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      Characterization of a Linezolid- and Vancomycin-Resistant Streptococcus suis Isolate That Harbors optrA and vanG Operons

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          Abstract

          Linezolid and vancomycin are among the last-resort antimicrobial agents in the treatment of multidrug-resistant Gram-positive bacterial infections. Linezolid- and vancomycin-resistant (LVR) Gram-positive bacteria may pose severe threats to public health. In this study, three optrA- and vanG-positive Streptococcus suis strains were isolated from two farms of different cities. There were only 1 and 343 single-nucleotide polymorphisms in coding region (cSNPs) of HCB4 and YSJ7 to YSJ17, respectively. Mobilome analysis revealed the presence of vanG, erm(B), tet(O/W/32/O), and aadE- apt- sat4- aphA3 cluster on an integrative and conjugative element, ICE SsuYSJ17, and erm(B), aphA3, aac(6′)-aph(2″), catpC 194, and optrA on a prophage, ΦSsuYSJ17-3. ICE SsuYSJ17 exhibited a mosaic structure and belongs to a highly prevalent and transferable ICE Sa2603 family of Streptococcus species. ΦSsuYSJ17-3 shared conserved backbone to a transferable prophage Φm46.1. A novel composite transposon, IS 1216E- araC- optrA- hp- catpC 194-IS 1216E, which can be circulated as translocatable unit (TU) by IS 1216E, was integrated on ΦSsuYSJ17-3. Vancomycin resistance phenotype and vanG transcription assays revealed that the vanG operon was inducible. The LVR strain YSJ17 exhibited moderate virulence in a zebrafish infection model. To our knowledge, this is the first report of LVR isolate, which is mediated by acquired resistance genes optrA and vanG operons in Gram-positive bacteria. Since S. suis has been recognized as an antimicrobial resistance reservoir in the spread of resistance genes to major streptococcal pathogens, the potential risks of disseminating of optrA and vanG from S. suis to other Streptococcus spp. are worrisome and routine surveillance should be strengthened.

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          Most cited references63

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          Streptococcus suis, an important pig pathogen and emerging zoonotic agent—an update on the worldwide distribution based on serotyping and sequence typing

          Streptococcus suis is an important pathogen causing economic problems in the pig industry. Moreover, it is a zoonotic agent causing severe infections to people in close contact with infected pigs or pork-derived products. Although considered sporadic in the past, human S. suis infections have been reported during the last 45 years, with two large outbreaks recorded in China. In fact, the number of reported human cases has significantly increased in recent years. In this review, we present the worldwide distribution of serotypes and sequence types (STs), as determined by multilocus sequence typing, for pigs (between 2002 and 2013) and humans (between 1968 and 2013). The methods employed for S. suis identification and typing, the current epidemiological knowledge regarding serotypes and STs and the zoonotic potential of S. suis are discussed. Increased awareness of S. suis in both human and veterinary diagnostic laboratories and further establishment of typing methods will contribute to our knowledge of this pathogen, especially in regions where complete and/or recent data is lacking. More research is required to understand differences in virulence that occur among S. suis strains and if these differences can be associated with specific serotypes or STs.
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            A novel gene, optrA, that confers transferable resistance to oxazolidinones and phenicols and its presence in Enterococcus faecalis and Enterococcus faecium of human and animal origin.

            The oxazolidinone-resistant Enterococcus faecalis E349 from a human patient tested negative for the cfr gene and 23S rRNA mutations. Here we report the identification of a novel oxazolidinone resistance gene, optrA, and a first investigation of the extent to which this gene was present in E. faecalis and Enterococcus faecium from humans and food-producing animals.
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              Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis.

              Streptococcus suis is a major swine pathogen responsible for important economic losses to the swine industry worldwide. It is also an emerging zoonotic agent of meningitis and streptococcal toxic shock-like syndrome. Since the recent recognition of the high prevalence of S. suis human disease in southeast and east Asia, the interest of the scientific community in this pathogen has significantly increased. In the last few years, as a direct consequence of these intensified research efforts, large amounts of data on putative virulence factors have appeared in the literature. Although the presence of some proposed virulence factors does not necessarily define a S. suis strain as being virulent, several cell-associated or secreted factors are clearly important for the pathogenesis of the S. suis infection. In order to cause disease, S. suis must colonize the host, breach epithelial barriers, reach and survive in the bloodstream, invade different organs, and cause exaggerated inflammation. In this review, we discuss the potential contribution of different described S. suis virulence factors at each step of the pathogenesis of the infection. Finally, we briefly discuss other described virulence factors, virulence factor candidates and virulence markers for which a precise role at specific steps of the pathogenesis of the S. suis infection has not yet been clearly established.
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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
                10 September 2019
                2019
                : 10
                : 2026
                Affiliations
                MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University , Nanjing, China
                Author notes

                Edited by: Peter Mullany, University College London, United Kingdom

                Reviewed by: Carla Novais, University of Porto, Portugal; Ana P. Tedim, Institute of Health Sciences Studies of Castilla y León (IECSCYL), Spain

                *Correspondence: Liping Wang, wlp71@ 123456163.com

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

                Article
                10.3389/fmicb.2019.02026
                6746840
                31551963
                12f7a925-aec1-4684-a3bc-56294eade024
                Copyright © 2019 Du, Lv, Duan, Wang and Huang.

                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) and the copyright owner(s) 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
                : 21 May 2019
                : 19 August 2019
                Page count
                Figures: 6, Tables: 2, Equations: 0, References: 75, Pages: 12, Words: 0
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31702292
                Award ID: 31872517
                Funded by: Natural Science Foundation of Jiangsu Province 10.13039/501100004608
                Award ID: BK20170710
                Funded by: China Postdoctoral Science Foundation 10.13039/501100002858
                Award ID: 2017M611841
                Award ID: 2018T110515
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                streptococcus suis,vancomycin resistance,vang,linezolid resistance,optra,mobile genetic elements,pathogenicity

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