Emergence of high-level colistin resistance mediated by multiple determinants, including mcr-1.1, mcr-8.2 and crrB mutations, combined with tigecycline resistance in an ST656 Klebsiella pneumoniae

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Abstract

Colistin and tigecycline are usually regarded as the last resort for multidrug-resistant Klebsiella pneumoniae infection treatment. Emergence of colistin and tigecycline resistance poses a global healthcare challenge and is associated with high mortality due to limited therapeutic options. Here, we report the ST656 extensively drug-resistant K. pneumoniae strain KP15-652, which was isolated from a patient’s urine in China. Antimicrobial susceptibility testing showed it to be resistant to tigecycline, amikacin, levofloxacin, ciprofloxacin, and high-level colistin resistance (> 2048 mg/L). Whole-genome sequencing revealed that it harbors one chromosome and seven plasmids, including four plasmids carrying multiple acquired resistance genes. Transformation/conjugation tests and plasmid curing assays confirmed that mcr-1.1, mcr-8.2 and crrB mutations are responsible for the high-level colistin resistance and that a series of efflux pump genes, such as tmexCD1-toprJ1, tet(A) and tet(M), contribute to tigecycline resistance. mcr-1.1 and tet(M) are located on an IncX1 plasmid, which has conjugation transfer potential. mcr-8.2 and tet(A) are located on a multireplicon IncR/IncN plasmid but unable to be transferred via conjugation. Moreover, another conjugable and fusion plasmid carries the tmexCD1-toprJ1 gene cluster, which may have arisen due to IS 26-mediated replicative transposition based on 8-bp target-site duplications. Importantly, a complex class 1 integron carrying various resistance genes was detected on this fusion plasmid. In conclusion, it is possible that the high-level of colistin resistance is caused by the accumulated effect of several factors on the chromosome and mcr-carrying plasmids, combined with many other resistances, including tigecycline. Effective surveillance should be performed to prevent further dissemination.

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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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NCBI prokaryotic genome annotation pipeline

Tatiana Tatusova, Michael DiCuccio, Azat Badretdin … (2016)

Recent technological advances have opened unprecedented opportunities for large-scale sequencing and analysis of populations of pathogenic species in disease outbreaks, as well as for large-scale diversity studies aimed at expanding our knowledge across the whole domain of prokaryotes. To meet the challenge of timely interpretation of structure, function and meaning of this vast genetic information, a comprehensive approach to automatic genome annotation is critically needed. In collaboration with Georgia Tech, NCBI has developed a new approach to genome annotation that combines alignment based methods with methods of predicting protein-coding and RNA genes and other functional elements directly from sequence. A new gene finding tool, GeneMarkS+, uses the combined evidence of protein and RNA placement by homology as an initial map of annotation to generate and modify ab initio gene predictions across the whole genome. Thus, the new NCBI's Prokaryotic Genome Annotation Pipeline (PGAP) relies more on sequence similarity when confident comparative data are available, while it relies more on statistical predictions in the absence of external evidence. The pipeline provides a framework for generation and analysis of annotation on the full breadth of prokaryotic taxonomy. For additional information on PGAP see https://www.ncbi.nlm.nih.gov/genome/annotation_prok/ and the NCBI Handbook, https://www.ncbi.nlm.nih.gov/books/NBK174280/.

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In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.

Alessandra Carattoli, Ea Zankari, Aurora García-Fernández … (2014)

