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

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 s...

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Main Authors: Jonathan Arzt, Ian Fish, Steven J Pauszek, Shannon L Johnson, Patrick S Chain, Devendra K Rai, Elizabeth Rieder, Tony L Goldberg, Luis L Rodriguez, Carolina Stenfeldt
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0210847
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author Jonathan Arzt
Ian Fish
Steven J Pauszek
Shannon L Johnson
Patrick S Chain
Devendra K Rai
Elizabeth Rieder
Tony L Goldberg
Luis L Rodriguez
Carolina Stenfeldt
author_facet Jonathan Arzt
Ian Fish
Steven J Pauszek
Shannon L Johnson
Patrick S Chain
Devendra K Rai
Elizabeth Rieder
Tony L Goldberg
Luis L Rodriguez
Carolina Stenfeldt
author_sort Jonathan Arzt
collection DOAJ
description 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.
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spelling doaj.art-fd95b7e1ee24476b95a24680a1f39f512022-12-21T19:18:05ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-01144e021084710.1371/journal.pone.0210847The evolution of a super-swarm of foot-and-mouth disease virus in cattle.Jonathan ArztIan FishSteven J PauszekShannon L JohnsonPatrick S ChainDevendra K RaiElizabeth RiederTony L GoldbergLuis L RodriguezCarolina StenfeldtFoot-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.https://doi.org/10.1371/journal.pone.0210847
spellingShingle Jonathan Arzt
Ian Fish
Steven J Pauszek
Shannon L Johnson
Patrick S Chain
Devendra K Rai
Elizabeth Rieder
Tony L Goldberg
Luis L Rodriguez
Carolina Stenfeldt
The evolution of a super-swarm of foot-and-mouth disease virus in cattle.
PLoS ONE
title The evolution of a super-swarm of foot-and-mouth disease virus in cattle.
title_full The evolution of a super-swarm of foot-and-mouth disease virus in cattle.
title_fullStr The evolution of a super-swarm of foot-and-mouth disease virus in cattle.
title_full_unstemmed The evolution of a super-swarm of foot-and-mouth disease virus in cattle.
title_short The evolution of a super-swarm of foot-and-mouth disease virus in cattle.
title_sort evolution of a super swarm of foot and mouth disease virus in cattle
url https://doi.org/10.1371/journal.pone.0210847
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