1. Dissecting the molecular evolution of fluoroquinolone-resistant Shigella sonnei
- Author
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Stephen Baker, To Nguyen Thi Nguyen, Ryan R. Wick, Paul Turner, Pieter-Jan Ceyssens, Vinh Phat Voong, Claire Jenkins, Vu Thuy Duong, François-Xavier Weill, Tuyen Ha Thanh, Guy E. Thwaites, Ladaporn Bodhidatta, Duy Pham Thanh, Martin Cormican, Kathryn E. Holt, Nicholas R. Thomson, Maia A. Rabaa, Sonam Wangchuk, Phu H. Nguyen, Christine J. Boinett, Mary Valcanis, Benjamin P Howden, Carl J. Mason, Niall De Lappe, Oxford University Clinical Research Unit [Ho Chi Minh City] (OUCRU), Public Health England [London], Centre National de Référence - National Reference Center Escherichia coli, Shigella et Salmonella (CNR-ESS), Institut Pasteur [Paris], The Peter Doherty Institute for Infection and Immunity [Melbourne], University of Melbourne-The Royal Melbourne Hospital, University Hospital Galway, National University of Ireland [Galway] (NUI Galway), Ministry of Health [Bhoutan], Armed Forces Research Institute of Medical Sciences [Bangkok] (AFRIMS), Hospital for Tropical Diseases, Centre for Tropical Medicine and Global Health [Oxford, UK], Nuffield Department of Medicine [Oxford, UK] (Big Data Institute), University of Oxford [Oxford]-University of Oxford [Oxford], Angkor Hospital for Children (AHC), Monash University [Melbourne], Sciensano [Bruxelles], Réseau International des Instituts Pasteur (RIIP), London School of Hygiene and Tropical Medicine (LSHTM), The Wellcome Trust Sanger Institute [Cambridge], University of Cambridge [UK] (CAM), H.C.T. received a DPhil scholarship from the Tropical Network Fund, Nuffield Department of Medicine, University of Oxford. S.B. is a Sir Henry Dale Fellow, jointly funded by the Wellcome Trust and the Royal Society (100087/Z/12/Z). We thank I. Carle, M. Lejay-Collin, and C. Ruckly from the Institut Pasteur for their excellent technical assistance. F.X.W is funded by the Institut Pasteur, Santé Publique France, and by the French Government 'Investissement d’Avenir' program (Integrative Biology of Emerging Infectious Diseases Laboratory of Excellence, grant no. ANR-10-LABX-62-IBEID)., ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010), Chung The, Hao [0000-0002-4028-4074], Weill, Francois-Xavier [0000-0001-9941-5799], Howden, Benjamin P [0000-0003-0237-1473], Mason, Carl J [0000-0002-3676-2811], Turner, Paul [0000-0002-1013-7815], Wick, Ryan [0000-0001-8349-0778], Holt, Kathryn E [0000-0003-3949-2471], Rabaa, Maia A [0000-0003-0529-2228], Baker, Stephen [0000-0003-1308-5755], Apollo - University of Cambridge Repository, Howden, Benjamin P. [0000-0003-0237-1473], Mason, Carl J. [0000-0002-3676-2811], Holt, Kathryn E. [0000-0003-3949-2471], Rabaa, Maia A. [0000-0003-0529-2228], Institut Pasteur [Paris] (IP), and University of Oxford-University of Oxford
- Subjects
0301 basic medicine ,General Physics and Astronomy ,Drug resistance ,Antimicrobial resistance ,Ciprofloxacin ,Bacterial genetics ,Shigella sonnei ,lcsh:Science ,Asia, Southeastern ,Phylogeny ,Genetics ,Experimental evolution ,education.field_of_study ,Molecular Epidemiology ,Multidisciplinary ,article ,3. Good health ,Anti-Bacterial Agents ,Europe ,DNA Gyrase ,Pathogens ,Fluoroquinolones ,DNA Topoisomerase IV ,Shigellosis ,Science ,030106 microbiology ,Population ,45/22 ,631/208/325/2482 ,45/23 ,Biology ,Polymorphism, Single Nucleotide ,General Biochemistry, Genetics and Molecular Biology ,Evolution, Molecular ,03 medical and health sciences ,Molecular evolution ,Phylogenetics ,Drug Resistance, Bacterial ,medicine ,Asia, Western ,Humans ,education ,Dysentery, Bacillary ,Molecular epidemiology ,45 ,631/326/421 ,Bayes Theorem ,General Chemistry ,biochemical phenomena, metabolism, and nutrition ,medicine.disease ,bacterial infections and mycoses ,[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology ,digestive system diseases ,030104 developmental biology ,692/699/255/1318 ,631/326/22/1434 ,Mutation ,bacteria ,lcsh:Q ,Bacterial infection ,Directed Molecular Evolution ,Genome, Bacterial - Abstract
Shigella sonnei increasingly dominates the international epidemiological landscape of shigellosis. Treatment options for S. sonnei are dwindling due to resistance to several key antimicrobials, including the fluoroquinolones. Here we analyse nearly 400 S. sonnei whole genome sequences from both endemic and non-endemic regions to delineate the evolutionary history of the recently emergent fluoroquinolone-resistant S. sonnei. We reaffirm that extant resistant organisms belong to a single clonal expansion event. Our results indicate that sequential accumulation of defining mutations (gyrA-S83L, parC-S80I, and gyrA-D87G) led to the emergence of the fluoroquinolone-resistant S. sonnei population around 2007 in South Asia. This clone was then transmitted globally, resulting in establishments in Southeast Asia and Europe. Mutation analysis suggests that the clone became dominant through enhanced adaptation to oxidative stress. Experimental evolution reveals that under fluoroquinolone exposure in vitro, resistant S. sonnei develops further intolerance to the antimicrobial while the susceptible counterpart fails to attain complete resistance., Shigella sonnei is one of the main species causing shigellosis worldwide. Here the authors analyse nearly 400 S. sonnei genome sequences and carry out experimental evolution experiments to shed light into the evolutionary processes underlying the recent emergence of fluoroquinolone resistance in this pathogen.
- Published
- 2019