Whole-Genome Sequencing-Based Species Classification, Multilocus Sequence Typing, and Antimicrobial Resistance Mechanism Analysis of the Enterobacter cloacae Complex in Southern China

Xu, Dong; Zhu, Mei; Li, Yaxuan; Huang, Dawei; Wang, Lan; Yan, Cheng; Zhang, Linhua; Dong, Fubo; Lü, Jing; Lin, Xiangmin; Li, Kewei; Bao, Qiyu; Chen, Cong; Pan, Wei

doi:10.1128/spectrum.02160-22

Cited by 10 publications

(11 citation statements)

References 41 publications

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“…Among these genes, beta-lactamase ACT ( blaACT ), fosfomycin resistance glutathione transferase ( fosA ), and multidrug efflux RND transporters ( oqxA and oqxB ) were consistently found in all strains belonging to the novel Enterobacter species. It is worth mentioning that blaACT genes were the most dominant beta-lactamase genes found among the members of the E. cloacae complex ( 2 ). Additionally, homologs of fosA , which contribute to intrinsic fosfomycin resistance ( 51 ), were present in the majority of genomes of several Enterobacteriaceae species including E. cloacae .…”

Section: Resultsmentioning

confidence: 99%

“…The focus of this study is the Enterobacter cloacae complex (ECC), which comprises several difficult-to-discriminate species of Enterobacter ( 1 ). ECC members are known to include nosocomial pathogens responsible for infections such as pneumonia, septicemia, and urinary tract infections ( 2 ). Additionally, Enterobacter is part of the ESKAPE group and also contains several multidrug-resistant pathogens ( 3 ).…”

Section: Introductionmentioning

confidence: 99%

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Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.

Rahi,

Mühle,

Scandola

et al. 2024

Microbiol Spectr

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Members of the Enterobacter cloacae complex (ECC) are almost ubiquitous in nature and can act as pathogens. In this study, we used a polyphasic taxonomy approach to establish the accurate taxonomic position of six strains within the ECC. Notably, the 16S rRNA gene-based phylogeny failed to group all Enterobacter species into a monophyletic cluster. As an alternative to this, we explored genome sequence-based phylogenetic approaches. The bac120 gene-based phylogeny successfully grouped all Enterobacter species into a monophyletic cluster, although some species-level clustering conflicted with average nucleotide identity (ANI) values. Furthermore, the Enterobacter -specific core gene phylogeny resolved all species, aligning with ANI results. Three strains were identified as Enterobacter asburiae , while strain P99 was classified as “ Enterobacter xiangfangensis ” and strain C45 as Enterobacter quasihormaechei . Conversely, strain A-8 T formed a distinct cluster in all phylogenies, with ANI and digital DNA-DNA hybridization (dDDH) values below the species threshold (<92% and <44%, respectively) with all known Enterobacter species. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry biotyper results confirmed that all strains belonged to the ECC. However, the comparison of mean spectrum profile of strain A-8 T with those of other strains revealed the presence of 18 unique peaks, highlighting its distinct protein profile. Based on comprehensive genotypic and phenotypic characterizations, we propose that strain A-8 T is a new species of the genus Enterobacter , which is named Enterobacter pasteurii sp. nov. The type strain is A-8 T (CIP 103550 T ; ATCC 23355 T ; DSM 26481 T ; and WDCM 00082 T ). This study advances our understanding of the ECC, emphasizing the need for multidimensional taxonomic techniques and contributing to the better management of microbial resource centers. IMPORTANCE Accurate taxonomy is essential for microbial biological resource centers, since the microbial resources are often used to support new discoveries and subsequent research. Here, we used genome sequence data, alongside matrix-assisted laser desorption/ionization time-of-flight mass spectrometer biotyper-based protein profiling, to accurately identify six Enterobacter cloacae complex strains. This approach effectively identified distinct species within the E. cloacae complex, including Enterobacter asburiae , “ Enterobacter xiangfangensis ,” and Enterobacter quasihormaechei . Moreover, the study revealed the existence of a novel species within the Enterobacter genus, for which we proposed the name Enterobacter pasteurii sp. nov. In summary, this study demonstrates the significance of adopting a genome sequence-driven taxonomy approach for the precise identification of bacterial strains in a biological resource center and expands our understanding of the E. cloacae complex.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.

