Evolutionary histories and antimicrobial resistance in Shigella flexneri and Shigella sonnei in Southeast Asia.
Anti-Bacterial Agents
/ pharmacology
Asia, Southeastern
/ epidemiology
Drug Resistance, Bacterial
/ genetics
Dysentery, Bacillary
/ drug therapy
Evolution, Molecular
Genetic Variation
Humans
Molecular Epidemiology
Phylogeny
Shigella flexneri
/ drug effects
Shigella sonnei
/ drug effects
Whole Genome Sequencing
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
19 03 2021
19 03 2021
Historique:
received:
04
09
2020
accepted:
10
02
2021
entrez:
20
3
2021
pubmed:
21
3
2021
medline:
12
8
2021
Statut:
epublish
Résumé
Conventional disease surveillance for shigellosis in developing country settings relies on serotyping and low-resolution molecular typing, which fails to contextualise the evolutionary history of the genus. Here, we interrogated a collection of 1,804 Shigella whole genome sequences from organisms isolated in four continental Southeast Asian countries (Thailand, Vietnam, Laos, and Cambodia) over three decades to characterise the evolution of both S. flexneri and S. sonnei. We show that S. sonnei and each major S. flexneri serotype are comprised of genetically diverse populations, the majority of which were likely introduced into Southeast Asia in the 1970s-1990s. Intranational and regional dissemination allowed widespread propagation of both species across the region. Our data indicate that the epidemiology of S. sonnei and the major S. flexneri serotypes were characterised by frequent clonal replacement events, coinciding with changing susceptibility patterns against contemporaneous antimicrobials. We conclude that adaptation to antimicrobial pressure was pivotal to the recent evolutionary trajectory of Shigella in Southeast Asia.
Identifiants
pubmed: 33742111
doi: 10.1038/s42003-021-01905-9
pii: 10.1038/s42003-021-01905-9
pmc: PMC7979695
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
353Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 218726/Z/19/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 215515/Z/19/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 106698/Z/14/Z
Pays : United Kingdom
Références
Kotloff, K. L. et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382, 209–222 (2013).
pubmed: 23680352
doi: 10.1016/S0140-6736(13)60844-2
Troeger, C. et al. Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the Global Burden of Disease Study 2015. Lancet Infect. Dis. 3099, 1–40 (2017).
Gu, B. et al. Comparison of the prevalence and changing resistance to nalidixic acid and ciprofloxacin of Shigella between Europe-America and Asia-Africa from 1998 to 2009. Int. J. Antimicrob. Agents 40, 9–17 (2012).
Thompson, C. N. et al. A prospective multi-center observational study of children hospitalized with diarrhea in Ho Chi Minh City, Vietnam. Am. J. Trop. Med. Hyg. 92, 1045–1052 (2015).
pubmed: 25802437
pmcid: 4426562
doi: 10.4269/ajtmh.14-0655
Bodhidatta, L. et al. Bacterial enteric pathogens in children with acute dysentery in thailand: increasing importance of quinolone-resistant Campylobacter. Southeast Asian J. Trop. Med. Public Health 33, 752–757 (2002).
pubmed: 12757222
Meng, C. Y. et al. Etiology of diarrhea in young children and patterns of antibiotic resistance in Cambodia. Pediatr. Infect. Dis. J. 30, 331–335 (2011).
pubmed: 21412204
doi: 10.1097/INF.0b013e3181fb6f82
von Seidlein, L. et al. A multicentre study of Shigella diarrhoea in six Asian countries: disease burden, clinical manifestations, and microbiology. PLoS Med 3, e353 (2006).
doi: 10.1371/journal.pmed.0030353
Holt, K. E. et al. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat. Genet. 44, 1056–1059 (2012).
pubmed: 22863732
pmcid: 3442231
doi: 10.1038/ng.2369
Holt, K. E. et al. Tracking the establishment of local endemic populations of an emergent enteric pathogen. Proc. Natl Acad. Sci. USA. 110, 17522–17527(2013).
pubmed: 24082120
doi: 10.1073/pnas.1308632110
pmcid: 3808646
Connor, T. R. et al. Species-wide whole genome sequencing reveals historical global spread and recent local persistence in Shigella flexneri. Elife 4, 1–16 (2015).
doi: 10.7554/eLife.07335
The, H. C., Thanh, D. P., Holt, K. E., Thomson, N. R. & Baker, S. The genomic signatures of Shigella evolution, adaptation and geographical spread. Nat. Rev. Microbiol. (2016). https://doi.org/10.1038/nrmicro.2016.10
Bangtrakulnonth, A. et al. Shigella from humans in Thailand during 1993 to 2006: spatial-time trends in species and serotype distribution. Foodborne Pathog. Dis. 5, 773–784 (2008).
