skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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:
Journal Article: 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},
url = {https://www.osti.gov/biblio/1627849}, journal = {PLoS ONE},
issn = {1932-6203},
number = 2,
volume = 13,
place = {United States},
year = {2018},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

Save / Share:

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


Foot-and-Mouth Disease
journal, April 2004


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


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


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


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


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


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


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


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


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


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


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


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


Molecular basis of pathogenesis of FMDV
journal, January 2003


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


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


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


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


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


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


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


Foot and mouth disease virus vaccines
journal, November 2009


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


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


MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001


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


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


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


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


Foot-And-Mouth Disease
journal, October 1968


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


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


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


    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


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