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Metagenomic data from cerebrospinal fluid permits tracing the origin and spread of Neisseria meningitidis CC4821 in China.

ABSTRACT: Metagenomic next-generation sequencing (mNGS) is useful for difficult to cultivate pathogens. Here, we use cerebrospinal fluid mNGS to diagnose invasive meningococcal disease. The complete genome sequences of Neisseria meningitidis were assembled using N. meningitidis of ST4821-serotype C isolated from four patients. To investigate the phylogeny, 165 CC4821 N. meningitidis genomes from 1972 to 2017 were also included. The core genome accumulated variation at a rate of 4.84×10^-8 substitutions/nucleotide site/year. CC4821 differentiated into four sub-lineages during evolution (A, B, C, and D). While evolving from sub-lineage A (early stage) to sub-lineage D (late stage), the ST and CC4821 serotype converged into the ST4821-serotype C clone. Most strains of sub-lineage D were isolated from invasive meningococcal disease, with increasing resistance to quinolones. Phylogeographic analysis suggests that CC4821 has spread across 14 countries. Thus, the selective pressure of quinolones may cause CC4821 to converge evolutionarily, making it more invasive and facilitating its spread.

SUBMITTER: Chen H

PROVIDER: S-EPMC9388655 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Metagenomic data from cerebrospinal fluid permits tracing the origin and spread of Neisseria meningitidis CC4821 in China.

Chen Hongbin H Li Mei M Tu Shangyu S Zhang Xiaoyang X Wang Xiaojuan X Zhang Yawei Y Zhao Chunjiang C Guo Yinghui Y Wang Hui H

Communications biology 20220818 1

Metagenomic next-generation sequencing (mNGS) is useful for difficult to cultivate pathogens. Here, we use cerebrospinal fluid mNGS to diagnose invasive meningococcal disease. The complete genome sequences of Neisseria meningitidis were assembled using N. meningitidis of ST4821-serotype C isolated from four patients. To investigate the phylogeny, 165 CC4821 N. meningitidis genomes from 1972 to 2017 were also included. The core genome accumulated variation at a rate of 4.84×10<sup>-8</sup> substi ...[more]

PMID: 35982241

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Project description:BackgroundThe human-specific, Gram-negative bacterium Neisseria meningitidis (Nm) is a leading cause of bacterial meningitis worldwide. The blood-cerebrospinal fluid barrier (BCSFB), which is constituted by the epithelial cells of the choroid plexus (CP), has been suggested as one of the potential entry sites of Nm into the CSF and can contribute to the inflammatory response during infectious diseases of the brain. Toll-like receptors (TLRs) are involved in mediating signal transduction caused by the pathogens.MethodsUsing a recently established in vitro model of the human BCSFB based on human malignant CP papilloma (HIBCPP) cells we investigated the cellular response of HIBCPP cells challenged with the meningitis-causing Nm strain, MC58, employing transcriptome and RT-PCR analysis, cytokine bead array, and enzyme-linked immunosorbent assay (ELISA). In comparison, we analyzed the answer to the closely related unencapsulated carrier isolate Nm α14. The presence of TLRs in HIBCPP and their role during signal transduction caused by Nm was studied by RT-PCR and the use of specific agonists and mutant bacteria.ResultsWe observed a stronger transcriptional response after infection with strain MC58, in particular with its capsule-deficient mutant MC58siaD-, which correlated with bacterial invasion levels. Expression evaluation and Gene Set Enrichment Analysis pointed to a NFκB-mediated pro-inflammatory immune response involving up-regulation of the transcription factor IκBζ. Infected cells secreted significant levels of pro-inflammatory chemokines and cytokines, including, among others, IL8, CXCL1-3, and the IκBζ target gene product IL6. The expression profile of pattern recognition receptors in HIBCPP cells and the response to specific agonists indicates that TLR2/TLR6, rather than TLR4 or TLR2/TLR1, is involved in the cellular reaction following Nm infection.ConclusionsOur data show that Nm can initiate a pro-inflammatory response in human CP epithelial cells probably involving TLR2/TLR6 signaling and the transcriptional regulator IκBζ.

Dataset Information

Metagenomic data from cerebrospinal fluid permits tracing the origin and spread of Neisseria meningitidis CC4821 in China.

Publications

Metagenomic data from cerebrospinal fluid permits tracing the origin and spread of Neisseria meningitidis CC4821 in China.

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