The evolution of a super-swarm of foot-and-mouth disease virus in cattle.


Journal

PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081

Informations de publication

Date de publication:
2019
Historique:
received: 21 12 2018
accepted: 05 04 2019
entrez: 26 4 2019
pubmed: 26 4 2019
medline: 1 1 2020
Statut: epublish

Résumé

Foot-and-mouth disease (FMD) is a highly contagious viral disease that severely impacts global food security and is one of the greatest constraints on international trade of animal products. Extensive viral population diversity and rapid, continuous mutation of circulating FMD viruses (FMDVs) pose significant obstacles to the control and ultimate eradication of this important transboundary pathogen. The current study investigated mechanisms contributing to within-host evolution of FMDV in a natural host species (cattle). Specifically, vaccinated and non-vaccinated cattle were infected with FMDV under controlled, experimental conditions and subsequently sampled for up to 35 days to monitor viral genomic changes as related to phases of disease and experimental cohorts. Consensus-level genomic changes across the entire FMDV coding region were characterized through three previously defined stages of infection: early, transitional, and persistent. The overall conclusion was that viral evolution occurred via a combination of two mechanisms: emergence of full-genomic minority haplotypes from within the inoculum super-swarm, and concurrent continuous point mutations. Phylogenetic analysis indicated that individuals were infected with multiple distinct haplogroups that were pre-existent within the ancestral inoculum used to infect all animals. Multiple shifts of dominant viral haplotype took place during the early and transitional phases of infection, whereas few shifts occurred during persistent infection. Overall, this work suggests that the establishment of the carrier state is not associated with specific viral genomic characteristics. These insights into FMDV population dynamics have important implications for virus sampling methodology and molecular epidemiology.

Identifiants

pubmed: 31022193
doi: 10.1371/journal.pone.0210847
pii: PONE-D-18-36559
pmc: PMC6483180
doi:

