Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses

PurposeThe type VI system (T6SS) has the potential to be a new virulence factor for hypervirulent Klebsiella pneumoniae (hvKp) strains. This study aimed to characterize the molecular and clinical features of T6SS-positive and T6SS-negative K. pneumoniae isolates that cause abscesses.Patients and met...

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Main Authors: Peilin Liu, Awen Yang, Bin Tang, Zhiqian Wang, Zijuan Jian, Yanjun Liu, Jiahui Wang, Baiyun Zhong, Qun Yan, Wenen Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1181701/full
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author Peilin Liu
Awen Yang
Bin Tang
Zhiqian Wang
Zijuan Jian
Yanjun Liu
Jiahui Wang
Jiahui Wang
Baiyun Zhong
Qun Yan
Wenen Liu
Wenen Liu
author_facet Peilin Liu
Awen Yang
Bin Tang
Zhiqian Wang
Zijuan Jian
Yanjun Liu
Jiahui Wang
Jiahui Wang
Baiyun Zhong
Qun Yan
Wenen Liu
Wenen Liu
author_sort Peilin Liu
collection DOAJ
description PurposeThe type VI system (T6SS) has the potential to be a new virulence factor for hypervirulent Klebsiella pneumoniae (hvKp) strains. This study aimed to characterize the molecular and clinical features of T6SS-positive and T6SS-negative K. pneumoniae isolates that cause abscesses.Patients and methodsA total of 169 non-duplicate K. pneumoniae strains were isolated from patients with abscesses in a tertiary hospital in China from January 2018 to June 2022, and clinical data were collected. For all isolates, capsular serotypes, T6SS genes, virulence, and drug resistance genes, antimicrobial susceptibility testing, and biofilm formation assays were assessed. Multilocus sequence typing was used to analyze the genotypes of hvKp. T6SS-positive hvKp, T6SS-negative hvKp, T6SS-positive cKP, and T6SS-negative cKP (n = 4 strains for each group) were chosen for the in vivo Galleria mellonella infection model and in vitro competition experiments to further explore the microbiological characteristics of T6SS-positive K. pneumoniae isolates.ResultsThe positive detection rate for T6SS was 36.1%. The rates of hvKp, seven virulence genes, K1 capsular serotype, and ST23 in T6SS-positive strains were all higher than those in T6SS-negative strains (p < 0.05). Multivariate logistic regression analysis indicated that the carriage of aerobactin (OR 0.01) and wcaG (OR 33.53) were independent risk factors for T6SS-positive strains (p < 0.05). The T6SS-positive strains had a stronger biofilm-forming ability than T6SS-negative strains (p < 0.05). The T6SS-positive and T6SS-negative strains showed no significant differences in competitive ability (p = 0.06). In the in vivo G. mellonella infection model, the T6SS(+)/hvKP group had the worst prognosis. Except for cefazolin and tegacyclin, T6SS-positive isolates displayed a lower rate of antimicrobial resistance to other drugs (p < 0.05). The T6SS-positive isolates were more likely to be acquired from community infections (p < 0.05).ConclusionKlebsiella pneumoniae isolates causing abscesses have a high prevalence of T6SS genes. T6SS-positive K. pneumoniae isolates are associated with virulence, and the T6SS genes may be involved in the hvKp virulence mechanism.
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spelling doaj.art-823154c137bf4ab88ad575c5d5a9c9ea2023-05-17T07:43:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.11817011181701Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscessesPeilin Liu0Awen Yang1Bin Tang2Zhiqian Wang3Zijuan Jian4Yanjun Liu5Jiahui Wang6Jiahui Wang7Baiyun Zhong8Qun Yan9Wenen Liu10Wenen Liu11Department of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaNational Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaDepartment of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan, ChinaNational Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Changsha, Hunan, ChinaPurposeThe type VI system (T6SS) has the potential to be a new virulence factor for hypervirulent Klebsiella pneumoniae (hvKp) strains. This study aimed to characterize the molecular and clinical features of T6SS-positive and T6SS-negative K. pneumoniae isolates that cause abscesses.Patients and methodsA total of 169 non-duplicate K. pneumoniae strains were isolated from patients with abscesses in a tertiary hospital in China from January 2018 to June 2022, and clinical data were collected. For all isolates, capsular serotypes, T6SS genes, virulence, and drug resistance genes, antimicrobial susceptibility testing, and biofilm formation assays were assessed. Multilocus sequence typing was used to analyze the genotypes of hvKp. T6SS-positive hvKp, T6SS-negative hvKp, T6SS-positive cKP, and T6SS-negative cKP (n = 4 strains for each group) were chosen for the in vivo Galleria mellonella infection model and in vitro competition experiments to further explore the microbiological characteristics of T6SS-positive K. pneumoniae isolates.ResultsThe positive detection rate for T6SS was 36.1%. The rates of hvKp, seven virulence genes, K1 capsular serotype, and ST23 in T6SS-positive strains were all higher than those in T6SS-negative strains (p < 0.05). Multivariate logistic regression analysis indicated that the carriage of aerobactin (OR 0.01) and wcaG (OR 33.53) were independent risk factors for T6SS-positive strains (p < 0.05). The T6SS-positive strains had a stronger biofilm-forming ability than T6SS-negative strains (p < 0.05). The T6SS-positive and T6SS-negative strains showed no significant differences in competitive ability (p = 0.06). In the in vivo G. mellonella infection model, the T6SS(+)/hvKP group had the worst prognosis. Except for cefazolin and tegacyclin, T6SS-positive isolates displayed a lower rate of antimicrobial resistance to other drugs (p < 0.05). The T6SS-positive isolates were more likely to be acquired from community infections (p < 0.05).ConclusionKlebsiella pneumoniae isolates causing abscesses have a high prevalence of T6SS genes. T6SS-positive K. pneumoniae isolates are associated with virulence, and the T6SS genes may be involved in the hvKp virulence mechanism.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1181701/fulltype VI system (T6SS)hypervirulent Klebsiella pneumoniae (hvKP)abscesshypervirulentvirulence
spellingShingle Peilin Liu
Awen Yang
Bin Tang
Zhiqian Wang
Zijuan Jian
Yanjun Liu
Jiahui Wang
Jiahui Wang
Baiyun Zhong
Qun Yan
Wenen Liu
Wenen Liu
Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses
Frontiers in Microbiology
type VI system (T6SS)
hypervirulent Klebsiella pneumoniae (hvKP)
abscess
hypervirulent
virulence
title Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses
title_full Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses
title_fullStr Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses
title_full_unstemmed Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses
title_short Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses
title_sort molecular epidemiology and clinical characteristics of the type vi secretion system in klebsiella pneumoniae causing abscesses
topic type VI system (T6SS)
hypervirulent Klebsiella pneumoniae (hvKP)
abscess
hypervirulent
virulence
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1181701/full
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