Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United States
For the first time, we describe phylogenomic signatures of an epidemic lineage of vesicular stomatitis Indiana virus (VSIV). We applied multiple evolutionary analyses to a dataset of 87 full-length genome sequences representing the circulation of an epidemic VSIV lineage in the US between 2019 and 2...
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2024-11-01
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| Online Access: | https://www.mdpi.com/1999-4915/16/11/1803 |
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| author | Selene Zarate Miranda Bertram Case Rodgers Kirsten Reed Angela Pelzel-McCluskey Ninnet Gomez-Romero Luis L. Rodriguez Christie Mayo Chad Mire Sergei L. Kosakovsky Pond Lauro Velazquez-Salinas |
| author_facet | Selene Zarate Miranda Bertram Case Rodgers Kirsten Reed Angela Pelzel-McCluskey Ninnet Gomez-Romero Luis L. Rodriguez Christie Mayo Chad Mire Sergei L. Kosakovsky Pond Lauro Velazquez-Salinas |
| author_sort | Selene Zarate |
| collection | DOAJ |
| description | For the first time, we describe phylogenomic signatures of an epidemic lineage of vesicular stomatitis Indiana virus (VSIV). We applied multiple evolutionary analyses to a dataset of 87 full-length genome sequences representing the circulation of an epidemic VSIV lineage in the US between 2019 and 2020. Based on phylogenetic analyses, we predicted the ancestral relationship of this lineage with a specific group of isolates circulating in the endemic zone of Chiapas, Mexico. Subsequently, our findings indicate that the lineage diversified into at least four different subpopulations during its circulation in the US. We identified single nucleotide polymorphisms (SNPs) that differentiate viral subpopulations and assessed their potential relevance using comparative phylogenetic methods, highlighting the preponderance of synonymous mutations during the differentiation of these populations. Purifying selection was the main evolutionary force favoring the conservation of this epidemic phenotype, with P and G genes as the main drivers of the evolution of this lineage. Our analyses identified multiple codon sites under positive selection and the association of these sites with specific functional domains at P, M, G, and L proteins. Based on ancestral reconstruction analyses, we showed the potential relevance of some of the sites identified under positive selection to the adaptation of the epidemic lineage at the population level. Finally, using a representative group of viruses from Colorado, we established a positive correlation between genetic and geographical distances, suggesting that positive selection on specific codon positions might have favored the adaptation of different subpopulations to circulation in specific geographical settings. Collectively, our study reveals the complex dynamics that accompany the evolution of an epidemic lineage of VSIV in nature. Our analytical framework provides a model for conducting future evolutionary analyses. The ultimate goal is to support the implementation of an early warning system for vesicular stomatitis virus in the US, enabling early detection of epidemic precursors from Mexico. |
| format | Article |
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| institution | Kabale University |
| issn | 1999-4915 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj-art-f23137f6c1344e47b13bcf3b28c9607f2024-11-26T18:25:43ZengMDPI AGViruses1999-49152024-11-011611180310.3390/v16111803Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United StatesSelene Zarate0Miranda Bertram1Case Rodgers2Kirsten Reed3Angela Pelzel-McCluskey4Ninnet Gomez-Romero5Luis L. Rodriguez6Christie Mayo7Chad Mire8Sergei L. Kosakovsky Pond9Lauro Velazquez-Salinas10Posgrado en Ciencias Genómicas, Universidad Autónoma de la Ciudad de Mexico, Ciudad de Mexico 03100, MexicoNational Bio-and Agro-defense Facility, Agricultural Research Services, United States Department of Agriculture, Manhattan, KS 66506, USADepartment of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USADepartment of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USAUnited States Department of Agriculture, Animal and Plant Health Inspection Service, Veterinary Services, Fort Collins, CO 80521, USADepartamento de Microbiología e Inmunología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Av. Universidad No. 3000 Col Copilco Universidad, Mexico City 14510, MexicoNational Bio-and Agro-defense Facility, Agricultural Research Services, United States Department of Agriculture, Manhattan, KS 66506, USADepartment of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USANational Bio-and Agro-defense Facility, Agricultural Research Services, United States Department of Agriculture, Manhattan, KS 66506, USAInstitute for Genomics and Evolutionary Medicine, Department of Biology, Temple University, Philadelphia, PA 19122, USANational Bio-and Agro-defense Facility, Agricultural Research Services, United States Department of Agriculture, Manhattan, KS 66506, USAFor the first time, we describe phylogenomic signatures of an epidemic lineage of vesicular stomatitis Indiana virus (VSIV). We applied multiple evolutionary analyses to a dataset of 87 full-length genome sequences representing the circulation of an epidemic VSIV lineage in the US between 2019 and 2020. Based on phylogenetic analyses, we predicted the ancestral relationship of this lineage with a specific group of isolates circulating in the endemic zone of Chiapas, Mexico. Subsequently, our findings indicate that the lineage diversified into at least four different subpopulations during its circulation in the US. We identified single nucleotide polymorphisms (SNPs) that differentiate viral subpopulations and assessed their potential relevance using comparative phylogenetic methods, highlighting the preponderance of synonymous mutations during the differentiation of these populations. Purifying selection was the main evolutionary force favoring the conservation of this epidemic phenotype, with P and G genes as the main drivers of the evolution of this lineage. Our analyses identified multiple codon sites under positive selection and the association of these sites with specific functional domains at P, M, G, and L proteins. Based on ancestral reconstruction analyses, we showed the potential relevance of some of the sites identified under positive selection to the adaptation of the epidemic lineage at the population level. Finally, using a representative group of viruses from Colorado, we established a positive correlation between genetic and geographical distances, suggesting that positive selection on specific codon positions might have favored the adaptation of different subpopulations to circulation in specific geographical settings. Collectively, our study reveals the complex dynamics that accompany the evolution of an epidemic lineage of VSIV in nature. Our analytical framework provides a model for conducting future evolutionary analyses. The ultimate goal is to support the implementation of an early warning system for vesicular stomatitis virus in the US, enabling early detection of epidemic precursors from Mexico.https://www.mdpi.com/1999-4915/16/11/1803vesicular stomatitis virusevolutionpositive selectionnegative selectionepidemic lineagesnatural selection |
| spellingShingle | Selene Zarate Miranda Bertram Case Rodgers Kirsten Reed Angela Pelzel-McCluskey Ninnet Gomez-Romero Luis L. Rodriguez Christie Mayo Chad Mire Sergei L. Kosakovsky Pond Lauro Velazquez-Salinas Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United States Viruses vesicular stomatitis virus evolution positive selection negative selection epidemic lineages natural selection |
| title | Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United States |
| title_full | Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United States |
| title_fullStr | Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United States |
| title_full_unstemmed | Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United States |
| title_short | Phylogenomic Signatures of a Lineage of Vesicular Stomatitis Indiana Virus Circulating During the 2019–2020 Epidemic in the United States |
| title_sort | phylogenomic signatures of a lineage of vesicular stomatitis indiana virus circulating during the 2019 2020 epidemic in the united states |
| topic | vesicular stomatitis virus evolution positive selection negative selection epidemic lineages natural selection |
| url | https://www.mdpi.com/1999-4915/16/11/1803 |
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