Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles

Abstract Background Increased reports of Neisseria meningitidis urethritis in multiple U.S. cities during 2015 have been attributed to the emergence of a novel clade of nongroupable N. meningitidis within the ST-11 clonal complex, the “U.S. NmNG urethritis clade”. Genetic recombination with N. gonor...

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Main Authors: Adam C. Retchless, Cécilia B. Kretz, How-Yi Chang, Jose A. Bazan, A. Jeanine Abrams, Abigail Norris Turner, Laurel T. Jenkins, David L. Trees, Yih-Ling Tzeng, David S. Stephens, Jessica R. MacNeil, Xin Wang
Format: Article
Language:English
Published: BMC 2018-03-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-4560-x
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author Adam C. Retchless
Cécilia B. Kretz
How-Yi Chang
Jose A. Bazan
A. Jeanine Abrams
Abigail Norris Turner
Laurel T. Jenkins
David L. Trees
Yih-Ling Tzeng
David S. Stephens
Jessica R. MacNeil
Xin Wang
spellingShingle Adam C. Retchless
Cécilia B. Kretz
How-Yi Chang
Jose A. Bazan
A. Jeanine Abrams
Abigail Norris Turner
Laurel T. Jenkins
David L. Trees
Yih-Ling Tzeng
David S. Stephens
Jessica R. MacNeil
Xin Wang
Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles
BMC Genomics
Neisseria meningitidis
Genital disease
Gene transfer
Speciation
Neisseria gonorrhoeae
author_facet Adam C. Retchless
Cécilia B. Kretz
How-Yi Chang
Jose A. Bazan
A. Jeanine Abrams
Abigail Norris Turner
Laurel T. Jenkins
David L. Trees
Yih-Ling Tzeng
David S. Stephens
Jessica R. MacNeil
Xin Wang
author_sort Adam C. Retchless
title Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles
title_short Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles
title_full Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles
title_fullStr Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles
title_full_unstemmed Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles
title_sort expansion of a urethritis-associated neisseria meningitidis clade in the united states with concurrent acquisition of n. gonorrhoeae alleles
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2018-03-01
description Abstract Background Increased reports of Neisseria meningitidis urethritis in multiple U.S. cities during 2015 have been attributed to the emergence of a novel clade of nongroupable N. meningitidis within the ST-11 clonal complex, the “U.S. NmNG urethritis clade”. Genetic recombination with N. gonorrhoeae has been proposed to enable efficient sexual transmission by this clade. To understand the evolutionary origin and diversification of the U.S. NmNG urethritis clade, whole-genome phylogenetic analysis was performed to identify its members among the N. meningitidis strain collection from the Centers for Disease Control and Prevention, including 209 urogenital and rectal N. meningitidis isolates submitted by U.S. public health departments in eleven states starting in 2015. Results The earliest representatives of the U.S. NmNG urethritis clade were identified from cases of invasive disease that occurred in 2013. Among 209 urogenital and rectal isolates submitted from January 2015 to September 2016, the clade accounted for 189/198 male urogenital isolates, 3/4 female urogenital isolates, and 1/7 rectal isolates. In total, members of the clade were isolated in thirteen states between 2013 and 2016, which evolved from a common ancestor that likely existed during 2011. The ancestor contained N. gonorrhoeae-like alleles in three regions of its genome, two of which may facilitate nitrite-dependent anaerobic growth during colonization of urogenital sites. Additional gonococcal-like alleles were acquired as the clade diversified. Notably, one isolate contained a sequence associated with azithromycin resistance in N. gonorrhoeae, but no other gonococcal antimicrobial resistance determinants were detected. Conclusions Interspecies genetic recombination contributed to the early evolution and subsequent diversification of the U.S. NmNG urethritis clade. Ongoing acquisition of N. gonorrhoeae alleles by the U.S. NmNG urethritis clade may facilitate the expansion of its ecological niche while also increasing the frequency with which it causes urethritis.
topic Neisseria meningitidis
Genital disease
Gene transfer
Speciation
Neisseria gonorrhoeae
url http://link.springer.com/article/10.1186/s12864-018-4560-x
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spelling doaj-bdd02c0786fd46c192c4a8e56004b3b52020-11-24T23:59:32ZengBMCBMC Genomics1471-21642018-03-0119111510.1186/s12864-018-4560-xExpansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae allelesAdam C. Retchless0Cécilia B. Kretz1How-Yi Chang2Jose A. Bazan3A. Jeanine Abrams4Abigail Norris Turner5Laurel T. Jenkins6David L. Trees7Yih-Ling Tzeng8David S. Stephens9Jessica R. MacNeil10Xin Wang11Division of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and PreventionDivision of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and PreventionDivision of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and PreventionDivision of Infectious Diseases, Department of Internal Medicine, Ohio State University College of MedicineDivision of STD Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, Centers for Disease Control and PreventionDivision of Infectious Diseases, Department of Internal Medicine, Ohio State University College of MedicineDivision of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and PreventionDivision of STD Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, Centers for Disease Control and PreventionDivision of Infectious Diseases, Department of Medicine, Emory University School of MedicineDivision of Infectious Diseases, Department of Medicine, Emory University School of MedicineDivision of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and PreventionDivision of Bacterial Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and PreventionAbstract Background Increased reports of Neisseria meningitidis urethritis in multiple U.S. cities during 2015 have been attributed to the emergence of a novel clade of nongroupable N. meningitidis within the ST-11 clonal complex, the “U.S. NmNG urethritis clade”. Genetic recombination with N. gonorrhoeae has been proposed to enable efficient sexual transmission by this clade. To understand the evolutionary origin and diversification of the U.S. NmNG urethritis clade, whole-genome phylogenetic analysis was performed to identify its members among the N. meningitidis strain collection from the Centers for Disease Control and Prevention, including 209 urogenital and rectal N. meningitidis isolates submitted by U.S. public health departments in eleven states starting in 2015. Results The earliest representatives of the U.S. NmNG urethritis clade were identified from cases of invasive disease that occurred in 2013. Among 209 urogenital and rectal isolates submitted from January 2015 to September 2016, the clade accounted for 189/198 male urogenital isolates, 3/4 female urogenital isolates, and 1/7 rectal isolates. In total, members of the clade were isolated in thirteen states between 2013 and 2016, which evolved from a common ancestor that likely existed during 2011. The ancestor contained N. gonorrhoeae-like alleles in three regions of its genome, two of which may facilitate nitrite-dependent anaerobic growth during colonization of urogenital sites. Additional gonococcal-like alleles were acquired as the clade diversified. Notably, one isolate contained a sequence associated with azithromycin resistance in N. gonorrhoeae, but no other gonococcal antimicrobial resistance determinants were detected. Conclusions Interspecies genetic recombination contributed to the early evolution and subsequent diversification of the U.S. NmNG urethritis clade. Ongoing acquisition of N. gonorrhoeae alleles by the U.S. NmNG urethritis clade may facilitate the expansion of its ecological niche while also increasing the frequency with which it causes urethritis.http://link.springer.com/article/10.1186/s12864-018-4560-xNeisseria meningitidisGenital diseaseGene transferSpeciationNeisseria gonorrhoeae