pubmed: 19086804
doi: 10.1089/fpd.2008.0109
Vinh, H. et al. A changing picture of shigellosis in southern Vietnam: shifting species dominance, antimicrobial susceptibility and clinical presentation. BMC Infect. Dis. 9, 204 (2009).
pubmed: 20003464
pmcid: 2803792
doi: 10.1186/1471-2334-9-204
Chung The, H. et al. Dissecting the molecular evolution of fluoroquinolone-resistant Shigella sonnei. Nat. Commun. 10, 4828 (2019).
pubmed: 31645551
pmcid: 6811581
doi: 10.1038/s41467-019-12823-0
Sadouki, Z. et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Shigella sonnei isolated from cases of diarrhoeal disease in England and Wales, 2015. J. Antimicrob. Chemother. 72, 2496–2502 (2017).
pubmed: 28591819
doi: 10.1093/jac/dkx170
Njamkepo, E. et al. Global phylogeography and evolutionary history of Shigella dysenteriae type 1. Nat. Microbiol. 16027 (2016). https://doi.org/10.1038/nmicrobiol.2016.27
Liang, B. et al. Transferable plasmid-borne mcr-1 in a colistin resistant Shigella flexneri isolate. Mbio. 84, 1–10 (2018).
Chung The, H. et al. South Asia as a reservoir for the global spread of ciprofloxacin resistant Shigella sonnei. PLoS Med 13, 1–12 (2016).
doi: 10.1371/journal.pmed.1002055
Pham, T. D. et al. Commensal Escherichia coli are a reservoir for the transfer of XDR plasmids into epidemic fluoroquinolone-resistant Shigella sonnei. Nat. Microbiol. 5, 1–9 (2020).
Phan, D. & Coxhead, I. Inter-provincial migration and inequality during Vietnam’s transition. J. Dev. Econ. 91, 100–112 (2010).
doi: 10.1016/j.jdeveco.2009.06.008
Zhao, Y., Zhu, Y., Zhu, Z. & Qu, B. Association between meteorological factors and bacillary dysentery incidence in Chaoyang city, China: an ecological study. BMJ Open 6, e013376 (2016).
pubmed: 27940632
pmcid: 5168663
doi: 10.1136/bmjopen-2016-013376
Thompson, C. N., Duy, P. T. & Baker, S. The rising dominance of Shigella sonnei: an intercontinental shift in the etiology of bacillary dysentery. PLoS Negl. Trop. Dis. 9, e0003708 (2015).
pubmed: 26068698
pmcid: 4466244
doi: 10.1371/journal.pntd.0003708
Niyogi, S. K. Increasing antimicrobial resistance-an emerging problem in the treatment of shigellosis. Clin. Microbiol. Infect. 13, 1141–1143 (2007).
pubmed: 17953700
doi: 10.1111/j.1469-0691.2007.01829.x
Baker, K. S. et al. Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study. Lancet Infect. Dis. 3099, 1–9 (2015).
Baker, K. S. et al. Horizontal antimicrobial resistance transfer drives epidemics of multiple Shigella species. Nat. Commun. 9, 1462 (2018).
pubmed: 29654279
pmcid: 5899146
doi: 10.1038/s41467-018-03949-8
Bardsley, M. et al. Persistent transmission of shigellosis in England is associated with a recently emerged multidrug-resistant strain of shigella sonnei. J. Clin. Microbiol. 58, e01692–e01719 (2020).
pubmed: 31969425
pmcid: 7098776
doi: 10.1128/JCM.01692-19
He, F. et al. Shigellosis outbreak associated with contaminated well water in a rural elementary school: Sichuan Province, China, June 7-16, 2009. PLoS One 7, 16–19 (2012).
doi: 10.1371/journal.pone.0047239
Rahman, M. Z. et al. Recovery and characterization of environmental variants of Shigella flexneri from surface water in Bangladesh. Curr. Microbiol. 63, 372–376 (2011).
pubmed: 21826486
doi: 10.1007/s00284-011-9992-3
McVicker, G. & Tang, C. M. Deletion of toxin–antitoxin systems in the evolution of Shigella sonnei as a host-adapted pathogen. Nat. Microbiol. 2, 16204 (2016).
pubmed: 27819667
doi: 10.1038/nmicrobiol.2016.204
Anderson, M. C., Vonaesch, P., Saffarian, A., Marteyn, B. S. & Sansonetti, P. J. Shigella sonnei encodes a functional T6SS used for interbacterial competition and niche occupancy. Cell Host Microbe 21, 769–776.e3 (2017).
