Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant Swine

Bovine viral diarrhea virus (BVDV) is one of the most economically important viruses of cattle, but this pathogen is also able to infect pigs, camelids, and a wide range of domestic and wild ruminants. BVDV isolates circulating in animal populations are genetically and antigenically highly diverse....

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Main Authors: Thibaud Kuca, Thomas Passler, Benjamin W. Newcomer, John D. Neill, Patricia K. Galik, Kay P. Riddell, Yijing Zhang, Darrell O. Bayles, Paul H. Walz
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.01138/full
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author Thibaud Kuca
Thomas Passler
Benjamin W. Newcomer
John D. Neill
Patricia K. Galik
Kay P. Riddell
Yijing Zhang
Darrell O. Bayles
Paul H. Walz
author_facet Thibaud Kuca
Thomas Passler
Benjamin W. Newcomer
John D. Neill
Patricia K. Galik
Kay P. Riddell
Yijing Zhang
Darrell O. Bayles
Paul H. Walz
author_sort Thibaud Kuca
collection DOAJ
description Bovine viral diarrhea virus (BVDV) is one of the most economically important viruses of cattle, but this pathogen is also able to infect pigs, camelids, and a wide range of domestic and wild ruminants. BVDV isolates circulating in animal populations are genetically and antigenically highly diverse. Acute BVDV infections in cattle cause the introduction of many substitutions in the viral genome. Serial infection of pregnant sheep with a BVDV-1b isolate of bovine origin was also associated with great numbers of substitutions. To our knowledge, genomic changes arising during BVDV infections in swine have not been investigated. The purpose of this study was to investigate the changes occurring in the open reading frame (ORF) of BVDV during serial infection of pregnant swine with a BVDV isolate of bovine origin. The BVDV-1b isolate AU526 was serially passaged in six pregnant gilts, two of which gave birth to live piglets congenitally infected with BVDV. The complete ORF sequences of 14 BVDV isolates obtained from pregnant gilts and their piglets were determined. Their analysis revealed that serial transmission of AU526 in pregnant swine resulted in many genomic changes. All isolates of porcine origin shared 32 nucleotide and 12 amino acid differences with the virus inoculum AU526. These changes were detected after a single passage in pregnant swine and were conserved during the subsequent five passages. Amino acid changes occurred primarily in genomic regions encoding the BVDV structural proteins E2 and Erns. These results suggest that BVDV infections in pregnant swine may contribute significantly to the genetic variability of BVDV and lead to the appearance of adaptive changes.
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spelling doaj.art-d8cd3764bc5c4d6382109089d382fcc12022-12-21T19:07:44ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-06-011110.3389/fmicb.2020.01138493141Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant SwineThibaud Kuca0Thomas Passler1Benjamin W. Newcomer2John D. Neill3Patricia K. Galik4Kay P. Riddell5Yijing Zhang6Darrell O. Bayles7Paul H. Walz8Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesDepartment of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesDepartment of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesRuminant Diseases and Immunology Research Unit, National Animal Disease Center, Agricultural Research Service, United States Department of Agriculture, Ames, IA, United StatesDepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesDepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesDepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesInfectious Bacterial Diseases Research Unit, National Animal Disease Center, Agricultural Research Service, United States Department of Agriculture, Ames, IA, United StatesDepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL, United StatesBovine viral diarrhea virus (BVDV) is one of the most economically important viruses of cattle, but this pathogen is also able to infect pigs, camelids, and a wide range of domestic and wild ruminants. BVDV isolates circulating in animal populations are genetically and antigenically highly diverse. Acute BVDV infections in cattle cause the introduction of many substitutions in the viral genome. Serial infection of pregnant sheep with a BVDV-1b isolate of bovine origin was also associated with great numbers of substitutions. To our knowledge, genomic changes arising during BVDV infections in swine have not been investigated. The purpose of this study was to investigate the changes occurring in the open reading frame (ORF) of BVDV during serial infection of pregnant swine with a BVDV isolate of bovine origin. The BVDV-1b isolate AU526 was serially passaged in six pregnant gilts, two of which gave birth to live piglets congenitally infected with BVDV. The complete ORF sequences of 14 BVDV isolates obtained from pregnant gilts and their piglets were determined. Their analysis revealed that serial transmission of AU526 in pregnant swine resulted in many genomic changes. All isolates of porcine origin shared 32 nucleotide and 12 amino acid differences with the virus inoculum AU526. These changes were detected after a single passage in pregnant swine and were conserved during the subsequent five passages. Amino acid changes occurred primarily in genomic regions encoding the BVDV structural proteins E2 and Erns. These results suggest that BVDV infections in pregnant swine may contribute significantly to the genetic variability of BVDV and lead to the appearance of adaptive changes.https://www.frontiersin.org/article/10.3389/fmicb.2020.01138/fullbovine viral diarrhea virusinterspecies transmissionopen reading framepersistent infectionpestivirusRNA virus
spellingShingle Thibaud Kuca
Thomas Passler
Benjamin W. Newcomer
John D. Neill
Patricia K. Galik
Kay P. Riddell
Yijing Zhang
Darrell O. Bayles
Paul H. Walz
Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant Swine
Frontiers in Microbiology
bovine viral diarrhea virus
interspecies transmission
open reading frame
persistent infection
pestivirus
RNA virus
title Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant Swine
title_full Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant Swine
title_fullStr Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant Swine
title_full_unstemmed Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant Swine
title_short Changes Introduced in the Open Reading Frame of Bovine Viral Diarrhea Virus During Serial Infection of Pregnant Swine
title_sort changes introduced in the open reading frame of bovine viral diarrhea virus during serial infection of pregnant swine
topic bovine viral diarrhea virus
interspecies transmission
open reading frame
persistent infection
pestivirus
RNA virus
url https://www.frontiersin.org/article/10.3389/fmicb.2020.01138/full
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