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

Atack, J.M.; Srikhanta, Y.N.; ,, K.Y.; Welch, J.P.; Hasri, N.H.M.; Steichen, C.T.; Vanden Hoven, R.N.; Grimmond, S.M.; Othman, D.S.M.P.; Kappler, U.; Apicella, M.A.; Jennings, M.P.; Edwards, J.L.; McEwan, A.G.

Authors

J.M. Atack

Y.N. Srikhanta

K.Y. ,

J.P. Welch

N.H.M. Hasri

C.T. Steichen

R.N. Vanden Hoven

S.M. Grimmond

D.S.M.P. Othman

U. Kappler

M.A. Apicella

M.P. Jennings

J.L. Edwards

A.G. McEwan



Contributors

Abstract

NtrYX is a sensor-histidine kinase/response regulator two-component system that has had limited characterization in a small number of Alphaproteobacteria. Phylogenetic analysis of the response regulator NtrX showed that this two-component system is extensively distributed across the bacterial domain, and it is present in a variety of Betaproteobacteria, including the human pathogen Neisseria gonorrhoeae. Microarray analysis revealed that the expression of several components of the respiratory chain was reduced in an N. gonorrhoeae ntrX mutant compared to that in the isogenic wild-type (WT) strain 1291. These included the cytochrome c oxidase subunit (ccoP), nitrite reductase (aniA), and nitric oxide reductase (norB). Enzyme activity assays showed decreased cytochrome oxidase and nitrite reductase activities in the ntrX mutant, consistent with microarray data. N. gonorrhoeae ntrX mutants had reduced capacity to survive inside primary cervical cells compared to the wild type, and although they retained the ability to form a biofilm, they exhibited reduced survival within the biofilm compared to wild-type cells, as indicated by LIVE/DEAD staining. Analyses of an ntrX mutant in a representative alphaproteobacterium, Rhodobacter capsulatus, showed that cytochrome oxidase activity was also reduced compared to that in the wild-type strain SB1003. Taken together, these data provide evidence that the NtrYX two-component system may be a key regulator in the expression of respiratory enzymes and, in particular, cytochrome c oxidase, across a wide range of proteobacteria, including a variety of bacterial pathogens.

Citation

Atack, J., Srikhanta, Y., ,, K., Welch, J., Hasri, N., Steichen, C., …McEwan, A. (2013). 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, 195(11), 2632-2641. https://doi.org/10.1128/jb.02062-12

Journal Article Type Article
Acceptance Date Mar 12, 2013
Online Publication Date Apr 5, 2013
Publication Date 2013-06
Deposit Date Sep 6, 2017
Journal Journal of Bacteriology
Print ISSN 0021-9193
Electronic ISSN 1098-5530
Publisher American Society for Microbiology
Peer Reviewed Peer Reviewed
Volume 195
Issue 11
Pages 2632-2641
DOI https://doi.org/10.1128/jb.02062-12