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Resistome and a Novel blaNDM-1-Harboring Plasmid of an Acinetobacter haemolyticus Strain from a Children's Hospital in Puebla, Mexico.

ABSTRACT: Acinetobacter calcoaceticus-baumannii complex isolates have been frequently associated with hospital and community infections, with A. baumannii being the most common. Other Acinetobacter spp. not belonging to this complex also cause infections in hospital settings, and the incidence has increased over the past few years. Some species of the Acinetobacter genus possess a great diversity of antibiotic resistance mechanisms, such as efflux pumps, porins, and resistance genes that can be acquired and disseminated by mobilizable genetic elements. By means of whole-genome sequencing, we describe in the clinical Acinetobacter haemolyticus strain AN54 different mechanisms of resistance that involve blaOXA-265, blaNDM-1, aphA6, aac(6')-Ig, and a resistance-nodulation-cell division-type efflux pump. This strain carries six plasmids, of which the plasmid pAhaeAN54e contains blaNDM-1 in a Tn125-like transposon that is truncated at the 3' end. This strain also has an insertion sequence IS91 and seven genes encoding hypothetical proteins. The pAhaeAN54e plasmid is nontypable and different from other plasmids carrying blaNDM-1 that have been reported in Mexico and other countries. The presence of these kinds of plasmids in an opportunistic pathogen such as A. haemolyticus highlights the role that these plasmids play in the dissemination of antibiotic resistance genes, especially against carbapenems, in Mexican hospitals.

SUBMITTER: Bello-Lopez E

PROVIDER: S-EPMC6743090 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Resistome and a Novel blaNDM-1-Harboring Plasmid of an Acinetobacter haemolyticus Strain from a Children's Hospital in Puebla, Mexico.

Bello-López Elena E Castro-Jaimes Semiramis S Cevallos Miguel Ángel MÁ Rocha-Gracia Rosa Del Carmen RDC Castañeda-Lucio Miguel M Sáenz Yolanda Y Torres Carmen C Gutiérrez-Cazares Zita Z Martínez-Laguna Ygnacio Y Lozano-Zarain Patricia P

Microbial drug resistance (Larchmont, N.Y.) 20190726 7

Acinetobacter calcoaceticus-baumannii complex isolates have been frequently associated with hospital and community infections, with A. baumannii being the most common. Other Acinetobacter spp. not belonging to this complex also cause infections in hospital settings, and the incidence has increased over the past few years. Some species of the Acinetobacter genus possess a great diversity of antibiotic resistance mechanisms, such as efflux pumps, porins, and resistance ...[more]

PMID: 31335270

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Project description:New Delhi metallo-β-lactamase (NDM)-producing clinical strains in Acinetobacter spp. have been recently reported in many countries and have received considerable attention. The vast majority of blaNDM cases occur on conjugative plasmids, which play a vital role in disseminating blaNDM. To characterize the conjugative plasmids bearing blaNDM genes in Acinetobacter spp., we analyzed the variants of blaNDM, conjugative transfer regions, genetic contexts of blaNDM, and the phylogenetic pattern of the 62 predicted blaNDM-positive plasmids, which were selected from 1,191 plasmids of Acinetobacter species from GenBank. We identified 30 conjugative plasmids from the 62 blaNDM-harboring plasmids in Acinetobacter species, with the oriT sites similar to plasmid pNDM-YR7 in our study, genes coding for relaxases of the MOBQ family, genes encoding type IV coupling proteins (T4CPs) of the TrwB/TraD subfamily, and VirB-like type IV secretion system (T4SS) gene clusters. The genome sizes of all 30 pNDM-YR7-like plasmids ranged from 39.36 kb to 49.65 kb, with a median size of 44.56 kb. The most common species of Acinetobacter containing the blaNDM-positive conjugative plasmids was A. baumannii, followed by Acinetobacter lwoffii and Acinetobacter indicus. Notably, pNDM-YR7 is the first report on a blaNDM-positive conjugative plasmid in Acinetobacter junii. Moreover, all 30 blaNDM-positive conjugative plasmids in Acinetobacter species were found to contain genetic contexts with the structure ISAba14-aph(3')-VI-ISAba125-blaNDM-ble. Our findings provide important insights into the phylogeny and evolution of blaNDM-positive plasmids of Acinetobacter species and further address their role in acquiring and spreading blaNDM genes in Acinetobacter species. IMPORTANCE Conjugative plasmids harboring the blaNDM gene play a vital role in disseminating carbapenem resistance. In this study, we first report a conjugative plasmid, pNDM-YR7, in Acinetobacter junii. Based on the genomic characteristics of the blaNDM-positive pNDM-YR7, we performed in silico typing and comparative analysis of blaNDM-positive plasmids using the 1,191 plasmids of Acinetobacter species available in the NCBI RefSeq database. We analyzed the characteristics of blaNDM-positive plasmids, including the variants of blaNDM, genetic features associated with blaNDM, conjugative transfer regions, and the phylogenetic pattern of the blaNDM-positive plasmids. All 30 blaNDM-positive conjugative plasmids were found to contain an ISAba14-aph(3')-VI-ISAba125-blaNDM-ble region. This study provides novel insights into the phylogeny and evolution of blaNDM-harboring conjugative plasmids and contributes to the repertoire of knowledge surrounding blaNDM-positive plasmids in the genus Acinetobacter.

