Whole-genome sequence analysis of clinically isolated carbapenem resistant <i>Escherichia coli</i> from Iran

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Abstract

Background

The emergence of carbapenem-resistant Enterobacterales (CRE) continues to threaten public health due to limited therapeutic options. In the current study the incidence of carbapenem resistance among the 104 clinical isolates of Escherichia coli and the genomic features of carbapenem resistant isolates were investigated.

Methods

The susceptibility to imipenem, tigecycline and colistin was tested by broth dilution method. Susceptibility to other classes of antimicrobials was examined by disk diffusion test. The presence of bla _OXA-48, bla _KPC, bla _NDM, and bla _VIM carbapenemase genes was examined by PCR. Molecular characteristics of carbapenem resistant isolates were further investigated by whole-genome sequencing (WGS) using Illumina and Nanopore platforms.

Results

Four isolates (3.8%) revealed imipenem MIC of ≥32 mg/L and positive results for modified carbapenem inactivation method and categorized as carbapenem resistant E. coli (CREC). Colistin, nitrofurantoin, fosfomycin, and tigecycline were the most active agents against all isolates (total susceptibility rate of 99, 99, 96 and 95.2% respectively) with the last three compounds being found as the most active antimicrobials for carbapenem resistant isolates (susceptibility rate of 100%). According to Multilocus Sequence Type (MLST) analysis the 4 CREC isolates belonged to ST167 ( n = 2), ST361 ( n = 1) and ST648 ( n = 1). NDM was detected in all CREC isolates (NDM-1 ( n = 1) and NMD-5 ( n = 3)) among which one isolate co-harbored NDM-5 and OXA-181 carbapenemases. WGS further detected bla _CTX-M-15, bla _CMY-145, bla _CMY-42 and bla _TEM-1 (with different frequencies) among CREC isolates. Co-occurrence of NDM-type carbapenemase and 16S rRNA methyltransferase RmtB and RmtC was found in two isolates belonging to ST167 and ST648. A colistin-carbapenem resistant isolate which was mcr-negative, revealed various amino acid substitutions in PmrB, PmrD and PhoPQ proteins.

Conclusion

About 1.9% of E. coli isolates studied here were resistant to imipenem, colistin and/or amikacin which raises the concern about the outbreaks of difficult-to-treat infection by these emerging superbugs in the future.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12866-023-02796-y.

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Most cited references 36

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Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel (2014)

Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.

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Prokka: rapid prokaryotic genome annotation.

T Seemann (2014)

The multiplex capability and high yield of current day DNA-sequencing instruments has made bacterial whole genome sequencing a routine affair. The subsequent de novo assembly of reads into contigs has been well addressed. The final step of annotating all relevant genomic features on those contigs can be achieved slowly using existing web- and email-based systems, but these are not applicable for sensitive data or integrating into computational pipelines. Here we introduce Prokka, a command line software tool to fully annotate a draft bacterial genome in about 10 min on a typical desktop computer. It produces standards-compliant output files for further analysis or viewing in genome browsers. Prokka is implemented in Perl and is freely available under an open source GPLv2 license from http://vicbioinformatics.com/. © The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.

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Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads

Ryan Wick, Louise Judd, Claire Gorrie … (2017)

The Illumina DNA sequencing platform generates accurate but short reads, which can be used to produce accurate but fragmented genome assemblies. Pacific Biosciences and Oxford Nanopore Technologies DNA sequencing platforms generate long reads that can produce complete genome assemblies, but the sequencing is more expensive and error-prone. There is significant interest in combining data from these complementary sequencing technologies to generate more accurate “hybrid” assemblies. However, few tools exist that truly leverage the benefits of both types of data, namely the accuracy of short reads and the structural resolving power of long reads. Here we present Unicycler, a new tool for assembling bacterial genomes from a combination of short and long reads, which produces assemblies that are accurate, complete and cost-effective. Unicycler builds an initial assembly graph from short reads using the de novo assembler SPAdes and then simplifies the graph using information from short and long reads. Unicycler uses a novel semi-global aligner to align long reads to the assembly graph. Tests on both synthetic and real reads show Unicycler can assemble larger contigs with fewer misassemblies than other hybrid assemblers, even when long-read depth and accuracy are low. Unicycler is open source (GPLv3) and available at github.com/rrwick/Unicycler.

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Author and article information

Contributors

Mehri Haeili: m.haeili@tabrizu.ac.ir , m.haeili@yahoo.com

Arash Ghodousi: ghodousi.arash@hsr.it

Journal

Journal ID (nlm-ta): BMC Microbiol

Journal ID (iso-abbrev): BMC Microbiol

Title: BMC Microbiology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2180

Publication date (Electronic): 27 February 2023

Publication date PMC-release: 27 February 2023

Publication date Collection: 2023

Volume: 23

Electronic Location Identifier: 49

Affiliations

[1 ]GRID grid.412831.d, ISNI 0000 0001 1172 3536, Department of Animal Biology, Faculty of Natural Sciences, , University of Tabriz, ; Tabriz, Iran

[2 ]GRID grid.18887.3e, ISNI 0000000417581884, IRCCS San Raffaele Scientific Institute, ; Milan, Italy

[3 ]GRID grid.412888.f, ISNI 0000 0001 2174 8913, Drug Applied Research Center, Faculty of Medicine, , Tabriz University of Medical Sciences, ; Tabriz, Iran

[4 ]GRID grid.18887.3e, ISNI 0000000417581884, Emerging Bacterial Pathogens Unit, Division of Immunology, , Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific Institute, ; Milan, Italy

[5 ]GRID grid.15496.3f, ISNI 0000 0001 0439 0892, Vita-Salute San Raffaele University, ; Milan, Italy

Article

Publisher ID: 2796

DOI: 10.1186/s12866-023-02796-y

PMC ID: 9969672

PubMed ID: 36850019

SO-VID: 4402d02f-0c15-445e-94e4-9e690870c602

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 29 September 2022

Date accepted : 16 February 2023

Custom metadata

ScienceOpen disciplines: Microbiology & Virology

Keywords: carbapenem resistance,escherichia coli,ndm-1,ndm-5,whole genome sequencing,epidemiology

Data availability:

ScienceOpen disciplines: Microbiology & Virology

Keywords: carbapenem resistance, escherichia coli, ndm-1, ndm-5, whole genome sequencing, epidemiology

Whole-genome sequence analysis of clinically isolated carbapenem resistant Escherichia coli from Iran

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Abstract

Background

Methods

Results

Conclusion

Supplementary Information

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Microbial Genomics

Most cited references 36

Trimmomatic: a flexible trimmer for Illumina sequence data

Prokka: rapid prokaryotic genome annotation.

Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads

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