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      Comparative genome analysis reveals niche-specific genome expansion in Acinetobacter baumannii strains

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          Abstract

          The nosocomial pathogen Acinetobacter baumannii acquired clinical significance due to the rapid development of its multi-drug resistant (MDR) phenotype. A. baumannii strains have the ability to colonize several ecological niches including soil, water, and animals, including humans. They also survive under extremely harsh environmental conditions thriving on rare and recalcitrant carbon compounds. However, the molecular basis behind such extreme adaptability of A. baumannii is unknown. We have therefore determined the complete genome sequence of A. baumannii DS002, which was isolated from agricultural soils, and compared it with 78 complete genome sequences of A. baumannii strains having complete information on the source of their isolation. Interestingly, the genome of A. baumannii DS002 showed high similarity to the genome of A. baumannii SDF isolated from the body louse. The environmental and clinical strains, which do not share a monophyletic origin, showed the existence of a strain-specific unique gene pool that supports niche-specific survival. The strains isolated from infected samples contained a genetic repertoire with a unique gene pool coding for iron acquisition machinery, particularly those required for the biosynthesis of acinetobactin. Interestingly, these strains also contained genes required for biofilm formation. However, such gene sets were either partially or completely missing in the environmental isolates, which instead harbored genes required for alternate carbon catabolism and a TonB-dependent transport system involved in the acquisition of iron via siderophores or xenosiderophores.

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          Acinetobacter baumannii: evolution of a global pathogen

          Acinetobacter baumannii is an opportunistic nosocomial pathogen and one of the six most important multidrug-resistant microorganisms in hospitals worldwide. This human pathogen is responsible for a vast array of infections, of which ventilator-associated pneumonia and bloodstream infections are the most common, and mortality rates can reach 35%. Community-acquired infections have also been reported, but few strains have been recovered from environmental sources and infection reservoirs external to the hospital have not been identified. The majority of A. baumannii infections are caused by two main population clones with worldwide distribution. Infection outbreaks are often associated with multidrug resistance, including the recent emergence of strains resistant to all available antibiotics. Nevertheless, A. baumannii virulence traits and pathogenic potential have mostly remained elusive. The recent expansion of A. baumannii sequenced genomes has permitted the development of large-array phylogenomic and phenotypic analyses, which can offer valuable insights into the evolution and adaptation of A. baumannii as a human pathogen. This review summarises these recent advances, with particular focus on A. baumannii evolutionary and genomic aspects, and proposes new avenues of research. © 2013 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved.
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            OXA β-lactamases.

            The OXA β-lactamases were among the earliest β-lactamases detected; however, these molecular class D β-lactamases were originally relatively rare and always plasmid mediated. They had a substrate profile limited to the penicillins, but some became able to confer resistance to cephalosporins. From the 1980s onwards, isolates of Acinetobacter baumannii that were resistant to the carbapenems emerged, manifested by plasmid-encoded β-lactamases (OXA-23, OXA-40, and OXA-58) categorized as OXA enzymes because of their sequence similarity to earlier OXA β-lactamases. It was soon found that every A. baumannii strain possessed a chromosomally encoded OXA β-lactamase (OXA-51-like), some of which could confer resistance to carbapenems when the genetic environment around the gene promoted its expression. Similarly, Acinetobacter species closely related to A. baumannii also possessed their own chromosomally encoded OXA β-lactamases; some could be transferred to A. baumannii, and they formed the basis of transferable carbapenem resistance in this species. In some cases, the carbapenem-resistant OXA β-lactamases (OXA-48) have migrated into the Enterobacteriaceae and are becoming a significant cause of carbapenem resistance. The emergence of OXA enzymes that can confer resistance to carbapenems, particularly in A. baumannii, has transformed these β-lactamases from a minor hindrance into a major problem set to demote the clinical efficacy of the carbapenems.
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              Changing patterns of infectious disease.

              M. Cohen (2000)
              Despite a century of often successful prevention and control efforts, infectious diseases remain an important global problem in public health, causing over 13 million deaths each year. Changes in society, technology and the microorganisms themselves are contributing to the emergence of new diseases, the re-emergence of diseases once controlled, and to the development of antimicrobial resistance. Two areas of special concern in the twenty-first century are food-borne disease and antimicrobial resistance. The effective control of infectious diseases in the new millennium will require effective public health infrastructures that will rapidly recognize and respond to them and will prevent emerging problems.
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                Author and article information

                Contributors
                Role: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: SoftwareRole: Writing – review & editing
                Role: Data curationRole: Formal analysis
                Role: ConceptualizationRole: Supervision
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                13 June 2019
                2019
                : 14
                : 6
                : e0218204
                Affiliations
                [1 ] Dept. of Animal Biology, School of Life Sciences, University of Hyderabad, Hyderabad, India
                [2 ] Department of Biological and Computer Sciences, Purdue University, West Lafayette, Indiana, United States of America
                Tianjin University, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-9437-717X
                Article
                PONE-D-19-05495
                10.1371/journal.pone.0218204
                6563999
                31194814
                1155408c-89f8-49fc-af1e-218c86ca49ba

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 25 February 2019
                : 28 May 2019
                Page count
                Figures: 8, Tables: 1, Pages: 26
                Funding
                HY is the recipient of women scientist grant from Department of Science and Technology (DST)(SR/WOS-A/LS-1225/2015(G)), New Delhi ( http://www.dst.gov.in/scientific-programmes/scientific-engineering-research/women-scientists-programs). CSIR, New Delhi and DST, New Delhi supported research work in DS* laboratory. Dept. of Animal Biology received special assistance from DST, New Delhi under FIST-level-II. School of Life Sciences received financial assistance under DBT-CREBB programme (Department of Biotechnology)( http://www.dbtindia.nic.in/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Biology and Life Sciences
                Anatomy
                Body Fluids
                Mucus
                Sputum
                Medicine and Health Sciences
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                Body Fluids
                Mucus
                Sputum
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                Custom metadata
                Complete genomes gbk file is available from the NCBI database. GenBank: CP027704.1.

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