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

Abstract

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 shiftsmore » 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.« less

Authors:
 [1];  [2];  [1]; ORCiD logo [3]; ORCiD logo [3];  [4];  [1];  [5];  [1]; ORCiD logo [4]
  1. US Dept. of Agriculture (USDA)., Greenport, NY (United States). Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS
  2. US Dept. of Agriculture (USDA)., Greenport, NY (United States). Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS; Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
  3. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  4. US Dept. of Agriculture (USDA)., Greenport, NY (United States). Foreign Animal Disease Research Unit, Plum Island Animal Disease Center, ARS; Univ. of Minnesota, St Paul, MN (United States). Dept. of Veterinary Population Medicine
  5. Univ. of Wisconsin-Madison, Stoughton, WI (United States). Synchrotron Radiation Center (SRC). Dept. of Pathobiological Sciences, School of Veterinary Medicine
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
U.S. Department of Homeland Security; USDOE
OSTI Identifier:
1511607
Report Number(s):
LA-UR-18-27558
Journal ID: ISSN 1932-6203
Grant/Contract Number:  
89233218CNA000001
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 14; Journal Issue: 4; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; Biological Science; Foot-and-mouth disease; FMD; cattle; Animal phylogenetics; Veterinary diseases

Citation Formats

Arzt, Jonathan, Fish, Ian, Pauszek, Steven J., Johnson, Shannon Lyn, Chain, Patrick S., Rai, Devendra K., Rieder, Elizabeth, Goldberg, Tony L., Rodriguez, Luis L., and Stenfeldt, Carolina. The evolution of a super-swarm of foot-and-mouth disease virus in cattle. United States: N. p., 2019. Web. doi:10.1371/journal.pone.0210847.
Arzt, Jonathan, Fish, Ian, Pauszek, Steven J., Johnson, Shannon Lyn, Chain, Patrick S., Rai, Devendra K., Rieder, Elizabeth, Goldberg, Tony L., Rodriguez, Luis L., & Stenfeldt, Carolina. The evolution of a super-swarm of foot-and-mouth disease virus in cattle. United States. doi:10.1371/journal.pone.0210847.
Arzt, Jonathan, Fish, Ian, Pauszek, Steven J., Johnson, Shannon Lyn, Chain, Patrick S., Rai, Devendra K., Rieder, Elizabeth, Goldberg, Tony L., Rodriguez, Luis L., and Stenfeldt, Carolina. Thu . "The evolution of a super-swarm of foot-and-mouth disease virus in cattle". United States. doi:10.1371/journal.pone.0210847. https://www.osti.gov/servlets/purl/1511607.
@article{osti_1511607,
title = {The evolution of a super-swarm of foot-and-mouth disease virus in cattle},
author = {Arzt, Jonathan and Fish, Ian and Pauszek, Steven J. and Johnson, Shannon Lyn and Chain, Patrick S. and Rai, Devendra K. and Rieder, Elizabeth and Goldberg, Tony L. and Rodriguez, Luis L. and Stenfeldt, Carolina},
abstractNote = {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.},
doi = {10.1371/journal.pone.0210847},
journal = {PLoS ONE},
number = 4,
volume = 14,
place = {United States},
year = {2019},
month = {4}
}

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Cited by: 5 works
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Figures / Tables:

Fig 1 Fig 1: Subconsensus variants present above 2% frequency in inoculum ultra-deep sequencing. Reference is the consensus sequence of the inoculum and minority represents the polymorphic base at each site. Nucleotide variation was not detected in inoculum 2A and 3B1-3 coding regions. Sample count indicates the number of sample consensus sequencesmore » (of 52 total) that encoded each nucleotide found at the minority (2–49%) level in the inoculum deep sequence. Animal count indicates the number of individual hosts that provided sequences with these variants of the 13 total. If no value is indicated (-), no sample sequence encoded the inoculum’s minority nucleotide at the consensus level. Roman numerals and colors indicate the presence of each specific site change in at least one clade member as described in Results: Phylogenetic Associations.« less

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    Works referencing / citing this record:

    Development and evaluation of multiplex real‐time RT‐PCR assays for the detection and differentiation of foot‐and‐mouth disease virus and Seneca Valley virus 1
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