Substances chimiques

Capsid Proteins 0
RNA, Viral 0
Viral Vaccines 0

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0210847

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

J Virol. 2014 Apr;88(8):4008-20
pubmed: 24453363
Infect Genet Evol. 2015 Jun;32:440-8
pubmed: 25861750
Virology. 2015 May;479-480:46-51
pubmed: 25824477
Transbound Emerg Dis. 2018 Dec;65(6):1836-1850
pubmed: 30035376
J Virol. 2016 Apr 29;90(10):5132-5140
pubmed: 26962214
Viruses. 2015 Oct 21;7(10):5443-75
pubmed: 26506369
J Virol. 2009 Nov;83(22):11456-66
pubmed: 19740991
J Virol. 2015 Oct 14;90(1):317-31
pubmed: 26468545
J Hyg (Lond). 1966 Mar;64(1):81-90
pubmed: 5219023
Transbound Emerg Dis. 2011 Aug;58(4):305-26
pubmed: 21672184
EMBO J. 1999 Feb 1;18(3):543-54
pubmed: 9927414
PLoS One. 2015 Nov 23;10(11):e0143666
pubmed: 26599543
Prev Vet Med. 2009 Feb 1;88(2):158-63
pubmed: 18929417
Science. 2011 May 6;332(6030):726-9
pubmed: 21551063
Vet Microbiol. 2007 Feb 25;120(1-2):50-62
pubmed: 17113729
Nature. 2006 Jan 19;439(7074):344-8
pubmed: 16327776
J Gen Virol. 2005 Jul;86(Pt 7):1909-1920
pubmed: 15958669
J Virol. 2011 Mar;85(5):2266-75
pubmed: 21159860
J Virol. 2016 Jun 24;90(14):6344-64
pubmed: 27147736
PLoS One. 2015 May 21;10(5):e0125698
pubmed: 25996935
Vet Q. 2000 Oct;22(4):193-7
pubmed: 11087128
mSphere. 2018 Sep 12;3(5):
pubmed: 30209130
PLoS One. 2015 Jun 25;10(6):e0128815
pubmed: 26110772
Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13910-3
pubmed: 10570172
Nat Commun. 2017 May 23;8:15408
pubmed: 28534487
J Virol. 2006 Dec;80(23):11827-32
pubmed: 16971423
mSphere. 2018 Dec 12;3(6):
pubmed: 30541776
J Comp Pathol. 2016 Nov;155(4):314-325
pubmed: 27697284
Vet Pathol. 2010 Nov;47(6):1048-63
pubmed: 20587691
Arch Gesamte Virusforsch. 1968;23(3):227-35
pubmed: 5680590
J Mol Biol. 2007 Jun 15;369(4):985-1000
pubmed: 17481660
mBio. 2015 Apr 07;6(2):
pubmed: 25852163
J Comp Pathol. 2003 Jul;129(1):1-36
pubmed: 12859905
Prev Vet Med. 2013 Nov 1;112(3-4):161-73
pubmed: 23958457
Vet Rec. 1965 Aug 14;77(33):968-9
pubmed: 5890082
Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1932-6
pubmed: 8127909
PLoS Pathog. 2015 Aug 27;11(8):e1005114
pubmed: 26313548
Transbound Emerg Dis. 2018 Apr;65(2):447-455
pubmed: 29076657
Vet Microbiol. 2012 Jan 27;154(3-4):230-9
pubmed: 21831538
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
Nat Rev Genet. 2008 Apr;9(4):267-76
pubmed: 18319742
Syst Biol. 2003 Oct;52(5):696-704
pubmed: 14530136
Transbound Emerg Dis. 2016 Jun;63 Suppl 1:14-29
pubmed: 27320163
Virology. 2008 Dec 20;382(2):250-6
pubmed: 18945462
Arch Virol. 2015 Jan;160(1):1-16
pubmed: 25377637
Rev Sci Tech. 2002 Dec;21(3):519-29
pubmed: 12523693
BMC Vet Res. 2016 Sep 15;12:205
pubmed: 27634113
Microbes Infect. 2002 Aug;4(10):1099-110
pubmed: 12191660
Clin Microbiol Rev. 2004 Apr;17(2):465-93
pubmed: 15084510
Philos Trans R Soc Lond B Biol Sci. 2013 Feb 04;368(1614):20120203
pubmed: 23382425
mSystems. 2016 Jun 7;1(3):
pubmed: 27822536
J Gen Virol. 2013 Jan;94(Pt 1):108-119
pubmed: 23034594
PLoS Pathog. 2008 Apr 18;4(4):e1000050
pubmed: 18421380
Virus Res. 2003 Jan;91(1):9-32
pubmed: 12527435
J Comp Pathol. 2001 Feb-Apr;124(2-3):89-94
pubmed: 11222004
Virus Res. 1985 Nov;3(4):373-84
pubmed: 3000107
Virus Res. 1994 Oct;34(1):31-48
pubmed: 7831963
Infect Genet Evol. 2016 Oct;44:286-292
pubmed: 27421209
Transbound Emerg Dis. 2016 Jun;63 Suppl 1:63-71
pubmed: 27320168
Mol Biol Evol. 2016 Jul;33(7):1870-4
pubmed: 27004904
Sci Rep. 2018 Apr 24;8(1):6472
pubmed: 29691483
Infect Genet Evol. 2008 Dec;8(6):786-98
pubmed: 18718559
Nature. 1993 Apr 8;362(6420):566-8
pubmed: 8385272
Arch Virol. 2005 May;150(5):911-28
pubmed: 15662482
Vet Res. 2013 Mar 01;44:12
pubmed: 23452550
Sci Rep. 2017 Dec 19;7(1):17800
pubmed: 29259271
J Gen Virol. 2013 Jul;94(Pt 7):1486-1495
pubmed: 23515027
J Virol. 2007 Oct;81(20):11341-51
pubmed: 17686868

Auteurs

Jonathan Arzt (J)

Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS, USDA, Greenport, NY, United States of America.

Ian Fish (I)

Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS, USDA, Greenport, NY, United States of America.
Oak Ridge Institute for Science and Education, PIADC Research Participation Program, Oak Ridge, TN, United States of America.

Steven J Pauszek (SJ)

Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS, USDA, Greenport, NY, United States of America.

Shannon L Johnson (SL)

Los Alamos National Laboratory, Los Alamos, NM, United States of America.

Patrick S Chain (PS)

Los Alamos National Laboratory, Los Alamos, NM, United States of America.

Devendra K Rai (DK)

Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS, USDA, Greenport, NY, United States of America.
Department of Veterinary Population Medicine, University of Minnesota, St Paul, MN, United States of America.

Elizabeth Rieder (E)

Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS, USDA, Greenport, NY, United States of America.

Tony L Goldberg (TL)

Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, Madison, WI, United States of America.

Luis L Rodriguez (LL)

Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS, USDA, Greenport, NY, United States of America.

Carolina Stenfeldt (C)

Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS, USDA, Greenport, NY, United States of America.
Department of Veterinary Population Medicine, University of Minnesota, St Paul, MN, United States of America.

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