Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage

Jay Lucidarme; Bingqing Zhu; Li Xu; Xilian Bai; Yuan Gao; Juan José González-López; Robert Mulhall; Kevin J. Scott; Andrew Smith; Paola Stefanelli; Bianca Stenmark; Paul Torpiano; Georgina Tzanakaki; Raymond Borrow; Zhujun Shao

doi:10.1371/journal.pone.0243426

Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage

Jay Lucidarme^*
, Bingqing Zhu
, Li Xu
, Xilian Bai
, Yuan Gao
, Juan José González-López
, Robert Mulhall
, Kevin J. Scott
, Andrew Smith
, Paola Stefanelli
, Bianca Stenmark
, Paul Torpiano
, Georgina Tzanakaki
, Raymond Borrow
, Zhujun Shao

^*Corresponding author for this work

Manchester Meningococcal Reference Unit General

Research output: Contribution to journal › Article › peer-review

12 Citations (Scopus)

14 Downloads (Pure)

Abstract

Introduction: The ST-4821 complex (cc4821) is a leading cause of serogroup C and serogroup B invasive meningococcal disease in China where diverse strains in two phylogenetic groups (groups 1 and 2) have acquired fluoroquinolone resistance. cc4821 was recently prevalent among carriage isolates in men who have sex with men in New York City (USA). Genome-level population studies have thus far been limited to Chinese isolates. The aim of the present study was to build upon these with an extended panel of international cc4821 isolates.

Methods: Genomes of isolates from Asia (1972 to 2017), Europe (2011 to 2018), North America (2007), and South America (2014) were sequenced or obtained from the PubMLST Neisseria database. Core genome comparisons were performed in PubMLST.

Results: Four lineages were identified. Western isolates formed a distinct, mainly serogroup B sublineage with alleles associated with fluoroquinolone susceptibility (MIC <0.03 mg/L) and reduced penicillin susceptibility (MIC 0.094 to 1 mg/L). A third of these were from anogenital sites in men who have sex with men and had unique denitrification gene alleles. Generally 4CMenB vaccine strain coverage was reliant on strain-specific NHBA peptides.

Discussion: The previously identified cc4821 group 2 was resolved into three separate lineages. Clustering of western isolates was surprising given the overall diversity of cc4821. Possible association of this cluster with the anogenital niche is worthy of monitoring given concerns surrounding antibiotic resistance and potential subcapsular vaccine escape.

Original language	English
Article number	e0243426
Journal	PLoS ONE
Volume	15
Issue number	12
DOIs	https://doi.org/10.1371/journal.pone.0243426
Publication status	Published - 10 Dec 2020

Bibliographical note

Funding Information: This work was supported by grants (ZS) from the National Key Program for Infectious Disease of China (contract no. 2013ZX10004221 and 2018ZX10714002-001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Open Access: This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Publisher Copyright: © 2020 Lucidarme et al.

Citation: Lucidarme J, Zhu B, Xu L, Bai X, Gao Y, González-López JJ, et al. (2020) Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage. PLoS ONE 15(12): e0243426.

DOI: https://doi.org/10.1371/journal.pone.0243426

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Cite this

Lucidarme, J., Zhu, B., Xu, L., Bai, X., Gao, Y., González-López, J. J., Mulhall, R., Scott, K. J., Smith, A., Stefanelli, P., Stenmark, B., Torpiano, P., Tzanakaki, G., Borrow, R., & Shao, Z. (2020). Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage. PLoS ONE, 15(12), Article e0243426. https://doi.org/10.1371/journal.pone.0243426

@article{4dbef905ce46418c9fbd2db83f28850b,

title = "Genomic analysis of the meningococcal ST-4821 complex{\textendash}Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage",

abstract = "Introduction: The ST-4821 complex (cc4821) is a leading cause of serogroup C and serogroup B invasive meningococcal disease in China where diverse strains in two phylogenetic groups (groups 1 and 2) have acquired fluoroquinolone resistance. cc4821 was recently prevalent among carriage isolates in men who have sex with men in New York City (USA). Genome-level population studies have thus far been limited to Chinese isolates. The aim of the present study was to build upon these with an extended panel of international cc4821 isolates. Methods: Genomes of isolates from Asia (1972 to 2017), Europe (2011 to 2018), North America (2007), and South America (2014) were sequenced or obtained from the PubMLST Neisseria database. Core genome comparisons were performed in PubMLST. Results: Four lineages were identified. Western isolates formed a distinct, mainly serogroup B sublineage with alleles associated with fluoroquinolone susceptibility (MIC <0.03 mg/L) and reduced penicillin susceptibility (MIC 0.094 to 1 mg/L). A third of these were from anogenital sites in men who have sex with men and had unique denitrification gene alleles. Generally 4CMenB vaccine strain coverage was reliant on strain-specific NHBA peptides. Discussion: The previously identified cc4821 group 2 was resolved into three separate lineages. Clustering of western isolates was surprising given the overall diversity of cc4821. Possible association of this cluster with the anogenital niche is worthy of monitoring given concerns surrounding antibiotic resistance and potential subcapsular vaccine escape.",

author = "Jay Lucidarme and Bingqing Zhu and Li Xu and Xilian Bai and Yuan Gao and Gonz{\'a}lez-L{\'o}pez, \{Juan Jos{\'e}\} and Robert Mulhall and Scott, \{Kevin J.\} and Andrew Smith and Paola Stefanelli and Bianca Stenmark and Paul Torpiano and Georgina Tzanakaki and Raymond Borrow and Zhujun Shao",

note = "Funding Information: This work was supported by grants (ZS) from the National Key Program for Infectious Disease of China (contract no. 2013ZX10004221 and 2018ZX10714002-001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Open Access: This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Publisher Copyright: {\textcopyright} 2020 Lucidarme et al. Citation: Lucidarme J, Zhu B, Xu L, Bai X, Gao Y, Gonz{\'a}lez-L{\'o}pez JJ, et al. (2020) Genomic analysis of the meningococcal ST-4821 complex{\textendash}Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage. PLoS ONE 15(12): e0243426. DOI: https://doi.org/10.1371/journal.pone.0243426",

