Genomic characterization of 99 viruses from the bunyavirus families Nairoviridae, Peribunyaviridae, and Phenuiviridae, including 35 previously unsequenced viruses

Bunyaviruses ( Negarnaviricota : Bunyavirales ) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid characterization of known and new emerging pathogens depends on the availability of comprehensive reference sequence databases that can be...

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Vydané v:PLoS pathogens Ročník 17; číslo 3; s. e1009315
Hlavní autori: Kapuscinski, Marylee L., Bergren, Nicholas A., Russell, Brandy J., Lee, Justin S., Borland, Erin M., Hartman, Daniel A., King, David C., Hughes, Holly R., Burkhalter, Kristen L., Kading, Rebekah C., Stenglein, Mark D.
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Public Library of Science 01.03.2021
Public Library of Science (PLoS)
Predmet:
Animals
Arboviruses - genetics
Arthropods - genetics
Base Sequence
Biology and life sciences
Bunyaviruses
Coccidioidomycosis
Computer and Information Sciences
Disease
Disease control
Fever
Genetic aspects
Genome, Viral - genetics
Genomes
Genomics
Glycoproteins
Humans
Identification and classification
Infectious diseases
Medicine and Health Sciences
Nairovirus - genetics
Nucleic acids
Nucleotide sequence
Orthobunyavirus - genetics
Pathogens
Phenuiviridae
Phylogenetics
Phylogeny
Polymerase chain reaction
Proteins
Public domain
Public health
Research and Analysis Methods
Rift Valley fever
RNA polymerase
RNA Viruses - genetics
Thrombocytopenia
Vector-borne diseases
Vectors (Biology)
Viral diseases
Viruses
United States
United States > US
ISSN:1553-7374, 1553-7366, 1553-7374
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Abstract Bunyaviruses ( Negarnaviricota : Bunyavirales ) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid characterization of known and new emerging pathogens depends on the availability of comprehensive reference sequence databases that can be used to match unknowns, infer evolutionary relationships and pathogenic potential, and make response decisions in an evidence-based manner. In this study, we determined the coding-complete genome sequences of 99 bunyaviruses in the Centers for Disease Control and Prevention’s Arbovirus Reference Collection, focusing on orthonairoviruses (family Nairoviridae ), orthobunyaviruses ( Peribunyaviridae ), and phleboviruses ( Phenuiviridae ) that either completely or partially lacked genome sequences. These viruses had been collected over 66 years from 27 countries from vertebrates and arthropods representing 37 genera. Many of the viruses had been characterized serologically and through experimental infection of animals but were isolated in the pre-sequencing era. We took advantage of our unusually large sample size to systematically evaluate genomic characteristics of these viruses, including reassortment, and co-infection. We corroborated our findings using several independent molecular and virologic approaches, including Sanger sequencing of 197 genome segments, and plaque isolation of viruses from putative co-infected virus stocks. This study contributes to the described genetic diversity of bunyaviruses and will enhance the capacity to characterize emerging human pathogenic bunyaviruses.
AbstractList Bunyaviruses (Negarnaviricota: Bunyavirales) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid characterization of known and new emerging pathogens depends on the availability of comprehensive reference sequence databases that can be used to match unknowns, infer evolutionary relationships and pathogenic potential, and make response decisions in an evidence-based manner. In this study, we determined the coding-complete genome sequences of 99 bunyaviruses in the Centers for Disease Control and Prevention’s Arbovirus Reference Collection, focusing on orthonairoviruses (family Nairoviridae), orthobunyaviruses (Peribunyaviridae), and phleboviruses (Phenuiviridae) that either completely or partially lacked genome sequences. These viruses had been collected over 66 years from 27 countries from vertebrates and arthropods representing 37 genera. Many of the viruses had been characterized serologically and through experimental infection of animals but were isolated in the pre-sequencing era. We took advantage of our unusually large sample size to systematically evaluate genomic characteristics of these viruses, including reassortment, and co-infection. We corroborated our findings using several independent molecular and virologic approaches, including Sanger sequencing of 197 genome segments, and plaque isolation of viruses from putative co-infected virus stocks. This study contributes to the described genetic diversity of bunyaviruses and will enhance the capacity to characterize emerging human pathogenic bunyaviruses. Prior knowledge about families of pathogens can enhance efforts to prepare for and respond to emerging disease threats. The CDC’s Arbovirus Reference Collection (ARC) comprises a world reference repository of arthropod-borne viruses that are either pathogenic or are related to known pathogens. Many viruses in this collection were isolated before genome sequencing was readily available, resulting in an incomplete understanding of their potential relevance to human or animal health. In this study, we sequenced the genomes of 99 bunyaviruses in the ARC. We performed detailed phylogenetic analyses, described multiple well-supported instances of genome segment reassortment, and identified co-infection in several virus stocks. These sequences enhance the public database of known bunyaviruses which can be interrogated to identify emerging viruses during an outbreak, and contribute to a better understanding of bunyavirus evolution and pathogenic potential.
