Virus adaptation and selection following challenge of animals vaccinated against classical swine fever virus

Ulrik Fahnøe; Anders Gorm Pedersen; Camille Melissa Johnston; Richard J. Orton; Dirk Höper; Martin Beer; Jens Bukh; Graham J. Belsham; Thomas Bruun Rasmussen

doi:10.3390/v11100932

Virus adaptation and selection following challenge of animals vaccinated against classical swine fever virus

Ulrik Fahnøe, Anders Gorm Pedersen, Camille Melissa Johnston, Richard J. Orton, Dirk Höper, Martin Beer, Jens Bukh, Graham J. Belsham, Thomas Bruun Rasmussen^*

^*Corresponding author af dette arbejde

4 Citationer (Scopus)

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Abstract

Vaccines against classical swine fever have proven very effective in protecting pigs from this deadly disease. However, little is known about how vaccination impacts the selective pressures acting on the classical swine fever virus (CSFV). Here we use high-throughput sequencing of viral genomes to investigate evolutionary changes in virus populations following the challenge of naïve and vaccinated pigs with the highly virulent CSFV strain "Koslov". The challenge inoculum contained an ensemble of closely related viral sequences, with three major haplotypes being present, termed A, B, and C. After the challenge, the viral haplotype A was preferentially located within the tonsils of naïve animals but was highly prevalent in the sera of all vaccinated animals. We find that the viral population structure in naïve pigs after infection is very similar to that in the original inoculum. In contrast, the viral population in vaccinated pigs, which only underwent transient low-level viremia, displayed several distinct changes including the emergence of 16 unique non-synonymous single nucleotide polymorphisms (SNPs) that were not detectable in the challenge inoculum. Further analysis showed a significant loss of heterogeneity and an increasing positive selection acting on the virus populations in the vaccinated pigs. We conclude that vaccination imposes a strong selective pressure on viruses that subsequently replicate within the vaccinated animal.

Originalsprog	Engelsk
Artikelnummer	932
Tidsskrift	Viruses
Vol/bind	11
Udgave nummer	10
ISSN	1999-4915
DOI	https://doi.org/10.3390/v11100932
Status	Udgivet - 2019

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10.3390/v11100932Licens: CC BY

Virus Adaptation and Selection Following Challenge of Animals Vaccinated against Classical Swine Fever VirusForlagets udgivne version, 1,9 MBLicens: CC BY

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title = "Virus adaptation and selection following challenge of animals vaccinated against classical swine fever virus",

abstract = "Vaccines against classical swine fever have proven very effective in protecting pigs from this deadly disease. However, little is known about how vaccination impacts the selective pressures acting on the classical swine fever virus (CSFV). Here we use high-throughput sequencing of viral genomes to investigate evolutionary changes in virus populations following the challenge of na{\"i}ve and vaccinated pigs with the highly virulent CSFV strain {"}Koslov{"}. The challenge inoculum contained an ensemble of closely related viral sequences, with three major haplotypes being present, termed A, B, and C. After the challenge, the viral haplotype A was preferentially located within the tonsils of na{\"i}ve animals but was highly prevalent in the sera of all vaccinated animals. We find that the viral population structure in na{\"i}ve pigs after infection is very similar to that in the original inoculum. In contrast, the viral population in vaccinated pigs, which only underwent transient low-level viremia, displayed several distinct changes including the emergence of 16 unique non-synonymous single nucleotide polymorphisms (SNPs) that were not detectable in the challenge inoculum. Further analysis showed a significant loss of heterogeneity and an increasing positive selection acting on the virus populations in the vaccinated pigs. We conclude that vaccination imposes a strong selective pressure on viruses that subsequently replicate within the vaccinated animal.",

keywords = "Classical swine fever virus, CSFV, Deep sequencing, Haplotype selection, Vaccination, Viral populations, Virulence, Virus evolution",

author = "Ulrik Fahn{\o}e and Pedersen, {Anders Gorm} and Johnston, {Camille Melissa} and Orton, {Richard J.} and Dirk H{\"o}per and Martin Beer and Jens Bukh and Belsham, {Graham J.} and Rasmussen, {Thomas Bruun}",

year = "2019",

doi = "10.3390/v11100932",

language = "English",

volume = "11",

journal = "Viruses",

issn = "1999-4915",

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TY - JOUR

T1 - Virus adaptation and selection following challenge of animals vaccinated against classical swine fever virus

AU - Fahnøe, Ulrik

AU - Pedersen, Anders Gorm

AU - Johnston, Camille Melissa

AU - Orton, Richard J.

AU - Höper, Dirk

AU - Beer, Martin

AU - Bukh, Jens

AU - Belsham, Graham J.

AU - Rasmussen, Thomas Bruun

PY - 2019

Y1 - 2019

N2 - Vaccines against classical swine fever have proven very effective in protecting pigs from this deadly disease. However, little is known about how vaccination impacts the selective pressures acting on the classical swine fever virus (CSFV). Here we use high-throughput sequencing of viral genomes to investigate evolutionary changes in virus populations following the challenge of naïve and vaccinated pigs with the highly virulent CSFV strain "Koslov". The challenge inoculum contained an ensemble of closely related viral sequences, with three major haplotypes being present, termed A, B, and C. After the challenge, the viral haplotype A was preferentially located within the tonsils of naïve animals but was highly prevalent in the sera of all vaccinated animals. We find that the viral population structure in naïve pigs after infection is very similar to that in the original inoculum. In contrast, the viral population in vaccinated pigs, which only underwent transient low-level viremia, displayed several distinct changes including the emergence of 16 unique non-synonymous single nucleotide polymorphisms (SNPs) that were not detectable in the challenge inoculum. Further analysis showed a significant loss of heterogeneity and an increasing positive selection acting on the virus populations in the vaccinated pigs. We conclude that vaccination imposes a strong selective pressure on viruses that subsequently replicate within the vaccinated animal.

AB - Vaccines against classical swine fever have proven very effective in protecting pigs from this deadly disease. However, little is known about how vaccination impacts the selective pressures acting on the classical swine fever virus (CSFV). Here we use high-throughput sequencing of viral genomes to investigate evolutionary changes in virus populations following the challenge of naïve and vaccinated pigs with the highly virulent CSFV strain "Koslov". The challenge inoculum contained an ensemble of closely related viral sequences, with three major haplotypes being present, termed A, B, and C. After the challenge, the viral haplotype A was preferentially located within the tonsils of naïve animals but was highly prevalent in the sera of all vaccinated animals. We find that the viral population structure in naïve pigs after infection is very similar to that in the original inoculum. In contrast, the viral population in vaccinated pigs, which only underwent transient low-level viremia, displayed several distinct changes including the emergence of 16 unique non-synonymous single nucleotide polymorphisms (SNPs) that were not detectable in the challenge inoculum. Further analysis showed a significant loss of heterogeneity and an increasing positive selection acting on the virus populations in the vaccinated pigs. We conclude that vaccination imposes a strong selective pressure on viruses that subsequently replicate within the vaccinated animal.

KW - Classical swine fever virus

KW - CSFV

KW - Deep sequencing

KW - Haplotype selection

KW - Vaccination

KW - Viral populations

KW - Virulence

KW - Virus evolution

U2 - 10.3390/v11100932

DO - 10.3390/v11100932

M3 - Journal article

C2 - 31658773

AN - SCOPUS:85074240212

SN - 1999-4915

VL - 11

JO - Viruses

JF - Viruses

IS - 10

M1 - 932

ER -

Virus adaptation and selection following challenge of animals vaccinated against classical swine fever virus

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