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      Interrelationship between tetracycline resistance determinants, phylogenetic group affiliation and carriage of class 1 integrons in commensal Escherichia coli isolates from cattle farms

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          Abstract

          Background

          Carriage of antibiotic-resistant foodborne pathogens by food production animals is one of many contributors to treatment failure in health care settings, and it necessitates an integrated approach to investigate the carriage of resistant pathogens harboring integrons in food-producing animals.

          Methods

          Escherichia coli isolates with reduced susceptibility to tetracycline antibiotics ( n = 92) were tested for associations between carriage of class1 integrons, phylogenetic group affiliation and tetracycline resistance determinants using the MIC method, PFGE analysis, PCR and sequencing.

          Results

          Phylogroups B1 and A were the most common (58.7 and 19.6%, respectively), followed by groups D (20.7%) and B2 (1.1%). All isolates carried at least one of the tet genes examined. In addition, 88 (95.7%) of all tetracycline-resistant isolates carried tet(A) or tet(B), while 47 (51.1%) and 41 (44.6%) harbored only tet(A) or tet(B), respectively. Likewise, isolates harboring these genes had a higher chance ( P < 0.05) of carrying class 1 integrons. Of the tested isolates, 38 (41.3%) carried the intI1 gene. Classical integrons with complete genes ( sul1 and qacE∆1) at the 3′-CS were recognized in 27 isolates. PCR screening and subsequent sequencing demonstrated that 84.2% (32/38) of the intI1-positive isolates harbored resistance gene cassettes. Overall, seven gene cassettes were identified, either solely or combined with another gene cassette. The most common gene was aadA1 (10 isolates), followed by a combination of aadA1-dfrA1 (seven isolates), aadA1-dfrA12 (six isolates) and aadA1-aadA2-dfrA12 (three isolates). Genetic typing using PFGE showed minimum clonal relatedness with 28 different clusters and 12–25 discernible DNA fragments.

          Conclusions

          This study brings new insight into the relationships between the presence of integrons, phylogenetic group association and characteristics of tetracycline antibiotic resistance determinants in commensal E. coli strains.

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          Most cited references47

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          Integrons: agents of bacterial evolution.

          Integrons are assembly platforms - DNA elements that acquire open reading frames embedded in exogenous gene cassettes and convert them to functional genes by ensuring their correct expression. They were first identified by virtue of their important role in the spread of antibiotic-resistance genes. More recently, our understanding of their importance in bacterial genome evolution has broadened with the discovery of larger integron structures, termed superintegrons. These DNA elements contain hundreds of accessory genes and constitute a significant fraction of the genomes of many bacterial species. Here, the basic biology of integrons and superintegrons, their evolutionary history and the evidence for the existence of a novel recombination pathway is reviewed.
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            Integrons: past, present, and future.

            Integrons are versatile gene acquisition systems commonly found in bacterial genomes. They are ancient elements that are a hot spot for genomic complexity, generating phenotypic diversity and shaping adaptive responses. In recent times, they have had a major role in the acquisition, expression, and dissemination of antibiotic resistance genes. Assessing the ongoing threats posed by integrons requires an understanding of their origins and evolutionary history. This review examines the functions and activities of integrons before the antibiotic era. It shows how antibiotic use selected particular integrons from among the environmental pool of these elements, such that integrons carrying resistance genes are now present in the majority of Gram-negative pathogens. Finally, it examines the potential consequences of widespread pollution with the novel integrons that have been assembled via the agency of human antibiotic use and speculates on the potential uses of integrons as platforms for biotechnology. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
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              Integrons.

              Integrons are genetic elements able to acquire and rearrange open reading frames (ORFs) embedded in gene cassette units and convert them to functional genes by ensuring their correct expression. They were originally identified as a mechanism used by Gram-negative bacteria to collect antibiotic resistance genes and express multiple resistance phenotypes in synergy with transposons. More recently, their role has been broadened with the discovery of chromosomal integron (CI) structures in the genomes of hundreds of bacterial species. This review focuses on the resources carried in these elements, on their unique recombination mechanisms, and on the different mechanisms controlling the cassette dynamics. We discuss the role of the toxin/antitoxin (TA) cassettes for the stabilization of the large cassette arrays carried in the larger CIs, known as superintegrons. Finally, we explore the central role played by single-stranded DNA in the integron cassette dynamics in light of the recent discovery that the integron integrase expression is controlled by the SOS response.
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                Author and article information

                Contributors
                fun.life18@snu.ac.kr
                aweinfection@gmail.com
                +82-2-880-1263 , yoohs@snu.ac.kr
                Journal
                BMC Vet Res
                BMC Vet. Res
                BMC Veterinary Research
                BioMed Central (London )
                1746-6148
                12 November 2018
                12 November 2018
                2018
                : 14
                : 340
                Affiliations
                ISNI 0000 0004 0470 5905, GRID grid.31501.36, Department of Infectious Diseases, College of Veterinary Medicine, , Seoul National University, ; Seoul, 08826 Republic of Korea
                Author information
                https://orcid.org/http://orcid.org/0000-0003-0548-0835
                Article
                1661
                10.1186/s12917-018-1661-3
                6233274
                30419899
                90066b34-0faf-47c8-b7d4-2862e6ebd5c8
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

                History
                : 8 December 2017
                : 22 October 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003627, Rural Development Administration;
                Award ID: PJ00897001
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Veterinary medicine
                e. coli,class 1 integrons,tetracycline resistance,phylogenetic group,pfge
                Veterinary medicine
                e. coli, class 1 integrons, tetracycline resistance, phylogenetic group, pfge

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