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Title: Genetic stability of foot-and-mouth disease virus during long-term infections in natural hosts

Abstract

Foot-and-mouth disease (FMD) is a severe infection caused by a picornavirus that affects livestock and wildlife. Persistence in ruminants is a well-documented feature of Foot-andmouth disease virus (FMDV) pathogenesis and a major concern for disease control. Persistently infected animals harbor virus for extended periods, providing a unique opportunity to study within-host virus evolution. This study investigated the genetic dynamics of FMDV during persistent infections of naturally infected Asian buffalo. Using next-generation sequencing (NGS) we obtained 21 near complete FMDV genome sequences from 12 sub-clinically infected buffalo over a period of one year. Four animals yielded only one virus isolate and one yielded two isolates of different serotype suggesting a serial infection. Seven persistently infected animals yielded more than one virus of the same serotype showing a longterm intra-host viral genetic divergence at the consensus level of less than 2.5%. Quasi-species analysis showed few nucleotide variants and non-synonymous substitutions of progeny virus despite intra-host persistence of up to 152 days. Phylogenetic analyses of serotype Asia-1 VP1 sequences clustered all viruses from persistent animals with Group VII viruses circulating in Pakistan in 2011, but distinct from those circulating on 2008–2009. Furthermore, signature amino acid (aa) substitutions were found in the antigenically relevantmore » VP1 of persistent viruses compared with viruses from 2008–2009. Intra-host purifying selective pressure was observed, with few codons in structural proteins undergoing positive selection. However, FMD persistent viruses did not show a clear pattern of antigenic selection. Our findings provide insight into the evolutionary dynamics of FMDV populations within naturally occurring subclinical and persistent infections that may have implications to vaccination strategies in the region.« less

Authors:
 [1];  [2];  [1];  [3];  [3];  [4];  [4];  [2]
  1. Plum Island Animal Disease Center, Greenport, NY (United States); Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
  2. Plum Island Animal Disease Center, Greenport, NY (United States)
  3. National Agricultural Research Center, Isamabad (Pakistan). Animal Health Program
  4. J. Craig Venter Inst., Rockville, MD (United States)
Publication Date:
Research Org.:
Oak Ridge Associated Univ., Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; USDA; Agricultural Research Service (ARS); US Department of State; US Department of Homeland Security (DHS); Plum Island Animal Disease Center Research Participation Program
OSTI Identifier:
1627849
Grant/Contract Number:  
SC0014664; HSHQDC-12-X-00060
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 13; Journal Issue: 2; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; Science & technology - other topics; Viral persistence and latency; Genomics; Phylogenetic analysis; Nucleotides; Viral genomics; Viral evolution; Foot and mouth disease; Structural proteins

Citation Formats

Ramirez-Carvajal, Lisbeth, Pauszek, Steven J., Ahmed, Zaheer, Farooq, Umer, Naeem, Khalid, Shabman, Reed S., Stockwell, Timothy B., and Rodriguez, Luis L. Genetic stability of foot-and-mouth disease virus during long-term infections in natural hosts. United States: N. p., 2018. Web. doi:10.1371/journal.pone.0190977.
Ramirez-Carvajal, Lisbeth, Pauszek, Steven J., Ahmed, Zaheer, Farooq, Umer, Naeem, Khalid, Shabman, Reed S., Stockwell, Timothy B., & Rodriguez, Luis L. Genetic stability of foot-and-mouth disease virus during long-term infections in natural hosts. United States. https://doi.org/10.1371/journal.pone.0190977
Ramirez-Carvajal, Lisbeth, Pauszek, Steven J., Ahmed, Zaheer, Farooq, Umer, Naeem, Khalid, Shabman, Reed S., Stockwell, Timothy B., and Rodriguez, Luis L. Thu . "Genetic stability of foot-and-mouth disease virus during long-term infections in natural hosts". United States. https://doi.org/10.1371/journal.pone.0190977. https://www.osti.gov/servlets/purl/1627849.
@article{osti_1627849,
title = {Genetic stability of foot-and-mouth disease virus during long-term infections in natural hosts},
author = {Ramirez-Carvajal, Lisbeth and Pauszek, Steven J. and Ahmed, Zaheer and Farooq, Umer and Naeem, Khalid and Shabman, Reed S. and Stockwell, Timothy B. and Rodriguez, Luis L.},
abstractNote = {Foot-and-mouth disease (FMD) is a severe infection caused by a picornavirus that affects livestock and wildlife. Persistence in ruminants is a well-documented feature of Foot-andmouth disease virus (FMDV) pathogenesis and a major concern for disease control. Persistently infected animals harbor virus for extended periods, providing a unique opportunity to study within-host virus evolution. This study investigated the genetic dynamics of FMDV during persistent infections of naturally infected Asian buffalo. Using next-generation sequencing (NGS) we obtained 21 near complete FMDV genome sequences from 12 sub-clinically infected buffalo over a period of one year. Four animals yielded only one virus isolate and one yielded two isolates of different serotype suggesting a serial infection. Seven persistently infected animals yielded more than one virus of the same serotype showing a longterm intra-host viral genetic divergence at the consensus level of less than 2.5%. Quasi-species analysis showed few nucleotide variants and non-synonymous substitutions of progeny virus despite intra-host persistence of up to 152 days. Phylogenetic analyses of serotype Asia-1 VP1 sequences clustered all viruses from persistent animals with Group VII viruses circulating in Pakistan in 2011, but distinct from those circulating on 2008–2009. Furthermore, signature amino acid (aa) substitutions were found in the antigenically relevant VP1 of persistent viruses compared with viruses from 2008–2009. Intra-host purifying selective pressure was observed, with few codons in structural proteins undergoing positive selection. However, FMD persistent viruses did not show a clear pattern of antigenic selection. Our findings provide insight into the evolutionary dynamics of FMDV populations within naturally occurring subclinical and persistent infections that may have implications to vaccination strategies in the region.},
doi = {10.1371/journal.pone.0190977},
journal = {PLoS ONE},
number = 2,
volume = 13,
place = {United States},
year = {Thu Feb 01 00:00:00 EST 2018},
month = {Thu Feb 01 00:00:00 EST 2018}
}

