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Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution

BACKGROUND: African swine fever virus (ASFV) is a most devastating pathogen affecting swine. In 2007, ASFV was introduced into Eastern Europe where it continuously circulates and recently reached Western Europe and Asia, leading to a socio-economic crisis of global proportion. In Africa, where ASFV...

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Autores principales: Forth, Jan H., Forth, Leonie F., Lycett, Samantha, Bell-Sakyi, Lesley, Keil, Günther M., Blome, Sandra, Calvignac-Spencer, Sébastien, Wissgott, Antje, Krause, Johannes, Höper, Dirk, Kampen, Helge, Beer, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7542975/
https://www.ncbi.nlm.nih.gov/pubmed/33032594
http://dx.doi.org/10.1186/s12915-020-00865-6
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author Forth, Jan H.
Forth, Leonie F.
Lycett, Samantha
Bell-Sakyi, Lesley
Keil, Günther M.
Blome, Sandra
Calvignac-Spencer, Sébastien
Wissgott, Antje
Krause, Johannes
Höper, Dirk
Kampen, Helge
Beer, Martin
author_facet Forth, Jan H.
Forth, Leonie F.
Lycett, Samantha
Bell-Sakyi, Lesley
Keil, Günther M.
Blome, Sandra
Calvignac-Spencer, Sébastien
Wissgott, Antje
Krause, Johannes
Höper, Dirk
Kampen, Helge
Beer, Martin
author_sort Forth, Jan H.
collection PubMed
description BACKGROUND: African swine fever virus (ASFV) is a most devastating pathogen affecting swine. In 2007, ASFV was introduced into Eastern Europe where it continuously circulates and recently reached Western Europe and Asia, leading to a socio-economic crisis of global proportion. In Africa, where ASFV was first described in 1921, it is transmitted between warthogs and soft ticks of the genus Ornithodoros in a so-called sylvatic cycle. However, analyses into this virus’ evolution are aggravated by the absence of any closely related viruses. Even ancient endogenous viral elements, viral sequences integrated into a host’s genome many thousand years ago that have proven extremely valuable to analyse virus evolution, remain to be identified. Therefore, the evolution of ASFV, the only known DNA virus transmitted by arthropods, remains a mystery. RESULTS: For the identification of ASFV-like sequences, we sequenced DNA from different recent Ornithodoros tick species, e.g. O. moubata and O. porcinus, O. moubata tick cells and also 100-year-old O. moubata and O. porcinus ticks using high-throughput sequencing. We used BLAST analyses for the identification of ASFV-like sequences and further analysed the data through phylogenetic reconstruction and molecular clock analyses. In addition, we performed tick infection experiments as well as additional small RNA sequencing of O. moubata and O. porcinus soft ticks. CONCLUSION: Here, we show that soft ticks of the Ornithodoros moubata group, the natural arthropod vector of ASFV, harbour African swine fever virus-like integrated (ASFLI) elements corresponding to up to 10% (over 20 kb) of the ASFV genome. Through orthologous dating and molecular clock analyses, we provide data suggesting that integration could have occurred over 1.47 million years ago. Furthermore, we provide data showing ASFLI-element specific siRNA and piRNA in ticks and tick cells allowing for speculations on a possible role of ASFLI-elements in RNA interference-based protection against ASFV in ticks. We suggest that these elements, shaped through many years of co-evolution, could be part of an evolutionary virus-vector ‘arms race’, a finding that has not only high impact on our understanding of the co-evolution of viruses with their hosts but also provides a glimpse into the evolution of ASFV.
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spelling pubmed-75429752020-10-13 Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution Forth, Jan H. Forth, Leonie F. Lycett, Samantha Bell-Sakyi, Lesley Keil, Günther M. Blome, Sandra Calvignac-Spencer, Sébastien Wissgott, Antje Krause, Johannes Höper, Dirk Kampen, Helge Beer, Martin BMC Biol Research Article BACKGROUND: African swine fever virus (ASFV) is a most devastating pathogen affecting swine. In 2007, ASFV was introduced into Eastern Europe where it continuously circulates and recently reached Western Europe and Asia, leading to a socio-economic crisis of global proportion. In Africa, where ASFV was first described in 1921, it is transmitted between warthogs and soft ticks of the genus Ornithodoros in a so-called sylvatic cycle. However, analyses into this virus’ evolution are aggravated by the absence of any closely related viruses. Even ancient endogenous viral elements, viral sequences integrated into a host’s genome many thousand years ago that have proven extremely valuable to analyse virus evolution, remain to be identified. Therefore, the evolution of ASFV, the only known DNA virus transmitted by arthropods, remains a mystery. RESULTS: For the identification of ASFV-like sequences, we sequenced DNA from different recent Ornithodoros tick species, e.g. O. moubata and O. porcinus, O. moubata tick cells and also 100-year-old O. moubata and O. porcinus ticks using high-throughput sequencing. We used BLAST analyses for the identification of ASFV-like sequences and further analysed the data through phylogenetic reconstruction and molecular clock analyses. In addition, we performed tick infection experiments as well as additional small RNA sequencing of O. moubata and O. porcinus soft ticks. CONCLUSION: Here, we show that soft ticks of the Ornithodoros moubata group, the natural arthropod vector of ASFV, harbour African swine fever virus-like integrated (ASFLI) elements corresponding to up to 10% (over 20 kb) of the ASFV genome. Through orthologous dating and molecular clock analyses, we provide data suggesting that integration could have occurred over 1.47 million years ago. Furthermore, we provide data showing ASFLI-element specific siRNA and piRNA in ticks and tick cells allowing for speculations on a possible role of ASFLI-elements in RNA interference-based protection against ASFV in ticks. We suggest that these elements, shaped through many years of co-evolution, could be part of an evolutionary virus-vector ‘arms race’, a finding that has not only high impact on our understanding of the co-evolution of viruses with their hosts but also provides a glimpse into the evolution of ASFV. BioMed Central 2020-10-08 /pmc/articles/PMC7542975/ /pubmed/33032594 http://dx.doi.org/10.1186/s12915-020-00865-6 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Forth, Jan H.
Forth, Leonie F.
Lycett, Samantha
Bell-Sakyi, Lesley
Keil, Günther M.
Blome, Sandra
Calvignac-Spencer, Sébastien
Wissgott, Antje
Krause, Johannes
Höper, Dirk
Kampen, Helge
Beer, Martin
Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution
title Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution
title_full Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution
title_fullStr Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution
title_full_unstemmed Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution
title_short Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution
title_sort identification of african swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7542975/
https://www.ncbi.nlm.nih.gov/pubmed/33032594
http://dx.doi.org/10.1186/s12915-020-00865-6
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