Rahi,

Mühle,

Scandola

et al. 2024

Microbiol Spectr

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“…To date, the mcr-9 gene has been associated with the co-occurrence of carbapenemase genes bla VIM , bla IMP , bla KPC , and bla NDM-1 [10] , [24] , [44] , [45] , however, case reports about co-existence of mcr-10 and carbapenemase genes ECC are still rare. A study has reported that the bla ACT gene was most prevalent among the ECC and its variants ( bla ACT-2 , bla ACT-3 ) were only present in E. asburiae [46] . In our findings, the bla ACT-3 genes were identified in all ST252 E. asburiae , indicating that it serves as a reservoir for bla ACT-3 genes.…”

Section: Discussionmentioning

confidence: 99%

Molecular epidemiology and genomic characterization of a plasmid-mediated mcr-10 and blaNDM-1 co-harboring multidrug-resistant Enterobacter asburiae

Jiang

et al. 2023

Computational and Structural Biotechnology Journal

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“…Resistance in these bacteria is also mediated by high expression of bacterial efflux pumps, decreased expression or loss of membrane pore proteins ompF and ompC, and alteration of drug binding sites. 1 , 11 , 12 Notably, ESBL-producing Enterobacterales were classified as one of the most significant pathogens in the World Health Organization’s list of priority pathogens. 13 , 14 A nationwide survey conducted in China revealed that the prevalence of ESBL-producing Enterobacterales was as high as 40.6%.…”

Section: Introductionmentioning

confidence: 99%

Clinical Characteristics, Prognosis and Treatment of Bloodstream Infections with Enterobacter Cloacae Complex in a Chinese Tertiary Hospital: A Retrospective Study

Liu,

Li,

Fang

et al. 2024

IDR

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Objective This research aimed to analyze the clinical characteristics, prognosis, and antimicrobial treatment of bloodstream infections (BSI) caused by Enterobacter cloacae complex (ECC). Methods The clinical data of patients with bloodstream infections caused by Enterobacter cloacae complex from April 2017 to June 2023 were collected retrospectively. These data were then analyzed in subgroups based on the detection results of extended-spectrum β-lactamase (ESBL), 30-day mortality, and the type of antimicrobial agent used (β-lactam/β-lactamase inhibitor combinations (BLICs) or carbapenems). Results The proportion of ESBL-producing Enterobacter cloacae complex was 32.5% (37/114). Meanwhile, ICU admission, receiving surgical treatment within 3 months, and biliary tract infection were identified as risk factors for ESBL-producing ECC-BSI. Additionally, immunocompromised status and Sequential Organ Failure Assessment (SOFA) score ≥ 6.0 were identified as independent risk factors of 30-day mortality in patients with ECC-BSI (n = 108). Further analysis in BSI patients caused by non-ESBL-producing ECC revealed that patients treated with BLICs (n = 45) had lower SOFA scores and lower incidence of hypoproteinemia and sepsis compared with patients treated with carbapenems (n = 20). Moreover, in non-ESBL-producing ECC-BSI patients, the univariate Cox regression analysis indicated a significantly lower 30-day mortality rate in patients treated with BLICs compared to those treated with carbapenems (hazard ratios (HR) [95% CI] 0.190 [0.055–0.662], P = 0.009; adjusted HR [95% CI] 0.106 [0.013–0.863], P = 0.036). Conclusion This study investigated the factors influencing the susceptibility to infection by ESBL-producing strains and risk factors for 30-day mortality in ECC-BSI patients. The results revealed that ESBL-negative ECC-BSI patients treated with BLICs exhibited significantly lower 30-day mortality compared to those treated with carbapenems. BLICs were found to be more effective in ECC-BSI patients with milder disease (ESBL-negative and SOFA ≤6.0).

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Whole-Genome Sequencing-Based Species Classification, Multilocus Sequence Typing, and Antimicrobial Resistance Mechanism Analysis of the Enterobacter cloacae Complex in Southern China

Cited by 10 publications

References 41 publications

Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.

Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.

Molecular epidemiology and genomic characterization of a plasmid-mediated mcr-10 and blaNDM-1 co-harboring multidrug-resistant Enterobacter asburiae

Clinical Characteristics, Prognosis and Treatment of Bloodstream Infections with Enterobacter Cloacae Complex in a Chinese Tertiary Hospital: A Retrospective Study

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