In the work presented here, we designed and developed two easy-to-use Web tools for in silico detection and characterization of whole-genome sequence (WGS) and whole-plasmid sequence data from members of the family Enterobacteriaceae. These tools will facilitate bacterial typing based on draft genomes of multidrug-resistant Enterobacteriaceae species by the rapid detection of known plasmid types. Replicon sequences from 559 fully sequenced plasmids associated with the family Enterobacteriaceae in the NCBI nucleotide database were collected to build a consensus database for integration into a Web tool called PlasmidFinder that can be used for replicon sequence analysis of raw, contig group, or completely assembled and closed plasmid sequencing data. The PlasmidFinder database currently consists of 116 replicon sequences that match with at least at 80% nucleotide identity all replicon sequences identified in the 559 fully sequenced plasmids. For plasmid multilocus sequence typing (pMLST) analysis, a database that is updated weekly was generated from www.pubmlst.org and integrated into a Web tool called pMLST. Both databases were evaluated using draft genomes from a collection of Salmonella enterica serovar Typhimurium isolates. PlasmidFinder identified a total of 103 replicons and between zero and five different plasmid replicons within each of 49 S. Typhimurium draft genomes tested. The pMLST Web tool was able to subtype genomic sequencing data of plasmids, revealing both known plasmid sequence types (STs) and new alleles and ST variants. In conclusion, testing of the two Web tools using both fully assembled plasmid sequences and WGS-generated draft genomes showed them to be able to detect a broad variety of plasmids that are often associated with antimicrobial resistance in clinically relevant bacterial pathogens. Copyright © 2014, American Society for Microbiology. All Rights Reserved.

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Author and article information

Contributors

Haiyang Liu: URI : https://loop.frontiersin.org/people/427446

Dongdong Zhao: URI : https://loop.frontiersin.org/people/1453362

Xueqing Wu: URI : https://loop.frontiersin.org/people/354129

Yunsong Yu: URI : https://loop.frontiersin.org/people/277905

Yan Jiang: URI : https://loop.frontiersin.org/people/1144504

Journal

Journal ID (nlm-ta): Front Cell Infect Microbiol

Journal ID (iso-abbrev): Front Cell Infect Microbiol

Journal ID (publisher-id): Front. Cell. Infect. Microbiol.

Title: Frontiers in Cellular and Infection Microbiology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 2235-2988

Publication date (Electronic): 26 January 2023

Publication date Collection: 2023

Volume: 13

Electronic Location Identifier: 1122532

Affiliations

[1] ¹ Department of Infectious Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou, China

[2] ² Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province , Hangzhou, China

[3] ³ Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou, China

[4] ⁴ Department of General Practice, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou, China

Author notes

Edited by: Biao Tang, Zhejiang Academy of Agricultural Sciences, China

Reviewed by: Fupin Hu, Fudan University, China; Ruichao Li, Yangzhou University, China; Tieli Zhou, First Affiliated Hospital of Wenzhou Medical University, China

*Correspondence: Yan Jiang, jiangy@ 123456zju.edu.cn ; Yunsong Yu, yvys119@ 123456zju.edu.cn

†These authors have contributed equally to this work and share first authorship

This article was submitted to Antibiotic Resistance and New Antimicrobial drugs, a section of the journal Frontiers in Cellular and Infection Microbiology

Article

DOI: 10.3389/fcimb.2023.1122532

PMC ID: 9909390

PubMed ID: 36779188

SO-VID: 70fa7efd-5a31-4740-b39b-f2b9d9e5a8f5

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 13 December 2022

Date accepted : 16 January 2023

Page count

Figures: 5, Tables: 1, Equations: 0, References: 41, Pages: 10, Words: 4429

Funding

Funded by: National Natural Science Foundation of China , doi 10.13039/501100001809;

Award ID: 32141001, 81802043, 81902102, 81830069

This work was supported by National Natural Science Foundation of China (32141001, 82172307, 81902102, 81830069).

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Convergence of plasmid-mediated Colistin and Tigecycline resistance in Klebsiella pneumoniae
Authors: Yujie Zhao, Changrui Qian, Jianzhong Ye …

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Emergence of high-level colistin resistance mediated by multiple determinants, including mcr-1.1, mcr-8.2 and crrB mutations, combined with tigecycline resistance in an ST656 Klebsiella pneumoniae

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Most cited references 41

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

NCBI prokaryotic genome annotation pipeline

In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing.

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