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Sequential Isolation in a Patient of Raoultella Planticola And Sequential Isolation in a Patient of Raoultella planticola and Escherichia coli Bearing a Novel ISCR1 Element Carrying blaNDM-1 Juan Li1., Ruiting Lan2., Yanwen Xiong1., Changyun Ye1., Min Yuan1, Xinfeng Liu3, Xia Chen1, Deshan Yu3, Bin Liu4, Wenchao Lin4, Xuemei Bai1, Yan Wang1, Qiangzheng Sun1, Yiting Wang1, Hongqing Zhao1, Qiong Meng1, Qiang Chen1, Ailan Zhao1, Jianguo Xu1* 1 State Key Laboratory for Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, National Institute for Communicable Disease Control and Prevention, China CDC, Changping, Beijing, China, 2 School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, Australia, 3 Gansu Provincial Center for Disease Control and Prevention, Lanzhou, Gansu Province, China, 4 College of Life Sciences, Nankai University, Tianjin, China Abstract Background: The gene for New Delhi metallo-b-lactamase 1 (NDM-1) has been reported to be transmitted via plasmids which are easily transferable and capable of wide distribution. We report the isolation of two NDM-1 producing strains and possible in vivo transfer of blaNDM-1 in a patient. Methods: Clinical samples were collected for bacterial culture and antibiotic susceptibility testing from a patient during a 34-day hospitalization. The presence of blaNDM-1 was detected by PCR and sequencing. Plasmids of interest were sequenced. Medical records were reviewed for evidence of association between the administration of antibiotics and the acquisition of the NDM-1 resistance. Results: A NDM-1 positive Raoultella planticola was isolated from blood on the ninth day of hospitalization without administration of any carbapenem antibiotics and a NDM-1 positive Escherichia coli was isolated from feces on the 29th day of hospitalization and eight days after imipenem administration. The blaNDM-1 was carried by a 280 kb plasmid pRpNDM1-1 in R. planticola and a 58 kb plasmid pEcNDM1-4 in E. coli. The two plasmids shared a 4812 bp NDM-1-ISCR1 element which was found to be excisable from the plasmid as a free form and transferrable in vitro to a NDM-1 negative plasmid from E. coli. Conclusion: blaNDM-1 was embedded in an ISCR1 complex class 1 integron as a novel 4812 bp NDM-1-ISCR1 element. The element was found to be able to self excise to become a free form, which may provide a new vehicle for NDM-1 dissemination. This mechanism could greatly accelerate the spread of NDM-1 mediated broad spectrum b-lactam resistance. Citation: Li J, Lan R, Xiong Y, Ye C, Yuan M, et al. (2014) Sequential Isolation in a Patient of Raoultella planticola and Escherichia coli Bearing a Novel ISCR1 Element Carrying blaNDM-1. PLoS ONE 9(3): e89893. doi:10.1371/journal.pone.0089893 Editor: Finbarr Hayes, University of Manchester, United Kingdom Received October 8, 2013; Accepted January 23, 2014; Published March 3, 2014 Copyright: ß 2014 Li et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the State Key Laboratory for Infectious Disease Prevention and Control of China [grant number 2012SKLID205] and the Priority Project on Infectious Disease Control and Prevention [grant number 2013ZX10004217] from the Ministry of Health and the Ministry of Science and Technology. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] . These authors contributed equally to this work. Introduction NDM-1 was first identified in a carbapenem-resistant Klebsiella pneumoniae strain isolated from urine and an Escherichia coli strain Carbapenems often represent last-resource drugs for Gram isolated from feces of the same patient that was resistant to almost negative bacterial infections. The most common mechanism of all antibiotics tested except colistin and tigecycline in 2009 in carbapenem resistance in Gram negative bacteria is the produc- Sweden [3]. NDM-1 positive K. pneuomoniae and E. coli were soon tion of carbapenemases, including metallo-b-lactamases (MBLs). detected in many other countries, including Australia, Canada, The New Delhi metallo-beta-lactamase (NDM-1), a recently Germany, China, France, Japan, the Nordic countries, United identified novel type of MBL can hydrolyze virtually all b-lactams, States and many others [4–8]. In addition, reported NDM-1 adding further burden to an already high level of antibiotic positive bacterial species extended to Acinetobacter spp, Citrobacter resistance. The emergence and global spread of NDM-1 mediated freundii, Enterobacter cloacae, Morganella morganii, Providencia spp, and broad spectrum b-lactam resistance has become a major concern Pseudomonas aeruginosa [9–11]. The world has been alarmed by the worldwide [1,2]. wide dissemination of NDM-1 isolates, for which new and effective PLOS ONE | www.plosone.org 1 March 2014 | Volume 9 | Issue 3 | e89893 A Novel ISCR1 Element Accelerates NDM-1 Transfer antibiotics are currently unavailable. The gene blaNDM-1 encoding fecal samples was analyzed by PFGE (Pulsed Field Gel Electro- NDM-1 has been mostly reported to be on plasmids, which could phoresis)-Xba I digestion method, following the protocol previously rapidly disseminate and spread between different bacterial species described [20]. by cell-to-cell transfer of the plasmids. However the plasmids carrying blaNDM-1 are different in sizes, ranging from 40 kb to PCR primers and detection of blaNDM-1 400 kb [9], suggesting that direct transfer by plasmid is only one PCR primers for detecting blaNDM-1 and for confirming the means of NDM-1 dissemination. Multiple mobile genetic elements genetic environment of the blaNDM-1 are listed in Table S1 in File are also associated with blaNDM-1 dissemination [4,11,12]. S1. Plasmids were analyzed and sized by the PFGE-S1 nuclease The insertion sequence common region 1 (ISCR1) is a well method [21]. Separation of large fragments from restriction recognized system of gene capture. Its role in antibiotic resistance enzyme digestion was done with PFGE by using of a CHEF-DR dissemination was first noted by the evidence that a wide variety of III apparatus (Bio-Rad, Hercules, CA) for 7 h at 6 V/cm and antimicrobial determinants are found in the immediate vicinity of 14uC with initial and final pulse times of 5 s and 20 s, respectively. ISCR1 [13,14]. ISCR1 is capable of mobilizing its upstream Southern hybridization was performed with a 560 bp segment of sequences by a process of rolling circle transposition [15]. the blaNDM-1 gene as a probe using the ECL direct nucleic acid Association of the ISCR1 element with blaNDM-1 has been observed labeling and detection system (GE Healthcare, Buckinghamshire, in plasmids pNDM-HK(HQ451074) [16], pMR0211(JN687470) UK). [17] and in K. pneumoniae strain 05-506 [3] and P. aeruginosa [18]. However the role of the ISCR1 element in the transfer of the NDM-1 within and between bacterial species is unclear. Conjugation and transformation of blaNDM-1 plasmids Conjugation experiments were carried out by the solid surface Here, we report that we identified two strains of different species r (Raoultella planticola and E. coli) carrying NDM-1 isolated 20 days methods with E. coli J53 Az as the recipient [4]. Transconjugants were selected on Luria-Bertani agar plates containing sodium apart from the same patient and showed that blaNDM-1 was located azide (100 mg/L) and ampicillin (100 mg/L), confirmed by PCR on two unrelated plasmids. The blaNDM-1 was embedded in an ISCR1 complex class 1 integron, which is most likely responsible amplification of the blaNDM-1 for NDM-1 positive donors and bla gene for NDM-1 negative donors and sequencing of the for blaNDM-1 transfer between R. planticola and E. coli in the patient OXA-30 in vivo. PCR products. The plasmid DNA of NDM-1 positive strain E. coli EcNDM1was used for transformation and E. coli JM109 was used Materials and Methods as the recipient. Ethics statement Whole genome sequencing and sequencing of plasmids The feces, urine, sputum and blood samples were obtained with The whole genome of the isolate R. planticola was sequenced the written informed consent from the patient. This study was using a combined strategy of Roche 454 Genome Sequencer FLX reviewed and approved by the ethics committee of the National System (Roche/454 Life Sciences, Branford, CT, USA) and Institute for Communicable Disease Control and Prevention, Illumina sequencing technology (Illumina, San Diego, CA, USA). China CDC, according to the medical research regulations of the The Burrows-Wheeler Alignment (BWA) tool was used to map all Ministry of Health, China. This research was conducted within the Illumina reads to the scaffolds generated by 454 Newbler. The China. inter- and intra-scaffold gaps were filled by local assembly of Roche and Illumina reads. The gaps between contigs were closed The Patient by targeted PCR amplification and sequencing of the PCR The patient was a 51-year-old farmer from a small village of products with BigDye terminator chemistry on an ABI 3730 Gansu Province, who has never visited any cities in China or other capillary sequencer. countries that have reported NDM-1. On October 1, 2010, the Plasmid DNA extracted from E. coli EcNDM1 was transformed patient was admitted to Lanzhou medical school hospital because into E. coli JM109, and a carbapenems resistant transformant of severe multiple left rib fractures as a result of traffic accident. carrying plasmid pEcNDM1-4 named JM109 (pEcNDM1-4) was Surgical operation was performed three hours after the accident. A recovered. Plasmid pEcNDM1-4 extracted from the E.
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