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Genetic Analysis of mcr-1-Carrying Plasmids From Gram-Negative Bacteria in a Dutch Tertiary Care Hospital: Evidence for Intrapatient and Interspecies Transmission Events.

ABSTRACT: The role of plasmids in the complex pandemic of antimicrobial resistance is increasingly being recognized. In this respect, multiple mobile colistin resistance (mcr) gene-carrying plasmids have been described. However, the characteristics and epidemiology of these plasmids within local healthcare settings are largely unknown. We retrospectively characterized the genetic composition and epidemiology of plasmids from mcr-1-positive bacterial isolates identified from patients from a large academic hospital in the Netherlands. Clinical Gram-negative bacteria with an MIC > 2 μg/mL for colistin, obtained from patients hospitalized at the Erasmus MC University Medical Center Rotterdam during the years 2010-2018, were screened for presence of the mcr-1 gene. Extracted plasmids from mcr-1-positive isolates were sequenced using a combination of short- and long-read sequencing platforms, characterized by incompatibility type and genetic composition and compared to publicly available mcr-1-carrying plasmid sequences. In 21 isolates from 14 patients, mcr-1 was located on a plasmid. These plasmids were of diverse genetic background involving Inc types IncX4, IncI2(delta), IncHI2, as well as double Inc types IncHI2/IncN and IncHI2/IncQ. mcr-1-carrying plasmids were found in Escherichia coli, Klebsiella pneumoniae, and Kluyvera georgiana, and within the chromosome of an ST147 K. pneumoniae isolate. In depth analysis indicated intrapatient, interpatient, and interspecies transmission events of mcr-1-carrying plasmids. In addition, our results show that the mcr-1 gene resides in a rich environment full of other (mcr-1 negative) plasmids and of many different Inc types, enabling interplasmidal transfer events and facilitating widespread dissemination of the mcr-1 gene. Multiple mcr-1-carrying plasmid transmission events had likely occurred among isolates from hospitalized patients. Recognition and identification of plasmid transmission events within hospitals is necessary in order to design and implement effective infection control measures.

SUBMITTER: Strepis N

PROVIDER: S-EPMC8450869 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The global dissemination of the mobile colistin resistance (mcr) gene illustrates how the use of colistin in veterinary medicine can affect human health, exemplifying the concept of One Health. This study screened for the existence of mcr variants (from mcr-1 to mcr-10) in a 5-year collection of clinical Klebsiella short-read whole-genome sequencing (WGS) data from a tertiary hospital in China (2013 to 2018) and aimed to identify the mechanisms of mcr spread. MICs were measured for the mcr-positive isolates, and long-read sequencing was performed to complete the mcr-positive genome sequences. Six variants (mcr-1.1, mcr-8.1, mcr-8.2, mcr-9.1, mcr-9.2, and mcr-10.1) were identified in 20 genomes, with plasmids from the IncFIIK, IncHI2, IncI2, and IncX4 groups. Highly similar plasmids (coverage, >75%; nucleotide identity, >98.5%) isolated from silver gulls, chickens, pigs, wastewater treatment plants, and hospital sewage were identified in GenBank. The MICs of the mcr-1- and mcr-8-carrying isolates were ≥4 μg/mL; however, the MICs of the mcr-9- and mcr-10-carrying isolates ranged from 0.5 μg/mL to 1 μg/mL (colistin susceptible). The variants mcr-1 to mcr-9 were found only in Klebsiella pneumoniae, while mcr-10.1 was found in K. pneumoniae, Klebsiella quasipneumoniae subsp. quasipneumoniae, and Klebsiella variicola. A pair of inverted repeats (IRs) was identified for hsdSMR-ISEc36-mcr-10.1-xerC; IR-1 (5'-TCAAACGTA) was inside the attL site of xerC, indicating that mcr-10.1 was originally integrated by xerC and mobilized by ISEc36 afterwards. In conclusion, this is the first report of mcr-10.1 susceptible to colistin in three species of Klebsiella. This study shows the genetic events that happened to mcr-10.1 in a stepwise manner, with the first step being XerC integration and the second being ISEc36 mobilization. Finally, this study also highlights mcr transmission between humans and nature. IMPORTANCE Reports of mcr-1 and mcr-8 are common in China; however, few studies have reported mcr-9 and mcr-10. One reason is that the newly described variants can be phenotypically colistin susceptible and thus may not be identified. This study identified the mcr-positive clinical isolates by investigating WGS data for 2,855 Klebsiella isolates (including K. pneumoniae, K. quasipneumoniae subsp. quasipneumoniae, and K. variicola) and found three mcr-9 and three mcr-10 cases (MICs, 0.5 μg/mL to 1 μg/mL; colistin susceptible). This study also reveals a pair of perfect 9-bp IRs of ISEc36 and the precise mcr-10.1 integration and insertion events that happened to the IncFIIK plasmids. A One Health analysis of highly similar plasmid structures from human and nonhuman sources emphasizes the plasmid transmission and evolution process.

Dataset Information

Genetic Analysis of mcr-1-Carrying Plasmids From Gram-Negative Bacteria in a Dutch Tertiary Care Hospital: Evidence for Intrapatient and Interspecies Transmission Events.

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