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      Composite mobile genetic elements disseminating macrolide resistance in Streptococcus pneumoniae

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          Abstract

          Macrolide resistance in Streptococcus pneumoniae emerged in the U.S. and globally during the early 1990's. The RNA methylase encoded by erm(B) and the macrolide efflux genes mef(E) and mel were identified as the resistance determining factors. These genes are disseminated in the pneumococcus on mobile, often chimeric elements consisting of multiple smaller elements. To better understand the variety of elements encoding macrolide resistance and how they have evolved in the pre- and post-conjugate vaccine eras, the genomes of 121 invasive and ten carriage isolates from Atlanta from 1994 to 2011 were analyzed for mobile elements involved in the dissemination of macrolide resistance. The isolates were selected to provide broad coverage of the genetic variability of antibiotic resistant pneumococci and included 100 invasive isolates resistant to macrolides. Tn 916-like elements carrying mef(E) and mel on the Macrolide Genetic Assembly (Mega) and erm(B) on the erm(B) element and Tn 917 were integrated into the pneumococcal chromosome backbone and into larger Tn 5253-like composite elements. The results reported here include identification of novel insertion sites for Mega and characterization of the insertion sites of Tn 916-like elements in the pneumococcal chromosome and in larger composite elements. The data indicate that integration of elements by conjugation was infrequent compared to recombination. Thus, it appears that conjugative mobile elements allow the pneumococcus to acquire DNA from distantly related bacteria, but once integrated into a pneumococcal genome, transformation and recombination is the primary mechanism for transmission of novel DNA throughout the pneumococcal population.

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          Most cited references46

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          A whole-genome assembly of Drosophila.

          We report on the quality of a whole-genome assembly of Drosophila melanogaster and the nature of the computer algorithms that accomplished it. Three independent external data sources essentially agree with and support the assembly's sequence and ordering of contigs across the euchromatic portion of the genome. In addition, there are isolated contigs that we believe represent nonrepetitive pockets within the heterochromatin of the centromeres. Comparison with a previously sequenced 2.9- megabase region indicates that sequencing accuracy within nonrepetitive segments is greater than 99. 99% without manual curation. As such, this initial reconstruction of the Drosophila sequence should be of substantial value to the scientific community.
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            Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae.

            Natural transformation is a widespread mechanism for genetic exchange in bacteria. Aminoglycoside and fluoroquinolone antibiotics, as well as mitomycin C, a DNA-damaging agent, induced transformation in Streptococcus pneumoniae. This induction required an intact competence regulatory cascade. Furthermore, mitomycin C induction of recA was strictly dependent on the development of competence. In response to antibiotic stress, S. pneumoniae, which lacks an SOS-like system, exhibited genetic transformation. The design of antibiotherapy should take into consideration this potential of a major human pathogen to increase its rate of genetic exchange in response to antibiotics.
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              Induction of competence regulons as a general response to stress in gram-positive bacteria.

              Bacterial transformation, a programmed mechanism for genetic exchange originally discovered in Streptococcus pneumoniae, is widespread in bacteria. It is based on the uptake and integration of exogenous DNA into the recipient genome. This review examines whether induction of competence for genetic transformation is a general response to stress in gram-positive bacteria. It compares data obtained with bacteria chosen for their different lifestyles, the soil-dweller Bacillus subtilis and the major human pathogen S. pneumoniae. The review focuses on the relationship between competence and other global responses in B. subtilis, as well as on recent evidence for competence induction in response to DNA damage or antibiotics and for the ability of S. pneumoniae to use competence as a substitute for SOS. This comparison reveals that the two species use different fitness-enhancing strategies in response to stress conditions. Whereas B. subtilis combines competence and SOS induction, S. pneumoniae relies only on competence to generate genetic diversity through transformation.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                09 February 2015
                2015
                : 6
                : 26
                Affiliations
                [1] 1Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine Atlanta, GA, USA
                [2] 2Laboratories of Microbial Pathogenesis, Department of Veterans Affairs Medical Center Atlanta, GA, USA
                [3] 3Institute for Genome Sciences, University of Maryland School of Medicine Baltimore, MD, USA
                [4] 4Department of Microbiology and Immunology, University of Maryland School of Medicine Baltimore, MD, USA
                Author notes

                Edited by: Claudio Palmieri, Polytechnic University of Marche, Italy

                Reviewed by: Agnese Lupo, University of Bern, Switzerland; Kelly L. Wyres, IBM Research - Australia, Australia

                *Correspondence: David S. Stephens, Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine, Atlanta, GA, USA; Laboratories of Microbial Pathogenesis, Department of Veterans Affairs Medical Center, Atlanta, GA, USA e-mail: dstep01@ 123456emory.edu

                This article was submitted to Antimicrobials, Resistance and Chemotherapy, a section of the journal Frontiers in Microbiology.

                †These authors have contributed equally to this work.

                Article
                10.3389/fmicb.2015.00026
                4321634
                25709602
                68257c79-87f8-44e4-a4db-438105f89454
                Copyright © 2015 Chancey, Agrawal, Schroeder, Farley, Tettelin and Stephens.

                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) or licensor 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
                : 07 October 2014
                : 08 January 2015
                Page count
                Figures: 6, Tables: 3, Equations: 0, References: 56, Pages: 14, Words: 10157
                Categories
                Microbiology
                Original Research Article

                Microbiology & Virology
                mobile genetic elements,transposons,integrative and conjugative elements,macrolides,antibiotic resistance,streptococcus pneumoniae

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