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Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus
Lumpy skin disease virus (LSDV) causes a disease of economic importance affecting cattle. Its global epidemiology is complex due to the combination of vector-borne and anthropogenic spread, the circulation of vaccine-like recombinants, and the use of vaccines. The slow molecular evolution of its DNA...
Autores principales: | , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10688313/ https://www.ncbi.nlm.nih.gov/pubmed/37905838 http://dx.doi.org/10.1128/jvi.01394-23 |
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author | Van Borm, Steven Dellicour, Simon Martin, Darren P. Lemey, Philippe Agianniotaki, Eirini I. Chondrokouki, Eleni D. Vidanovic, Dejan Vaskovic, Nikola Petroviċ, Tamaš Laziċ, Sava Koleci, Xhelil Vodica, Ani Djadjovski, Igor Krstevski, Kiril Vandenbussche, Frank Haegeman, Andy De Clercq, Kris Mathijs, Elisabeth |
author_facet | Van Borm, Steven Dellicour, Simon Martin, Darren P. Lemey, Philippe Agianniotaki, Eirini I. Chondrokouki, Eleni D. Vidanovic, Dejan Vaskovic, Nikola Petroviċ, Tamaš Laziċ, Sava Koleci, Xhelil Vodica, Ani Djadjovski, Igor Krstevski, Kiril Vandenbussche, Frank Haegeman, Andy De Clercq, Kris Mathijs, Elisabeth |
author_sort | Van Borm, Steven |
collection | PubMed |
description | Lumpy skin disease virus (LSDV) causes a disease of economic importance affecting cattle. Its global epidemiology is complex due to the combination of vector-borne and anthropogenic spread, the circulation of vaccine-like recombinants, and the use of vaccines. The slow molecular evolution of its DNA genome limits the utility of genetic variation for accurate tracing based on evolutionary analyses, but this limitation has not yet been formally assessed. Furthermore, until present, whole genome sequencing in affected areas has remained patchy. This study combines the first fine-grained sampling of LSDV whole genomes from a time-constrained (2015–2017) southeastern European (SEE) LSDV outbreak, which we analyze along with curated public genomes to investigate the global and regional viral dispersal dynamics. First, haplotype networks visualizing the limited genetic variability associated with the SEE LSDV outbreak show intense intermixing between countries. We also assess at which spatial scale a correlation between genetic and geographic distances can be detected for LSDV. On a global scale, we show the importance of accounting for recombination events that can impact phylogenetic and phylogeographic reconstructions. Following the assessment of the temporal signal in the recombination-free alignment, our time-scaled continuous phylogeographic analysis of Kenya-like and recent wild-type viruses confirms the origin and global dissemination history of LSDV. Our analyses highlight the importance of careful selection and application of phylodynamic approaches to DNA viruses, as well as the importance of whole genome sampling in endemic and outbreak areas to improve our understanding of the evolution, epidemiology, and transmission dynamics of DNA viruses. IMPORTANCE: Lumpy skin disease virus (LSDV) has a complex epidemiology involving multiple strains, recombination, and vaccination. Its DNA genome provides limited genetic variation to trace outbreaks in space and time. Sequencing of LSDV whole genomes has also been patchy at global and regional scales. Here, we provide the first fine-grained whole genome sequence sampling of a constrained LSDV outbreak (southeastern Europe, 2015–2017), which we analyze along with global publicly available genomes. We formally evaluate the past occurrence of recombination events as well as the temporal signal that is required for calibrating molecular clock models and subsequently conduct a time-calibrated spatially explicit phylogeographic reconstruction. Our study further illustrates the importance of accounting for recombination events before reconstructing global and regional dynamics of DNA viruses. More LSDV whole genomes from endemic areas are needed to obtain a comprehensive understanding of global LSDV dispersal dynamics. |
format | Online Article Text |
