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Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation

Neisseria meningitidis historically has been an infrequent and sporadic cause of urethritis and other urogenital infections. However, a nonencapsulated meningococcal clade belonging to the hyperinvasive clonal complex 11.2 lineage has recently emerged and caused clusters of urethritis cases in the U...

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Autores principales: Tzeng, Yih-Ling, Sannigrahi, Soma, Berman, Zachary, Bourne, Emily, Edwards, Jennifer L., Bazan, Jose A., Turner, Abigail Norris, Moir, James W. B., Stephens, David S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10187123/
https://www.ncbi.nlm.nih.gov/pubmed/37092998
http://dx.doi.org/10.1128/iai.00079-23
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author Tzeng, Yih-Ling
Sannigrahi, Soma
Berman, Zachary
Bourne, Emily
Edwards, Jennifer L.
Bazan, Jose A.
Turner, Abigail Norris
Moir, James W. B.
Stephens, David S.
author_facet Tzeng, Yih-Ling
Sannigrahi, Soma
Berman, Zachary
Bourne, Emily
Edwards, Jennifer L.
Bazan, Jose A.
Turner, Abigail Norris
Moir, James W. B.
Stephens, David S.
author_sort Tzeng, Yih-Ling
collection PubMed
description Neisseria meningitidis historically has been an infrequent and sporadic cause of urethritis and other urogenital infections. However, a nonencapsulated meningococcal clade belonging to the hyperinvasive clonal complex 11.2 lineage has recently emerged and caused clusters of urethritis cases in the United States and other countries. One of the genetic signatures of the emerging N. meningitidis urethritis clade (NmUC) is a chromosomal gene conversion event resulting in the acquisition of the Neisseria gonorrhoeae denitrification apparatus—the N. gonorrhoeae alleles encoding the nitrite reductase AniA, the nitric oxide (NO) reductase NorB, and the intergenic promoter region. The biological importance of the N. gonorrhoeae AniA-NorB for adaptation of the NmUC to a new environmental niche is investigated herein. We found that oxygen consumption, nitrite utilization, and NO production were significantly altered by the conversion event, resulting in different denitrifying aerobic and microaerobic growth of the clade. Further, transcription of aniA and norB in NmUC isolates differed from canonical N. meningitidis, and important polymorphisms within the intergenic region, which influenced aniA promoter activity of the NmUC, were identified. The contributions of three known meningococcal regulators (NsrR, FNR, and NarQP) in controlling the denitrification pathway and endogenous NO metabolism were distinct. Overall, transcription of aniA was dampened relative to canonical N. meningitidis, and this correlated with the lower NO accumulation in the clade. Denitrification and microaerobic respiration were bolstered, and protection against host-derived NO was likely enhanced. The acquisition of the N. gonorrhoeae denitrification pathway by the NmUC supports the clade’s adaptation and survival in a microaerobic urogenital environment.
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spelling pubmed-101871232023-05-17 Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation Tzeng, Yih-Ling Sannigrahi, Soma Berman, Zachary Bourne, Emily Edwards, Jennifer L. Bazan, Jose A. Turner, Abigail Norris Moir, James W. B. Stephens, David S. Infect Immun Molecular Pathogenesis Neisseria meningitidis historically has been an infrequent and sporadic cause of urethritis and other urogenital infections. However, a nonencapsulated meningococcal clade belonging to the hyperinvasive clonal complex 11.2 lineage has recently emerged and caused clusters of urethritis cases in the United States and other countries. One of the genetic signatures of the emerging N. meningitidis urethritis clade (NmUC) is a chromosomal gene conversion event resulting in the acquisition of the Neisseria gonorrhoeae denitrification apparatus—the N. gonorrhoeae alleles encoding the nitrite reductase AniA, the nitric oxide (NO) reductase NorB, and the intergenic promoter region. The biological importance of the N. gonorrhoeae AniA-NorB for adaptation of the NmUC to a new environmental niche is investigated herein. We found that oxygen consumption, nitrite utilization, and NO production were significantly altered by the conversion event, resulting in different denitrifying aerobic and microaerobic growth of the clade. Further, transcription of aniA and norB in NmUC isolates differed from canonical N. meningitidis, and important polymorphisms within the intergenic region, which influenced aniA promoter activity of the NmUC, were identified. The contributions of three known meningococcal regulators (NsrR, FNR, and NarQP) in controlling the denitrification pathway and endogenous NO metabolism were distinct. Overall, transcription of aniA was dampened relative to canonical N. meningitidis, and this correlated with the lower NO accumulation in the clade. Denitrification and microaerobic respiration were bolstered, and protection against host-derived NO was likely enhanced. The acquisition of the N. gonorrhoeae denitrification pathway by the NmUC supports the clade’s adaptation and survival in a microaerobic urogenital environment. American Society for Microbiology 2023-04-24 /pmc/articles/PMC10187123/ /pubmed/37092998 http://dx.doi.org/10.1128/iai.00079-23 Text en Copyright © 2023 Tzeng et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Molecular Pathogenesis
Tzeng, Yih-Ling
Sannigrahi, Soma
Berman, Zachary
Bourne, Emily
Edwards, Jennifer L.
Bazan, Jose A.
Turner, Abigail Norris
Moir, James W. B.
Stephens, David S.
Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation
title Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation
title_full Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation
title_fullStr Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation
title_full_unstemmed Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation
title_short Acquisition of Gonococcal AniA-NorB Pathway by the Neisseria meningitidis Urethritis Clade Confers Denitrifying and Microaerobic Respiration Advantages for Urogenital Adaptation
title_sort acquisition of gonococcal ania-norb pathway by the neisseria meningitidis urethritis clade confers denitrifying and microaerobic respiration advantages for urogenital adaptation
topic Molecular Pathogenesis
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10187123/
https://www.ncbi.nlm.nih.gov/pubmed/37092998
http://dx.doi.org/10.1128/iai.00079-23
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