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Works referenced in this record:

Use of a portable real-time reverse transcriptasepolymerase chain reaction assay for rapid detection of foot-and-mouth disease virus
journal, June 2002

  • Callahan, Johnny D.; Brown, Fred; Osorio, Fernando A.
  • Journal of the American Veterinary Medical Association, Vol. 220, Issue 11
  • DOI: 10.2460/javma.2002.220.1636

KaKs_Calculator: Calculating Ka and Ks Through Model Selection and Model Averaging
journal, January 2006


Differential Persistence of Foot-and-Mouth Disease Virus in African Buffalo Is Related to Virus Virulence
journal, March 2016

  • Maree, Francois; de Klerk-Lorist, Lin-Mari; Gubbins, Simon
  • Journal of Virology, Vol. 90, Issue 10
  • DOI: 10.1128/JVI.00166-16

Quasispecies Theory and the Behavior of RNA Viruses
journal, July 2010


Comparative genomics of serotype Asia 1 foot-and-mouth disease virus isolates from India sampled over the last two decades
journal, September 2008


Genetic and antigenic characterisation of serotype A FMD viruses from East Africa to select new vaccine strains
journal, October 2014


Viral genome sequencing by random priming methods
journal, January 2008

  • Djikeng, Appolinaire; Halpin, Rebecca; Kuzmickas, Ryan
  • BMC Genomics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2164-9-5

Viral genome sequencing by random priming methods
journal, January 2008

  • Djikeng, Appolinaire; Halpin, Rebecca; Kuzmickas, Ryan
  • BMC Genomics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2164-9-5

Datamonkey: rapid detection of selective pressure on individual sites of codon alignments
journal, February 2005


Foot-and-Mouth Disease
journal, April 2004


Genetic and antigenic characterisation of serotype A FMD viruses from East Africa to select new vaccine strains
journal, October 2014


Evolutionary analysis of serotype A foot-and-mouth disease viruses circulating in Pakistan and Afghanistan during 2002–2009
journal, December 2011

  • Jamal, Syed M.; Ferrari, Giancarlo; Ahmed, Safia
  • Journal of General Virology, Vol. 92, Issue 12
  • DOI: 10.1099/vir.0.035626-0

Comparative genomics of serotype Asia 1 foot-and-mouth disease virus isolates from India sampled over the last two decades
journal, September 2008


Natural transmission of foot-and-mouth disease virus from African buffalo (Syncerus caffer) to cattle in a wildlife area of Zimbabwe
journal, March 1994

  • Dawe, P.; Flanagan, F.; Madekurozwa, R.
  • Veterinary Record, Vol. 134, Issue 10
  • DOI: 10.1136/vr.134.10.230

Application of next-generation sequencing technologies in virology
journal, September 2012

  • Radford, Alan D.; Chapman, David; Dixon, Linda
  • Journal of General Virology, Vol. 93, Issue 9
  • DOI: 10.1099/vir.0.043182-0

Evolutionary analysis of serotype A foot-and-mouth disease viruses circulating in Pakistan and Afghanistan during 2002–2009
journal, December 2011