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doi = "10.1371/journal.pone.0243426",

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Lucidarme, J, Zhu, B, Xu, L, Bai, X, Gao, Y, González-López, JJ, Mulhall, R, Scott, KJ, Smith, A, Stefanelli, P, Stenmark, B, Torpiano, P, Tzanakaki, G, Borrow, R & Shao, Z 2020, 'Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage', PLoS ONE, vol. 15, no. 12, e0243426. https://doi.org/10.1371/journal.pone.0243426

TY - JOUR

T1 - Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage

AU - Lucidarme, Jay

AU - Zhu, Bingqing

AU - Xu, Li

AU - Bai, Xilian

AU - Gao, Yuan

AU - González-López, Juan José

AU - Mulhall, Robert

AU - Scott, Kevin J.

AU - Smith, Andrew

AU - Stefanelli, Paola

AU - Stenmark, Bianca

AU - Torpiano, Paul

AU - Tzanakaki, Georgina

AU - Borrow, Raymond

AU - Shao, Zhujun

N1 - Funding Information: This work was supported by grants (ZS) from the National Key Program for Infectious Disease of China (contract no. 2013ZX10004221 and 2018ZX10714002-001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Open Access: This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Publisher Copyright: © 2020 Lucidarme et al. Citation: Lucidarme J, Zhu B, Xu L, Bai X, Gao Y, González-López JJ, et al. (2020) Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage. PLoS ONE 15(12): e0243426. DOI: https://doi.org/10.1371/journal.pone.0243426

PY - 2020/12/10

Y1 - 2020/12/10

N2 - Introduction: The ST-4821 complex (cc4821) is a leading cause of serogroup C and serogroup B invasive meningococcal disease in China where diverse strains in two phylogenetic groups (groups 1 and 2) have acquired fluoroquinolone resistance. cc4821 was recently prevalent among carriage isolates in men who have sex with men in New York City (USA). Genome-level population studies have thus far been limited to Chinese isolates. The aim of the present study was to build upon these with an extended panel of international cc4821 isolates. Methods: Genomes of isolates from Asia (1972 to 2017), Europe (2011 to 2018), North America (2007), and South America (2014) were sequenced or obtained from the PubMLST Neisseria database. Core genome comparisons were performed in PubMLST. Results: Four lineages were identified. Western isolates formed a distinct, mainly serogroup B sublineage with alleles associated with fluoroquinolone susceptibility (MIC <0.03 mg/L) and reduced penicillin susceptibility (MIC 0.094 to 1 mg/L). A third of these were from anogenital sites in men who have sex with men and had unique denitrification gene alleles. Generally 4CMenB vaccine strain coverage was reliant on strain-specific NHBA peptides. Discussion: The previously identified cc4821 group 2 was resolved into three separate lineages. Clustering of western isolates was surprising given the overall diversity of cc4821. Possible association of this cluster with the anogenital niche is worthy of monitoring given concerns surrounding antibiotic resistance and potential subcapsular vaccine escape.

AB - Introduction: The ST-4821 complex (cc4821) is a leading cause of serogroup C and serogroup B invasive meningococcal disease in China where diverse strains in two phylogenetic groups (groups 1 and 2) have acquired fluoroquinolone resistance. cc4821 was recently prevalent among carriage isolates in men who have sex with men in New York City (USA). Genome-level population studies have thus far been limited to Chinese isolates. The aim of the present study was to build upon these with an extended panel of international cc4821 isolates. Methods: Genomes of isolates from Asia (1972 to 2017), Europe (2011 to 2018), North America (2007), and South America (2014) were sequenced or obtained from the PubMLST Neisseria database. Core genome comparisons were performed in PubMLST. Results: Four lineages were identified. Western isolates formed a distinct, mainly serogroup B sublineage with alleles associated with fluoroquinolone susceptibility (MIC <0.03 mg/L) and reduced penicillin susceptibility (MIC 0.094 to 1 mg/L). A third of these were from anogenital sites in men who have sex with men and had unique denitrification gene alleles. Generally 4CMenB vaccine strain coverage was reliant on strain-specific NHBA peptides. Discussion: The previously identified cc4821 group 2 was resolved into three separate lineages. Clustering of western isolates was surprising given the overall diversity of cc4821. Possible association of this cluster with the anogenital niche is worthy of monitoring given concerns surrounding antibiotic resistance and potential subcapsular vaccine escape.

UR - https://www.scopus.com/pages/publications/85097826145

U2 - 10.1371/journal.pone.0243426

DO - 10.1371/journal.pone.0243426

M3 - Article

C2 - 33301524

AN - SCOPUS:85097826145

SN - 1932-6203

VL - 15

JO - PLoS ONE

JF - PLoS ONE

IS - 12

M1 - e0243426

ER -

Genomic analysis of the meningococcal ST-4821 complex–Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage

Abstract

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