Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traits

Cysteiniphilum is a newly discovered genus in 2017 and is phylogenetically closely related to highly pathogenic Francisella tularensis. Recently, it has become an emerging pathogen in humans. However, the complete genome sequence of genus Cysteiniphilum is lacking, and the genomic characteristics of...

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Main Authors: Changrui Qian, Mengxin Xu, Zeyu Huang, Miran Tan, Cheng Fu, Tieli Zhou, Jianming Cao, Cui Zhou
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Virulence
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Online Access:https://www.tandfonline.com/doi/10.1080/21505594.2023.2214416
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author Changrui Qian
Mengxin Xu
Zeyu Huang
Miran Tan
Cheng Fu
Tieli Zhou
Jianming Cao
Cui Zhou
author_facet Changrui Qian
Mengxin Xu
Zeyu Huang
Miran Tan
Cheng Fu
Tieli Zhou
Jianming Cao
Cui Zhou
author_sort Changrui Qian
collection DOAJ
description Cysteiniphilum is a newly discovered genus in 2017 and is phylogenetically closely related to highly pathogenic Francisella tularensis. Recently, it has become an emerging pathogen in humans. However, the complete genome sequence of genus Cysteiniphilum is lacking, and the genomic characteristics of genetic diversity, evolutionary dynamics, and pathogenicity have not been characterized. In this study, the complete genome of the first reported clinical isolate QT6929 of genus Cysteiniphilum was sequenced, and comparative genomics analyses to Francisella genus were conducted to unveil the genomic landscape and diversity of the genus Cysteiniphilum. Our results showed that the complete genome of QT6929 consists of one 2.61 Mb chromosome and a 76,819 bp plasmid. The calculated average nucleotide identity and DNA–DNA hybridization values revealed that two clinical isolates QT6929 and JM-1 should be reclassified as two novel species in genus Cysteiniphilum. Pan-genome analysis revealed genomic diversity within the genus Cysteiniphilum and an open pan-genome state. Genomic plasticity analysis exhibited abundant mobile genetic elements including genome islands, insertion sequences, prophages, and plasmids on Cysteiniphilum genomes, which facilitated the broad exchange of genetic material between Cysteiniphilum and other genera like Francisella and Legionella. Several potential virulence genes associated with lipopolysaccharide/lipooligosaccharide, capsule, and haem biosynthesis specific to clinical isolates were predicted and might contribute to their pathogenicity in humans. Incomplete Francisella pathogenicity island was identified in most Cysteiniphilum genomes. Overall, our study provides an updated phylogenomic relationship of members of the genus Cysteiniphilum and comprehensive genomic insights into this rare emerging pathogen.
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spelling doaj-art-a322eac85b1f44e883d03b232b2061662025-08-20T03:27:33ZengTaylor & Francis GroupVirulence2150-55942150-56082023-12-0114110.1080/21505594.2023.2214416Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traitsChangrui Qian0Mengxin Xu1Zeyu Huang2Miran Tan3Cheng Fu4Tieli Zhou5Jianming Cao6Cui Zhou7Department of Clinical Laboratory, The First Affiliated Hospital of Wenzhou Medical University; Key Laboratory of Clinical Laboratory Diagnosis and Translational Research of Zhejiang Province, Wenzhou, ZhejiangProvince, ChinaDepartment of Clinical Laboratory, The First Affiliated Hospital of Wenzhou Medical University; Key Laboratory of Clinical Laboratory Diagnosis and Translational Research of Zhejiang Province, Wenzhou, ZhejiangProvince, ChinaDepartment of Clinical Laboratory, The First Affiliated Hospital of Wenzhou Medical University; Key Laboratory of Clinical Laboratory Diagnosis and Translational Research of Zhejiang Province, Wenzhou, ZhejiangProvince, ChinaDepartment of Clinical Laboratory, The First Affiliated Hospital of Wenzhou Medical University; Key Laboratory of Clinical Laboratory Diagnosis and Translational Research of Zhejiang Province, Wenzhou, ZhejiangProvince, ChinaDepartment of Clinical Laboratory, The First Affiliated Hospital of Wenzhou Medical University; Key Laboratory of Clinical Laboratory Diagnosis and Translational Research of Zhejiang Province, Wenzhou, ZhejiangProvince, ChinaDepartment of Clinical Laboratory, The First Affiliated Hospital of Wenzhou Medical University; Key Laboratory of Clinical Laboratory Diagnosis and Translational Research of Zhejiang Province, Wenzhou, ZhejiangProvince, ChinaSchool of Laboratory Medicine and Life Science, Wenzhou Medical University, Wenzhou, Zhejiang Province, ChinaDepartment of Clinical Laboratory, The First Affiliated Hospital of Wenzhou Medical University; Key Laboratory of Clinical Laboratory Diagnosis and Translational Research of Zhejiang Province, Wenzhou, ZhejiangProvince, ChinaCysteiniphilum is a newly discovered genus in 2017 and is phylogenetically closely related to highly pathogenic Francisella tularensis. Recently, it has become an emerging pathogen in humans. However, the complete genome sequence of genus Cysteiniphilum is lacking, and the genomic characteristics of genetic diversity, evolutionary dynamics, and pathogenicity have not been characterized. In this study, the complete genome of the first reported clinical isolate QT6929 of genus Cysteiniphilum was sequenced, and comparative genomics analyses to Francisella genus were conducted to unveil the genomic landscape and diversity of the genus Cysteiniphilum. Our results showed that the complete genome of QT6929 consists of one 2.61 Mb chromosome and a 76,819 bp plasmid. The calculated average nucleotide identity and DNA–DNA hybridization values revealed that two clinical isolates QT6929 and JM-1 should be reclassified as two novel species in genus Cysteiniphilum. Pan-genome analysis revealed genomic diversity within the genus Cysteiniphilum and an open pan-genome state. Genomic plasticity analysis exhibited abundant mobile genetic elements including genome islands, insertion sequences, prophages, and plasmids on Cysteiniphilum genomes, which facilitated the broad exchange of genetic material between Cysteiniphilum and other genera like Francisella and Legionella. Several potential virulence genes associated with lipopolysaccharide/lipooligosaccharide, capsule, and haem biosynthesis specific to clinical isolates were predicted and might contribute to their pathogenicity in humans. Incomplete Francisella pathogenicity island was identified in most Cysteiniphilum genomes. Overall, our study provides an updated phylogenomic relationship of members of the genus Cysteiniphilum and comprehensive genomic insights into this rare emerging pathogen.https://www.tandfonline.com/doi/10.1080/21505594.2023.2214416CysteiniphilumFrancisellapan-genomepathogengenetic diversitycomparative genomic
spellingShingle Changrui Qian
Mengxin Xu
Zeyu Huang
Miran Tan
Cheng Fu
Tieli Zhou
Jianming Cao
Cui Zhou
Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traits
Virulence
Cysteiniphilum
Francisella
pan-genome
pathogen
genetic diversity
comparative genomic
title Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traits
title_full Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traits
title_fullStr Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traits
title_full_unstemmed Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traits
title_short Complete genome sequence of the emerging pathogen Cysteiniphilum spp. and comparative genomic analysis with genus Francisella: Insights into its genetic diversity and potential virulence traits
title_sort complete genome sequence of the emerging pathogen cysteiniphilum spp and comparative genomic analysis with genus francisella insights into its genetic diversity and potential virulence traits
topic Cysteiniphilum
Francisella
pan-genome
pathogen
genetic diversity
comparative genomic
url https://www.tandfonline.com/doi/10.1080/21505594.2023.2214416
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