Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus

Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) is the most important endemic pathogen in the U.S. swine industry. Despite control efforts involving improved biosecurity and different vaccination protocols, the virus continues to circulate and evolve. One of the foremost challenges in it...

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Main Authors: Igor Adolfo Dexheimer Paploski, Cesar Corzo, Albert Rovira, Michael P. Murtaugh, Juan Manuel Sanhueza, Carles Vilalta, Declan C. Schroeder, Kimberly VanderWaal
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02486/full
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spelling doaj-8bd257f9810f476d94a8f1f5df2acddb2020-11-25T02:45:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-11-011010.3389/fmicb.2019.02486488085Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome VirusIgor Adolfo Dexheimer Paploski0Cesar Corzo1Albert Rovira2Michael P. Murtaugh3Juan Manuel Sanhueza4Carles Vilalta5Declan C. Schroeder6Declan C. Schroeder7Kimberly VanderWaal8Department of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN, United StatesDepartment of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN, United StatesDepartment of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN, United StatesDepartment of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, MN, United StatesDepartment of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN, United StatesDepartment of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN, United StatesDepartment of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN, United StatesSchool of Biological Sciences, University of Reading, Reading, United KingdomDepartment of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN, United StatesPorcine Reproductive and Respiratory Syndrome Virus (PRRSV) is the most important endemic pathogen in the U.S. swine industry. Despite control efforts involving improved biosecurity and different vaccination protocols, the virus continues to circulate and evolve. One of the foremost challenges in its control is high levels of genetic and antigenic diversity. Here, we quantify the co-circulation, emergence and sequential turnover of multiple PRRSV lineages in a single swine-producing region in the United States over a span of 9 years (2009–2017). By classifying over 4,000 PRRSV sequences (open-reading frame 5) into phylogenetic lineages and sub-lineages, we document the ongoing diversification and temporal dynamics of the PRRSV population, including the rapid emergence of a novel sub-lineage that appeared to be absent globally pre-2008. In addition, lineage 9 was the most prevalent lineage from 2009 to 2010, but its occurrence fell to 0.5% of all sequences identified per year after 2014, coinciding with the emergence or re-emergence of lineage 1 as the dominant lineage. The sequential dominance of different lineages, as well as three different sub-lineages within lineage 1, is consistent with the immune-mediated selection hypothesis for the sequential turnover in the dominant lineage. As host populations build immunity through natural infection or vaccination toward the most common variant, this dominant (sub-) lineage may be replaced by an emerging variant to which the population is more susceptible. An analysis of patterns of non- synonymous and synonymous mutations revealed evidence of positive selection on immunologically important regions of the genome, further supporting the potential that immune-mediated selection shapes the evolutionary and epidemiological dynamics for this virus. This has important implications for patterns of emergence and re-emergence of genetic variants of PRRSV that have negative impacts on the swine industry. Constant surveillance on PRRSV occurrence is crucial to a better understanding of the epidemiological and evolutionary dynamics of co-circulating viral lineages. Further studies utilizing whole genome sequencing and exploring the extent of cross-immunity between heterologous PRRS viruses could shed further light on PRRSV immunological response and aid in developing strategies that might be able to diminish disease impact.https://www.frontiersin.org/article/10.3389/fmicb.2019.02486/fullPRRSVepidemiologyecologyevolutionmulti-strain dynamicsemergence
collection DOAJ
language English
format Article
sources DOAJ
author Igor Adolfo Dexheimer Paploski
Cesar Corzo
Albert Rovira
Michael P. Murtaugh
Juan Manuel Sanhueza
Carles Vilalta
Declan C. Schroeder
Declan C. Schroeder
Kimberly VanderWaal
spellingShingle Igor Adolfo Dexheimer Paploski
Cesar Corzo
Albert Rovira
Michael P. Murtaugh
Juan Manuel Sanhueza
Carles Vilalta
Declan C. Schroeder
Declan C. Schroeder
Kimberly VanderWaal
Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus
Frontiers in Microbiology
PRRSV
epidemiology
ecology
evolution
multi-strain dynamics
emergence
author_facet Igor Adolfo Dexheimer Paploski
Cesar Corzo
Albert Rovira
Michael P. Murtaugh
Juan Manuel Sanhueza
Carles Vilalta
Declan C. Schroeder
Declan C. Schroeder
Kimberly VanderWaal
author_sort Igor Adolfo Dexheimer Paploski
title Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus
title_short Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus
title_full Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus
title_fullStr Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus
title_full_unstemmed Temporal Dynamics of Co-circulating Lineages of Porcine Reproductive and Respiratory Syndrome Virus
title_sort temporal dynamics of co-circulating lineages of porcine reproductive and respiratory syndrome virus
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-11-01
description Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) is the most important endemic pathogen in the U.S. swine industry. Despite control efforts involving improved biosecurity and different vaccination protocols, the virus continues to circulate and evolve. One of the foremost challenges in its control is high levels of genetic and antigenic diversity. Here, we quantify the co-circulation, emergence and sequential turnover of multiple PRRSV lineages in a single swine-producing region in the United States over a span of 9 years (2009–2017). By classifying over 4,000 PRRSV sequences (open-reading frame 5) into phylogenetic lineages and sub-lineages, we document the ongoing diversification and temporal dynamics of the PRRSV population, including the rapid emergence of a novel sub-lineage that appeared to be absent globally pre-2008. In addition, lineage 9 was the most prevalent lineage from 2009 to 2010, but its occurrence fell to 0.5% of all sequences identified per year after 2014, coinciding with the emergence or re-emergence of lineage 1 as the dominant lineage. The sequential dominance of different lineages, as well as three different sub-lineages within lineage 1, is consistent with the immune-mediated selection hypothesis for the sequential turnover in the dominant lineage. As host populations build immunity through natural infection or vaccination toward the most common variant, this dominant (sub-) lineage may be replaced by an emerging variant to which the population is more susceptible. An analysis of patterns of non- synonymous and synonymous mutations revealed evidence of positive selection on immunologically important regions of the genome, further supporting the potential that immune-mediated selection shapes the evolutionary and epidemiological dynamics for this virus. This has important implications for patterns of emergence and re-emergence of genetic variants of PRRSV that have negative impacts on the swine industry. Constant surveillance on PRRSV occurrence is crucial to a better understanding of the epidemiological and evolutionary dynamics of co-circulating viral lineages. Further studies utilizing whole genome sequencing and exploring the extent of cross-immunity between heterologous PRRS viruses could shed further light on PRRSV immunological response and aid in developing strategies that might be able to diminish disease impact.
topic PRRSV
epidemiology
ecology
evolution
multi-strain dynamics
emergence
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02486/full
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