D, Vik å, Viburiene R, Tønjum T, Moir J, Maiden MCJ, Koomey M. 2010. Structural alterations in a component of cytochrome c oxidase and molecular evolution of pathogenic Neisseria in humans. PLoS Pathog. 6:e1001055. doi:10.1371/journal.ppat.1001055.
3. Colburn-Clifford J, Allen C. 2010. A cbb3-type cytochrome c oxidase contributes to Ralstonia solanacearum R3bv2 growth in microaerobic environments and to bacterial wilt disease development in tomato. Mol. Plant Microbe Interact. 23:1042-1052.
4. Pitcher RS, Watmough NJ. 2004. The bacterial cytochrome cbb3 oxidases. Biochim. Biophys. Acta 1655:388-399.
5. Nagata K, Tsukita S, Tamura T, Sone N. 1996. A db-type cytochrome c oxidase terminates the respiratory chain in Helicobacter pylori. Microbiology 142:1757-1763.
6. Gordon J, McLeod JW. 1928. The practical application of the direct oxidase reaction in bacteriology. J. Pathol. Bacteriol. 31:185-190.
7. Kovacs N. 1956. Identification of Pseudomonas pyocyanae by the oxidase reaction. Nature 178:703.
8. Ekici S, Pawlik G, Lohmeyer E, Koch Daldal H-GF. 2012. Biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus. Biochim. Biophys. Acta 1817:898-910.
9. Garcia-Horsman JA, Barquera B, Rumbley J, Ma J, Gennis RB. 1994. The superfamily of heme-copper respiratory oxidases. J. Bacteriol. 176: 5587-5600.
10. Preisig O, Zufferey R, Thony-Meyer L, Appleby CA, Hennecke H. 1996. A high-affinity cbb3-type cytochrome oxidase terminates the symbiosisspecific respiratory chain of Bradyrhizobium japonicum. J. Bacteriol. 178: 1532-1538.
11. Preisig O, Anthamatten D, Hennecke H. 1993. Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. U. S. A. 90:3309-3313.
12. Swem LR, Elsen S, Bird TH, Swem DL, Koch Myllykallio H-GH, Daldal F, Bauer CE. 2001. The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus. J. Mol. Biol. 309:121-138.
13. Partridge JD, Sanguinetti G, Dibden DP, Roberts RE, Poole RK, Green J. 2007. Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components. J. Biol. Chem. 282:11230-11237.
14. Park SJ, Chao G, Gunsalus RP. 1997. Aerobic regulation of the sucABCD genes of Escherichia coli, which encode alpha-ketoglutarate dehydrogenase and succinyl coenzyme A synthetase: roles of ArcA, Fnr, and the upstream sdhCDAB promoter. J. Bacteriol. 179:4138-4142.
15. Park SJ, Cotter PA, Gunsalus RP. 1995. Regulation of malate dehydrogenase (mdh) gene expression in Escherichia coli in response to oxygen, carbon, and heme availability. J. Bacteriol. 177:6652-6656.
16. Cotter PA, Melville SB, Albrecht JA, Gunsalus RP. 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.
17. Govantes F, Albrecht JA, Gunsalus RP. 2000. Oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon: roles of multiple promoters and the Fnr-1 and Fnr-2 binding sites. Mol. Microbiol. 37: 1456-1469.
18. Bauer C, Elsen S, Swem LR, Swem DL, Masuda S. 2003. Redox and light regulation of gene expression in photosynthetic prokaryotes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358:147-154.
19. Swem DL, Bauer CE. 2002. Coordination of ubiquinol oxidase and cytochrome cbb3 oxidase expression by multiple regulators in Rhodobacter capsulatus. J. Bacteriol. 184:2815-2820.
20. Swem LR, Kraft BJ, Swem DL, Setterdahl AT, Masuda S, Knaff DB, Zaleski JM, Bauer CE. 2003. Signal transduction by the global regulator RegB is mediated by a redox-active cysteine. EMBO J. 22:4699-4708.
21. Ishida ML, Assumpcao MC, Machado HB, Benelli EM, Souza EM, Pedrosa FO. 2002. Identification and characterization of the twocomponent NtrY/NtrX regulatory system in Azospirillum brasilense. Braz. J. Med. Biol. Res. 35:651-661.
22. Pawlowski K, Klosse U, de Bruijn FJ. 1991. Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism. Mol. Gen. Genet. 231:124-138.
23. Masepohl B, Klipp W, Puhler A. 1988. Genetic characterization and sequence analysis of the duplicated nifA/nifB gene region of Rhodobacter capsulatus. Mol. Gen. Genet. 212:27-37.
24. Carrica MdC, Fernandez I, Martí MA, Paris G, Goldbaum FA. 2012. The NtrY/X two-component system of Brucella spp. acts as a redox sensor and regulates the expression of nitrogen respiration enzymes. Mol. Microbiol. 85:39-50.
