Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolate

IntroductionAn extended-spectrum beta-lactamase (ESBL)-hypervirulent Klebsiella pneumoniae (HvKP) strain HKE9 was isolated from the blood in an outpatient.MethodsThe effect of the global regulatory factor RpoS on antimicrobial resistance, pathogenicity, and environmental adaptability was elucidated....

Full description

Bibliographic Details
Main Authors: Yi Zhou, Yue Cheng, Tianyou Ma, Jun Wang, Shaoru Li, Jingdan Wang, Lei Han, Xinyao Hou, Xinxin Ma, Sijin Jiang, Pu Li, Jia Lv, Bei Han, Rong Da
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1259472/full
_version_ 1827786358817554432
author Yi Zhou
Yue Cheng
Tianyou Ma
Jun Wang
Jun Wang
Shaoru Li
Jingdan Wang
Lei Han
Xinyao Hou
Xinxin Ma
Sijin Jiang
Pu Li
Jia Lv
Bei Han
Rong Da
author_facet Yi Zhou
Yue Cheng
Tianyou Ma
Jun Wang
Jun Wang
Shaoru Li
Jingdan Wang
Lei Han
Xinyao Hou
Xinxin Ma
Sijin Jiang
Pu Li
Jia Lv
Bei Han
Rong Da
author_sort Yi Zhou
collection DOAJ
description IntroductionAn extended-spectrum beta-lactamase (ESBL)-hypervirulent Klebsiella pneumoniae (HvKP) strain HKE9 was isolated from the blood in an outpatient.MethodsThe effect of the global regulatory factor RpoS on antimicrobial resistance, pathogenicity, and environmental adaptability was elucidated.ResultsHKE9 is a novel ST3355 (K20/O2a) hypervirulent strain with a positive string test and resistant to cephems except cefotetan. It has a genome size of 5.6M, including two plasmids. CTX-M-15 was found in plasmid 2, and only ompk37 was found in the chromosome. HKE9 could produce bacterial siderophores, and genes of enterobactin, yersiniabactin, aerobactin, and salmochelin have been retrieved in the genome. As a global regulatory factor, knockout of rpoS did not change antimicrobial resistance or hemolytic phenotype while increasing the virulence to Galleria mellonella larvae and showing higher viscosity. Moreover, rpoS knockout can increase bacterial competitiveness and cell adhesion ability. Interestingly, HKE9-M-rpoS decreased resistance to acidic pH, high osmotic pressure, heat shock, and ultraviolet and became sensitive to disinfectants (H2O2, alcohol, and sodium hypochlorite). Although there were 13 Type 6 secretion system (T6SS) core genes divided into two segments with tle1 between segments in the chromosome, transcriptomic analysis showed that rpoS negatively regulated T4SS located on plasmid 2, type 1, and type 3 fimbriae and positively regulate genes responsible for acidic response, hyperosmotic pressure, heat shock, oxidative stress, alcohol and hypochlorous acid metabolism, and quorum sensing.DiscussionHere, this novel ST3355 ESBL-HvKP strain HKE9 may spread via various clonal types. The important regulation effect of rpoS is the enhanced tolerance and resistance to environmental stress and disinfectants, which may be at the cost of reducing virulence and regulated by T4SS.
first_indexed 2024-03-11T16:33:19Z
format Article
id doaj.art-7fca79b43707425695a984fbf400bd8a
institution Directory Open Access Journal
issn 2235-2988
language English
last_indexed 2024-03-11T16:33:19Z
publishDate 2023-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular and Infection Microbiology
spelling doaj.art-7fca79b43707425695a984fbf400bd8a2023-10-23T21:04:19ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-10-011310.3389/fcimb.2023.12594721259472Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolateYi Zhou0Yue Cheng1Tianyou Ma2Jun Wang3Jun Wang4Shaoru Li5Jingdan Wang6Lei Han7Xinyao Hou8Xinxin Ma9Sijin Jiang10Pu Li11Jia Lv12Bei Han13Rong Da14School of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaDepartment of Microbiology Laboratory, Tongchuan Center for Disease Control and Prevention, Tongchuan, Shaanxi, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Basic Medicine, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaSchool of Public Health, Health Science Center, Xi’an Jiaotong University, Xi’an, ChinaDepartment of Clinical Laboratory, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, ChinaIntroductionAn extended-spectrum beta-lactamase (ESBL)-hypervirulent Klebsiella pneumoniae (HvKP) strain HKE9 was isolated from the blood in an outpatient.MethodsThe effect of the global regulatory