pubmed: 28618272
doi: 10.1016/j.chom.2017.05.004
Caboni, M. et al. An O antigen capsule modulates bacterial pathogenesis in Shigella sonnei. PLOS Pathog. 11, e1004749 (2015).
pubmed: 25794007
pmcid: 4368438
doi: 10.1371/journal.ppat.1004749
Watson, J. L. et al. Shigella sonnei O-antigen inhibits internalization, vacuole escape, and inflammation activation. MBio. 10, 1–14 (2019).
doi: 10.1128/mBio.02654-19
Torraca, V. et al. Shigella sonnei infection of zebrafish reveals that O-antigen mediates neutrophil tolerance and dysentery incidence. PLoS Pathog. 15, 1–26 (2019).
doi: 10.1371/journal.ppat.1008006
Weill, F. et al. Genomic history of the seventh pandemic of cholera in Africa. Science 789, 785–789 (2017).
doi: 10.1126/science.aad5901
Duong, V. T. et al. No Clinical benefit of empirical antimicrobial therapy for pediatric diarrhea in a high-usage, high-resistance setting. Clin. Infect. Dis. 66, 504–511 (2018).
pubmed: 29029149
doi: 10.1093/cid/cix844
Sun, Q. et al. Development of a multiplex PCR assay targeting O-antigen modification genes for molecular serotyping of Shigella flexneri. J. Clin. Microbiol. 49, 3766–3770 (2011).
pubmed: 21880974
pmcid: 3209073
doi: 10.1128/JCM.01259-11
Gentle, A., Ashton, P. M., Dallman, T. J. & Jenkins, C. Evaluation of molecular methods for serotyping Shigella flexneri. J. Clin. Microbiol. 54, 1456–1461 (2016).
pubmed: 26984974
pmcid: 4879286
doi: 10.1128/JCM.03386-15
Ponsting, H. & Ning, Z. SMALT—A new mapper for DNA sequencing reads. F1000Posters 1 (2010). https://doi.org/10.7490/F1000RESEARCH.327.1
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Croucher, N. J. et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic. Acids. Res. 44, 1–13 (2014).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Page, A. J. et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693 (2015).
pubmed: 26198102
pmcid: 4817141
doi: 10.1093/bioinformatics/btv421
Chung The, H. et al. Introduction and establishment of fluoroquinolone resistant Shigella sonnei into Bhutan. Microb. Genomics 1, 1–11 (2015).
doi: 10.1099/mgen.0.000042
Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic. Acids. Res. 44, W242–W245 (2016).
pubmed: 27095192
pmcid: 4987883
doi: 10.1093/nar/gkw290
Rambaut, A., Lam, T. T., Max Carvalho, L. & Pybus, O. G. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2, vew007 (2016).
pubmed: 27774300
pmcid: 4989882
doi: 10.1093/ve/vew007
Nguyen, L. T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430
doi: 10.1093/molbev/msu300
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Drummond, A. J. & Rambaut, A. BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).
pubmed: 17996036
pmcid: 2247476
doi: 10.1186/1471-2148-7-214
Baele, G. et al. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol. Biol. Evol. 29, 2157–2167 (2012).
pubmed: 22403239
pmcid: 3424409
doi: 10.1093/molbev/mss084
Baele, G., Li, W. L. S., Drummond, A. J., Suchard, M. A. & Lemey, P. Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol. Biol. Evol. 30, 239–243 (2013).
pubmed: 23090976
doi: 10.1093/molbev/mss243
Bollback, J. P. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinforma. 7, 88 (2006).
doi: 10.1186/1471-2105-7-88
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
doi: 10.1111/j.2041-210X.2011.00169.x
Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome. Res. 18, 821–829 (2008).
pubmed: 18349386
pmcid: 2336801
doi: 10.1101/gr.074492.107
Page, A. J. et al. Robust high-throughput prokaryote de novo assembly and improvement pipeline for Illumina data. Microb. Genomics. 2, 1–7 (2016).
doi: 10.1099/mgen.0.000083
Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
doi: 10.1093/bioinformatics/btu153
pubmed: 24642063
Hunt, M. et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb. Genomics. 3, 1–11 (2017).
doi: 10.1099/mgen.0.000131
Zankari, E. et al. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640–2644 (2012).
pubmed: 22782487
pmcid: 3468078
doi: 10.1093/jac/dks261
Carattoli, A. et al. In Silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903 (2014).
pubmed: 24777092
pmcid: 4068535
doi: 10.1128/AAC.02412-14
R Core Team. R: a language and environment for statistical computing. (2016).
Team Rs. RStudio: integrated development for R. (2020).