25. Weaver PF, Wall JD, Gest H. 1975. Characterization of Rhodopseudomonas capsulata. Arch. Microbiol. 105:207-216.
26. Beringer JE. 1974. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84:188-198.
27. Kappler U, Huston WM, McEwan AG. 2002. Control of dimethylsulfoxide reductase expression in Rhodobacter capsulatus: the role of carbon metabolites and the response regulators DorR and RegA. Microbiology 148:605-614.
28. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Biotechnol. 1:784-791.
29. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Steichen CT, Shao JQ, Ketterer MR, Apicella MA. 2008. Gonococcal cervicitis: a role for biofilm in pathogenesis. J. Infect. Dis. 198:1856-1861.
31. Drepper T, Wiethaus J, Giaourakis D, Gross S, Schubert B, Vogt M, Wiencek Y, McEwan AG, Masepohl B. 2006. Cross-talk towards the response regulator NtrC controlling nitrogen metabolism in Rhodobacter capsulatus. FEMS Microbiol. Lett. 258:250-256.
32. Kappler U, Sly LI, McEwan AG. 2005. Respiratory gene clusters of Metallosphaera sedula-differential expression and transcriptional organization. Microbiology 151:35-43.
33. Markwell JP, Lascelles J. 1978. Membrane-bound, pyridine nucleotideindependent L-lactate dehydrogenase of Rhodopseudomonas sphaeroides. J. Bacteriol. 133:593-600.
34. Markwell MAK, Haas SM, Bieber LL, Tolbert NE. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87:206-210.
35. Dupuis A, Peinnequin A, Darrouzet E, Lunardi J. 1997. Genetic disruption of the respiratory NADH-ubiquinone reductase of Rhodobacter capsulatus leads to an unexpected photosynthesis-negative phenotype. FEMS Microbiol. Lett. 148:107-114.
36. Anderlund M, Nissen TL, Nielsen J, Villadsen J, Rydstram J, Hahn-Hagerdal B, Kielland-Brandt MC. 1999. Expression of the Escherichia coli pntA and pntB genes, encoding nicotinamide nucleotide transhydrogenase, in Saccharomyces cerevisiae and its effect on product formation dur-ing anaerobic glucose fermentation. Appl. Environ. Microbiol. 65:2333-2340.
37. Sellars MJ, Hall SJ, Kelly DJ. 2002. Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-Noxide, or dimethyl sulfoxide requires oxygen. J. Bacteriol. 184:4187-4196.
38. Seib KL, Wu HJ, Srikhanta YN, Edwards JL, Falsetta ML, Hamilton AJ, Maguire TL, Grimmond SM, Apicella MA, McEwan AG, Jennings MP. 2007. Characterization of the OxyR regulon of Neisseria gonorrhoeae. Mol. Microbiol. 63:54-68.
39. Edwards JL, Apicella MA. 2005. I-domain-containing integrins serve as pilus receptors for Neisseria gonorrhoeae adherence to human epithelial cells. Cell. Microbiol. 7:1197-1211.
40. Falsetta ML, Bair TB, Ku SC, vanden Hoven RN, Steichen CT, McEwan AG, Jennings MP, Apicella MA. 2009. Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms. Infect. Immun. 77:3522-3532.
41. Neil RB, Apicella MA. 2009. Role of HrpA in biofilm formation of Neisseria meningitidis and regulation of the hrpBAS transcripts. Infect. Immun. 77:2285-2293.
42. Edwards JL, Shao JQ, Ault KA, Apicella MA. 2000. Neisseria gonorrhoeae elicits membrane ruffling and cytoskeletal rearrangements upon infection of primary human endocervical and ectocervical cells. Infect. Immun. 68:5354-5363.
43. Wu HJ, Seib KL, Edwards JL, Apicella MA, McEwan AG, Jennings MP. 2005. Azurin of pathogenic Neisseria spp. is involved in defense against hydrogen peroxide and survival within cervical epithelial cells. Infect. Immun. 73:8444-8448.
44. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
45. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
46. Deeudom M, Koomey M, Moir JWB. 2008. Roles of c-type cytochromes in respiration in Neisseria meningitidis. Microbiology 154:2857-2864.
47. Snyder LAS, Davies JK, Ryan CS, Saunders NJ. 2005. Comparative overview of the genomic and genetic differences between the pathogenic Neisseria strains and species. Plasmid 54:191-218.
48. Atack JM, Kelly DJ. 2007. Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases. Adv. Microb. Physiol. 52:73-106.
49. Barth KR, Isabella VM, Clark VL. 2009. Biochemical and genomic analysis of the denitrification pathway within the genus Neisseria. Microbiology 155:4093-4103.
50. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462.