id | pubmed-10688313 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-106883132023-12-01 Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus Van Borm, Steven Dellicour, Simon Martin, Darren P. Lemey, Philippe Agianniotaki, Eirini I. Chondrokouki, Eleni D. Vidanovic, Dejan Vaskovic, Nikola Petroviċ, Tamaš Laziċ, Sava Koleci, Xhelil Vodica, Ani Djadjovski, Igor Krstevski, Kiril Vandenbussche, Frank Haegeman, Andy De Clercq, Kris Mathijs, Elisabeth J Virol Genetic Diversity and Evolution Lumpy skin disease virus (LSDV) causes a disease of economic importance affecting cattle. Its global epidemiology is complex due to the combination of vector-borne and anthropogenic spread, the circulation of vaccine-like recombinants, and the use of vaccines. The slow molecular evolution of its DNA genome limits the utility of genetic variation for accurate tracing based on evolutionary analyses, but this limitation has not yet been formally assessed. Furthermore, until present, whole genome sequencing in affected areas has remained patchy. This study combines the first fine-grained sampling of LSDV whole genomes from a time-constrained (2015–2017) southeastern European (SEE) LSDV outbreak, which we analyze along with curated public genomes to investigate the global and regional viral dispersal dynamics. First, haplotype networks visualizing the limited genetic variability associated with the SEE LSDV outbreak show intense intermixing between countries. We also assess at which spatial scale a correlation between genetic and geographic distances can be detected for LSDV. On a global scale, we show the importance of accounting for recombination events that can impact phylogenetic and phylogeographic reconstructions. Following the assessment of the temporal signal in the recombination-free alignment, our time-scaled continuous phylogeographic analysis of Kenya-like and recent wild-type viruses confirms the origin and global dissemination history of LSDV. Our analyses highlight the importance of careful selection and application of phylodynamic approaches to DNA viruses, as well as the importance of whole genome sampling in endemic and outbreak areas to improve our understanding of the evolution, epidemiology, and transmission dynamics of DNA viruses. IMPORTANCE: Lumpy skin disease virus (LSDV) has a complex epidemiology involving multiple strains, recombination, and vaccination. Its DNA genome provides limited genetic variation to trace outbreaks in space and time. Sequencing of LSDV whole genomes has also been patchy at global and regional scales. Here, we provide the first fine-grained whole genome sequence sampling of a constrained LSDV outbreak (southeastern Europe, 2015–2017), which we analyze along with global publicly available genomes. We formally evaluate the past occurrence of recombination events as well as the temporal signal that is required for calibrating molecular clock models and subsequently conduct a time-calibrated spatially explicit phylogeographic reconstruction. Our study further illustrates the importance of accounting for recombination events before reconstructing global and regional dynamics of DNA viruses. More LSDV whole genomes from endemic areas are needed to obtain a comprehensive understanding of global LSDV dispersal dynamics. American Society for Microbiology 2023-10-31 /pmc/articles/PMC10688313/ /pubmed/37905838 http://dx.doi.org/10.1128/jvi.01394-23 Text en Copyright © 2023 Van Borm et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Genetic Diversity and Evolution Van Borm, Steven Dellicour, Simon Martin, Darren P. Lemey, Philippe Agianniotaki, Eirini I. Chondrokouki, Eleni D. Vidanovic, Dejan Vaskovic, Nikola Petroviċ, Tamaš Laziċ, Sava Koleci, Xhelil Vodica, Ani Djadjovski, Igor Krstevski, Kiril Vandenbussche, Frank Haegeman, Andy De Clercq, Kris Mathijs, Elisabeth Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus |
title | Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus |
title_full | Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus |
title_fullStr | Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus |
title_full_unstemmed | Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus |
title_short | Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus |
title_sort | complete genome reconstruction of the global and european regional dispersal history of the lumpy skin disease virus |
topic | Genetic Diversity and Evolution |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10688313/ https://www.ncbi.nlm.nih.gov/pubmed/37905838 http://dx.doi.org/10.1128/jvi.01394-23 |
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