  • Jamal, Syed M.; Ferrari, Giancarlo; Ahmed, Safia
  • Journal of General Virology, Vol. 92, Issue 12
  • DOI: 10.1099/vir.0.035626-0

Evolution of foot-and-mouth disease virus intra-sample sequence diversity during serial transmission in bovine hosts
journal, January 2013

  • Morelli, Marco J.; Wright, Caroline F.; Knowles, Nick J.
  • Veterinary Research, Vol. 44, Issue 1
  • DOI: 10.1186/1297-9716-44-12

Detecting Individual Sites Subject to Episodic Diversifying Selection
journal, July 2012


Foot-and-mouth disease in Indian buffaloes
journal, August 1983


The Cell Attachment Site on Foot-and-Mouth Disease Virus Includes the Amino Acid Sequence RGD (Arginine-Glycine-Aspartic Acid)
journal, March 1989


Status of foot-and-mouth disease in Pakistan
journal, June 2010


Virus Excretion from Foot-And-Mouth Disease Virus Carrier Cattle and Their Potential Role in Causing New Outbreaks
journal, June 2015


Multiple Origins of Foot-and-Mouth Disease Virus Serotype Asia 1 Outbreaks, 2003–2007
journal, July 2009

  • Valarcher, Jean-Francois; Knowles, Nick J.; Zakharov, Valery
  • Emerging Infectious Diseases, Vol. 15, Issue 7
  • DOI: 10.3201/eid1507.081621

Phylogeny and genetic diversity of foot and mouth disease virus serotype Asia1 in India during 1964–2012
journal, December 2013

  • Subramaniam, Saravanan; Mohapatra, Jajati K.; Sharma, Gaurav K.
  • Veterinary Microbiology, Vol. 167, Issue 3-4
  • DOI: 10.1016/j.vetmic.2013.08.023

The comparative utility of oral swabs and probang samples for detection of foot-and-mouth disease virus infection in cattle and pigs
journal, March 2013


Status of foot-and-mouth disease in Pakistan
journal, June 2010


Foot-and-mouth disease: past, present and future
journal, January 2013


Retrospective evaluation of foot-and-mouth disease vaccine effectiveness in Turkey
journal, April 2014


Transmission Pathways of Foot-and-Mouth Disease Virus in the United Kingdom in 2007
journal, April 2008


GARD: a genetic algorithm for recombination detection
journal, November 2006


Application of next-generation sequencing technologies in virology
journal, September 2012

  • Radford, Alan D.; Chapman, David; Dixon, Linda
  • Journal of General Virology, Vol. 93, Issue 9
  • DOI: 10.1099/vir.0.043182-0

Natural transmission of foot-and-mouth disease virus from African buffalo (Syncerus caffer) to cattle in a wildlife area of Zimbabwe
journal, March 1994

  • Dawe, P.; Flanagan, F.; Madekurozwa, R.
  • Veterinary Record, Vol. 134, Issue 10
  • DOI: 10.1136/vr.134.10.230

Hydrophobic, Hydrophilic, and Charged Amino Acid Networks within Protein
journal, July 2007


Datamonkey: rapid detection of selective pressure on individual sites of codon alignments
journal, February 2005


Seroprevalence of foot-and-mouth disease in large ruminants in periurban dairy farms near Islamabad, Pakistan
journal, January 2016


Molecular epidemiology of foot-and-mouth disease virus
journal, January 2003


Evolution of foot-and-mouth disease virus intra-sample sequence diversity during serial transmission in bovine hosts
journal, January 2013

  • Morelli, Marco J.; Wright, Caroline F.; Knowles, Nick J.
  • Veterinary Research, Vol. 44, Issue 1
  • DOI: 10.1186/1297-9716-44-12

The Foot-and-Mouth Disease Carrier State Divergence in Cattle
journal, May 2016

  • Stenfeldt, Carolina; Eschbaumer, Michael; Rekant, Steven I.
  • Journal of Virology, Vol. 90, Issue 14
  • DOI: 10.1128/JVI.00388-16

Evidence for Positive Selection in Foot-and-Mouth Disease Virus Capsid Genes From Field Isolates
journal, January 2001


Mechanisms of Foot-and-Mouth Disease Virus Tropism Inferred from Differential Tissue Gene Expression
journal, May 2013


CLUSTAL V: improved software for multiple sequence alignment
journal, January 1992


Spatial trend of Foot and Mouth Disease virus (FMDV) serotypes in cattle and buffaloes, Pakistan
journal, October 2012


Serotype-specific differences in antigenic regions of foot-and-mouth disease virus (FMDV): A comprehensive statistical analysis
journal, December 2008


MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Experimental transmission of foot-and-mouth disease virus from carrier African buffalo (Syncerus caffer) to cattle in Zimbabwe
journal, February 1994


Foot and mouth disease virus vaccines
journal, November 2009


Foot and mouth disease virus vaccines
journal, November 2009


Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology
journal, July 2010


Molecular basis of pathogenesis of FMDV
journal, January 2003


MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001


MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001


Genetic relationships between foot–and–mouth disease type Asia 1 viruses
journal, February 1994

  • Ansell, D. M.; Samuel, A. R.; Carpenter, W. C.
  • Epidemiology and Infection, Vol. 112, Issue 1
  • DOI: 10.1017/s0950268800057587

Full-Length Human Immunodeficiency Virus Type 1 Genomes from Subtype C-Infected Seroconverters in India, with Evidence of Intersubtype Recombination
journal, January 1999


MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Virus Excretion from Foot-And-Mouth Disease Virus Carrier Cattle and Their Potential Role in Causing New Outbreaks
journal, June 2015


Foot-and-mouth disease: past, present and future
journal, January 2013


Multiple Origins of Foot-and-Mouth Disease Virus Serotype Asia 1 Outbreaks, 2003–2007
journal, July 2009

  • Valarcher, Jean-Francois; Knowles, Nick J.; Zakharov, Valery
  • Emerging Infectious Diseases, Vol. 15, Issue 7
  • DOI: 10.3201/eid1507.081621

Performance comparison of benchtop high-throughput sequencing platforms
journal, April 2012

  • Loman, Nicholas J.; Misra, Raju V.; Dallman, Timothy J.
  • Nature Biotechnology, Vol. 30, Issue 5
  • DOI: 10.1038/nbt.2198

Foot-And-Mouth Disease
journal, October 1968


GARD: a genetic algorithm for recombination detection
journal, November 2006


Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology
journal, July 2010


Transmission Pathways of Foot-and-Mouth Disease Virus in the United Kingdom in 2007
journal, April 2008


Genomics and outbreaks: foot and mouth disease: -EN- -FR- La génomique et le contrôle des foyers : la fièvre aphteuse -ES- Genómica y brotes: fiebre aftosa
journal, April 2016

  • Freimanis, G. L.; Di Nardo, A.; Bankowska, K.
  • Revue Scientifique et Technique de l'OIE, Vol. 35, Issue 1
  • DOI: 10.20506/rst.35.1.2426

A Continuous Bovine Kidney Cell Line Constitutively Expressing Bovine  V 6 Integrin Has Increased Susceptibility to Foot-and-Mouth Disease Virus
journal, March 2013

  • LaRocco, M.; Krug, P. W.; Kramer, E.
  • Journal of Clinical Microbiology, Vol. 51, Issue 6
  • DOI: 10.1128/jcm.03370-12

Quasispecies Theory and the Behavior of RNA Viruses
journal, July 2010


Rates of Molecular Evolution in RNA Viruses: A Quantitative Phylogenetic Analysis
journal, February 2002

  • Jenkins, Gareth M.; Rambaut, Andrew; Pybus, Oliver G.
  • Journal of Molecular Evolution, Vol. 54, Issue 2
  • DOI: 10.1007/s00239-001-0064-3

Read and assembly metrics inconsequential for clinical utility of whole-genome sequencing in mapping outbreaks
journal, July 2013

  • Harris, Simon R.; Török, M. E.; Cartwright, Edward J. P.
  • Nature Biotechnology, Vol. 31, Issue 7
  • DOI: 10.1038/nbt.2616

Evidence for Positive Selection in Foot-and-Mouth Disease Virus Capsid Genes From Field Isolates
journal, January 2001


Works referencing / citing this record:

Model of persistent foot‐and‐mouth disease virus infection in multilayered cells derived from bovine dorsal soft palate
journal, August 2019

  • Hägglund, Sara; Laloy, Eve; Näslund, Katarina
  • Transboundary and Emerging Diseases, Vol. 67, Issue 1
  • DOI: 10.1111/tbed.13332

Within-Host Recombination in the Foot-and-Mouth Disease Virus Genome
journal, April 2018

  • Ferretti, Luca; Di Nardo, Antonello; Singer, Benjamin
  • Viruses, Vol. 10, Issue 5
  • DOI: 10.3390/v10050221

Within-Host Recombination in the Foot-and-Mouth Disease Virus Genome
journal, April 2018

  • Ferretti, Luca; Di Nardo, Antonello; Singer, Benjamin
  • Viruses, Vol. 10, Issue 5
  • DOI: 10.3390/v10050221

Knowledge and behavior of cattle and sheep owners and herders regarding foot-and-mouth disease in Northern Algeria
journal, August 2019