51. Dempsey JA, Litaker W, Madhure A, Snodgrass TL, Cannon JG. 1991. Physical map of the chromosome of Neisseria gonorrhoeae FA1090 with locations of genetic markers, including opa and pil genes. J. Bacteriol. 173:5476-5486.
52. Falsetta ML, McEwan AG, Jennings MP, Apicella MA. 2010. Anaerobic metabolism occurs in the substratum of gonococcal biofilms and may be sustained in part by nitric oxide. Infect. Immun. 78:2320-2328.
53. Falsetta ML, Steichen CT, McEwan AG, Cho C, Ketterer M, Shao J, Hunt J, Jennings MP, Apicella MA. 2011. The composition and metabolic phenotype of Neisseria gonorrhoeae biofilms. Front. Microbiol. 2:75. doi:10.3389/fmicb.2011.00075.
54. Kern D, Volkman BF, Luginbuhl P, Nohaile MJ, Kustu S, Wemmer DE. 1999. Structure of a transiently phosphorylated switch in bacterial signal transduction. Nature 402:894-898.
55. Pelton JG, Kustu S, Wemmer DE. 1999. Solution structure of the DNAbinding domain of NtrC with three alanine substitutions. J. Mol. Biol. 292:1095-1110.
56. Volkman BF, Nohaile MJ, Amy NK, Kustu S, Wemmer DE. 1995. Three-dimensional solution structure of the N-terminal receiver domain of NTRC. Biochemistry 34:1413-1424.
57. Kumagai Y, Cheng Z, Lin M, Rikihisa Y. 2006. Biochemical activities of three pairs of Ehrlichia chaffeensis two-component regulatory system proteins involved in inhibition of lysosomal fusion. Infect. Immun. 74:5014-5022.
58. Beier D, Gross R. 2006. Regulation of bacterial virulence by twocomponent systems. Curr. Opin. Microbiol. 9:143-152.
59. Wong SMS, St. Michael F, Cox A, Ram S, Akerley BJ. 2011. ArcAregulated glycosyltransferase Lic2B promotes complement evasion and pathogenesis of non-typeable Haemophilus influenzae. Infect. Immun. 79: 1971-1983.
60. Halling SM, Peterson-Burch BD, Bricker BJ, Zuerner RL, Qing Z, Li LL, Kapur V, Alt DP, Olsen SC. 2005. Completion of the genome sequence of Brucella abortus and comparison to the highly similar genomes of Brucella melitensis and Brucella suis. J. Bacteriol. 187:2715-2726.
61. Taylor BL, Zhulin IB. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
62. Way SS, Sallustio S, Magliozzo RS, Goldberg MB. 1999. Impact of either elevated or decreased levels of cytochrome bd expression on Shigella flexneri virulence. J. Bacteriol. 181:1229-1237.
63. Jiménez de Bagüés MP, Loisel-Meyer S, Liautard JP, Jubier-Maurin V. 2007. Different roles of the two high-oxygen-affinity terminal oxidases of Brucella suis: cytochrome c oxidase, but not ubiquinol oxidase, is required for persistence in mice. Infect. Immun. 75:531-535.
64. Edwards JL. 2010. Neisseria gonorrhoeae survival during primary human cervical epithelial cell infection requires nitric oxide and is augmented by progesterone. Infect. Immun. 78:1202-1213.
65. Edwards JL, Butler EK. 2011. The pathobiology of Neisseria gonorrhoeae lower female genital tract infection. Front. Microbiol. 2:102. doi:10.3389/fmicb.2011.00102.
66. Whitehead RN, Overton TW, Snyder LA, McGowan SJ, Smith H, Cole JA, Saunders NJ. 2007. The small FNR regulon of Neisseria gonorrhoeae: comparison with the larger Escherichia coli FNR regulon and interaction with the NarQ-NarP regulon. BMC Genomics 8:35. doi:10.1186/1471-2164-8-35.
67. Overton TW, Whitehead R, Li Y, Snyder LAS, Saunders NJ, Smith H, Cole JA. 2006. Coordinated regulation of the Neisseria gonorrhoeae truncated denitrification pathway by the nitric oxide-sensitive repressor, NsrR, and nitrite-insensitive NarQ-NarP. J. Biol. Chem. 281:33115-33126.
68. Masepohl B, Drepper T, Paschen A, Gross S, Pawlowski A, Raabe K, Riedel KU, Klipp W. 2002. Regulation of nitrogen fixation in the phototrophic purple bacterium Rhodobacter capsulatus. J. Mol. Microbiol. Biotechnol. 4:243-248.
69. Laskos L, Dillard JP, Seifert HS, Fyfe JA, Davies JK. 1998. The pathogenic Neisseriae contain an inactive rpoN gene and do not utilize the pilE sigma54 promoter. Gene 208:95-102.