Project description:IncX3 and IncL plasmids have been named as catalysts advancing dissemination of blaOXA-181 and blaOXA-48 genes. However, their impact on the performance of host cells is vastly understudied. Genetic characteristics of blaOXA-48- and blaOXA-181-containing Klebsiella pneumoniae (EFN299), Klebsiella quasipneumoniae (EFN262), and Enterobacter cloacae (EFN743) isolated from clinical samples in a Ghanaian hospital were investigated by whole-genome sequencing. Transfer of plasmids by conjugation and electroporation, plasmid stability, fitness cost, and genetic context of blaOXA-48, blaOXA-181, and blaDHA-1 were assessed. blaOXA-181 was carried on two IncX3 plasmids, an intact 51.5-kb IncX3 plasmid (p262-OXA-181) and a 45.3-kb IncX3 plasmid (p743-OXA-181) without replication protein sequence. The fluoroquinolone-resistant gene qnrS1 region was also excised, and unlike in p262-OXA-181, the blaOXA-181 drug-resistant region was not found on a composite transposon. blaOXA-48 was carried on a 74.6-kb conjugative IncL plasmid with unknown ~10.9-kb sequence insertion. This IncL plasmid proved to be highly transferable, with a conjugation efficiency of 1.8 × 10-2. blaDHA-1 was present on an untypeable 22.2 kb genetic structure. Plasmid stability test revealed plasmid loss rate between 4.3% and 12.4%. The results also demonstrated that carriage of IncX3-blaOXA-181 or IncL-blaOXA-48 plasmids was not associated with any fitness defect, but rather an enhanced competitive ability of host cells. This study underscores the significant contribution of IncX3 and IncL plasmids in the dissemination of resistance genes and their efficient transfer calls for regular monitoring to control the expansion of resistant strains. IMPORTANCE The growing rate of antibiotic resistance is an important global health threat. This threat is exacerbated by the lack of safe and potent alternatives to carbapenems in addition to the slow developmental process of newer and effective antibiotics. Infections by carbapenem-resistant Gram-negative bacteria are becoming almost untreatable, leading to poor clinical outcomes and high mortality rates. OXA-48-like carbapenemases are one of the most widespread carbapenemases accounting for resistance among Enterobacteriaecae. We characterized OXA-48- and OXA-181-producing Enterobacteriaecae to gain insights into the genetic basis and mechanism of resistance to carbapenems. Findings from the study showed that the genes encoding these enzymes were carried on highly transmissible plasmids, one of which had sequences absent in other similar plasmids. This implies that mobile genetic elements are important players in the dissemination of resistance genes. Further characterization of this plasmid is warranted to determine the role of this sequence in the spread of resistance genes.

Project description:Dissemination of blaNDM, which is carried on the IncX3 plasmid, among Enterobacterales has been reported worldwide. In particular, blaNDM-5-carrying IncX3 plasmids can spread among several hosts, facilitating their dissemination. Other variants, such as blaNDM-17-, blaNDM-19-, blaNDM-20-, blaNDM-21-, and blaNDM-33-carrying IncX3 plasmids, have also been reported. Here, we characterized, using whole-genome sequencing (WGS), a blaNDM-16b-carrying IncX3 plasmid harbored by Escherichia coli strain TA8571, which was isolated from a urine specimen of a hospital inpatient in Tokyo, Japan. The blaNDM-16b differed in sequence from blaNDM-5 (C > T at site 698, resulting in an Ala233Val substitution). This blaNDM-16b-carrying IncX3 plasmid (pTMTA8571-1) is 46,161 bp in length and transferred via conjugation. Transconjugants showed high resistance to β-lactam antimicrobials (except for aztreonam). Because pTMTA8571-1, which carries the Tn125-related region containing blaNDM and conjugative transfer genes, was similar to the previously reported IncX3 plasmids, we performed phylogenetic analysis based on the sequence of 34 shared genes in 142 blaNDM-carrying IncX3 plasmids (22,846/46,923 bp). Comparative analysis of the shared genes revealed short branches on the phylogenetic tree (average of 1.08 nucleotide substitutions per shared genes), but each blaNDM variant was divided into separate groups, and the structure of the tree correlated with the flowchart of blaNDM nucleotide substitutions. The blaNDM-carrying IncX3 plasmids may thereby have evolved from the same ancestral plasmid with subsequent mutation of the blaNDM. Therefore, pTMTA8571-1 likely emerged from a blaNDM-5-carrying IncX3 plasmid. This study suggested that the spread of blaNDM-carrying IncX3 plasmids may be a hotbed for the emergence of novel variants of blaNDM. IMPORTANCE blaNDM-carrying IncX3 plasmids have been reported worldwide. Harbored blaNDM variants were mainly blaNDM-5, but there were also rare variants like blaNDM-17, blaNDM-19, blaNDM-20, blaNDM-21, and blaNDM-33, including blaNDM-16b detected in this study. For these plasmids, previous reports analyzed whole genomes or parts of sequences among a small number of samples, whereas, in this study, we performed an analysis of 142 blaNDM-carrying IncX3 plasmids detected around the world. The results showed that regardless of the blaNDM variants, blaNDM-carrying IncX3 plasmids harbored highly similar shared genes. Because these plasmids already spread worldwide may be a hotbed for the emergence of rare or novel variants of blaNDM, increased attention should be paid to blaNDM-carrying IncX3 plasmids in the future.

Dataset Information

Resistome and a Novel blaNDM-1-Harboring Plasmid of an Acinetobacter haemolyticus Strain from a Children's Hospital in Puebla, Mexico.

Publications

Resistome and a Novel <i>bla</i><sub>NDM-1</sub>-Harboring Plasmid of an <i>Acinetobacter haemolyticus</i> Strain from a Children's Hospital in Puebla, Mexico.

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