factor RpoS on antimicrobial resistance, pathogenicity, and environmental adaptability was elucidated.ResultsHKE9 is a novel ST3355 (K20/O2a) hypervirulent strain with a positive string test and resistant to cephems except cefotetan. It has a genome size of 5.6M, including two plasmids. CTX-M-15 was found in plasmid 2, and only ompk37 was found in the chromosome. HKE9 could produce bacterial siderophores, and genes of enterobactin, yersiniabactin, aerobactin, and salmochelin have been retrieved in the genome. As a global regulatory factor, knockout of rpoS did not change antimicrobial resistance or hemolytic phenotype while increasing the virulence to Galleria mellonella larvae and showing higher viscosity. Moreover, rpoS knockout can increase bacterial competitiveness and cell adhesion ability. Interestingly, HKE9-M-rpoS decreased resistance to acidic pH, high osmotic pressure, heat shock, and ultraviolet and became sensitive to disinfectants (H2O2, alcohol, and sodium hypochlorite). Although there were 13 Type 6 secretion system (T6SS) core genes divided into two segments with tle1 between segments in the chromosome, transcriptomic analysis showed that rpoS negatively regulated T4SS located on plasmid 2, type 1, and type 3 fimbriae and positively regulate genes responsible for acidic response, hyperosmotic pressure, heat shock, oxidative stress, alcohol and hypochlorous acid metabolism, and quorum sensing.DiscussionHere, this novel ST3355 ESBL-HvKP strain HKE9 may spread via various clonal types. The important regulation effect of rpoS is the enhanced tolerance and resistance to environmental stress and disinfectants, which may be at the cost of reducing virulence and regulated by T4SS.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1259472/fullhypervirulent Klebsiella pneumoniaeESBLspathogenomicrpoSvirulenceenvironmental stress and disinfectants tolerance
spellingShingle Yi Zhou
Yue Cheng
Tianyou Ma
Jun Wang
Jun Wang
Shaoru Li
Jingdan Wang
Lei Han
Xinyao Hou
Xinxin Ma
Sijin Jiang
Pu Li
Jia Lv
Bei Han
Rong Da
Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolate
Frontiers in Cellular and Infection Microbiology
hypervirulent Klebsiella pneumoniae
ESBLs
pathogenomic
rpoS
virulence
environmental stress and disinfectants tolerance
title Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolate
title_full Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolate
title_fullStr Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolate
title_full_unstemmed Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolate
title_short Transcriptomic and phenotype analysis revealed the role of rpoS in stress resistance and virulence of a novel ST3355 ESBL-producing hypervirulent Klebsiella pneumoniae isolate
title_sort transcriptomic and phenotype analysis revealed the role of rpos in stress resistance and virulence of a novel st3355 esbl producing hypervirulent klebsiella pneumoniae isolate
topic hypervirulent Klebsiella pneumoniae
ESBLs
pathogenomic
rpoS
virulence
environmental stress and disinfectants tolerance
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1259472/full
work_keys_str_mv AT yizhou transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT yuecheng transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT tianyouma transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT junwang transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT junwang transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT shaoruli transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT jingdanwang transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT leihan transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT xinyaohou transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT xinxinma transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT sijinjiang transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT puli transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT jialv transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT beihan transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate
AT rongda transcriptomicandphenotypeanalysisrevealedtheroleofrposinstressresistanceandvirulenceofanovelst3355esblproducinghypervirulentklebsiellapneumoniaeisolate