Bunyaviruses (Negarnaviricota: Bunyavirales) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid characterization of known and new emerging pathogens depends on the availability of comprehensive reference sequence databases that can be used to match unknowns, infer evolutionary relationships and pathogenic potential, and make response decisions in an evidence-based manner. In this study, we determined the coding-complete genome sequences of 99 bunyaviruses in the Centers for Disease Control and Prevention's Arbovirus Reference Collection, focusing on orthonairoviruses (family Nairoviridae), orthobunyaviruses (Peribunyaviridae), and phleboviruses (Phenuiviridae) that either completely or partially lacked genome sequences. These viruses had been collected over 66 years from 27 countries from vertebrates and arthropods representing 37 genera. Many of the viruses had been characterized serologically and through experimental infection of animals but were isolated in the pre-sequencing era. We took advantage of our unusually large sample size to systematically evaluate genomic characteristics of these viruses, including reassortment, and co-infection. We corroborated our findings using several independent molecular and virologic approaches, including Sanger sequencing of 197 genome segments, and plaque isolation of viruses from putative co-infected virus stocks. This study contributes to the described genetic diversity of bunyaviruses and will enhance the capacity to characterize emerging human pathogenic bunyaviruses.
Iquitos and Itaya viruses are emerging reassortant viruses (Peribunyaviridae: Orthobunyavirus) that have both been associated with human illness in Peru [9,13]; an intra-lineage reassortant strain of Rift Valley fever virus (Phenuiviridae: Phlebovirus) was recently isolated from an ill traveler returning home to China [20]; and severe fever with thrombocytopenia syndrome virus (SFTSV) is a newly-recognized, tick-borne phenuivirus that causes severe human disease and for which reassortment has been recognized in strains detected in human patients [21]. The US Center for Disease Control and Prevention’s (CDC) Division of Vector-borne Diseases (DVBD), Arboviral Diseases Branch (ADB), maintains an Arbovirus Reference Collection (ARC). Genetic characterization of the viruses in the ARC would expand the value and impact of this collection even further as a scientific and public health resource and infuse a significant amount of novel and important molecular data into the public domain for actionable use. [...]the objective of this project was to generate additional and novel genome sequence and phylogenetic data for a large group of bunyaviruses lacking genetic characterization to facilitate the rapid identification and characterization of emerging bunyaviruses. Nucleic acids were eluted in 100 μl AVE elution buffer supplied with the extraction kit, and stored at -20°C. Amplification of viral RNA was performed in both forward and reverse directions using the Qiagen OneStep RT-PCR kit (Qiagen, Valencia, CA, USA) according to manufacturer’s instructions and using the appropriate primer pair listed in S1 Table.
Bunyaviruses ( Negarnaviricota : Bunyavirales ) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid characterization of known and new emerging pathogens depends on the availability of comprehensive reference sequence databases that can be used to match unknowns, infer evolutionary relationships and pathogenic potential, and make response decisions in an evidence-based manner. In this study, we determined the coding-complete genome sequences of 99 bunyaviruses in the Centers for Disease Control and Prevention’s Arbovirus Reference Collection, focusing on orthonairoviruses (family Nairoviridae ), orthobunyaviruses ( Peribunyaviridae ), and phleboviruses ( Phenuiviridae ) that either completely or partially lacked genome sequences. These viruses had been collected over 66 years from 27 countries from vertebrates and arthropods representing 37 genera. Many of the viruses had been characterized serologically and through experimental infection of animals but were isolated in the pre-sequencing era. We took advantage of our unusually large sample size to systematically evaluate genomic characteristics of these viruses, including reassortment, and co-infection. We corroborated our findings using several independent molecular and virologic approaches, including Sanger sequencing of 197 genome segments, and plaque isolation of viruses from putative co-infected virus stocks. This study contributes to the described genetic diversity of bunyaviruses and will enhance the capacity to characterize emerging human pathogenic bunyaviruses.
Bunyaviruses (Negarnaviricota: Bunyavirales) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid characterization of known and new emerging pathogens depends on the availability of comprehensive reference sequence databases that can be used to match unknowns, infer evolutionary relationships and pathogenic potential, and make response decisions in an evidence-based manner. In this study, we determined the coding-complete genome sequences of 99 bunyaviruses in the Centers for Disease Control and Prevention's Arbovirus Reference Collection, focusing on orthonairoviruses (family Nairoviridae), orthobunyaviruses (Peribunyaviridae), and phleboviruses (Phenuiviridae) that either completely or partially lacked genome sequences. These viruses had been collected over 66 years from 27 countries from vertebrates and arthropods representing 37 genera. Many of the viruses had been characterized serologically and through experimental infection of animals but were isolated in the pre-sequencing era. We took advantage of our unusually large sample size to systematically evaluate genomic characteristics of these viruses, including reassortment, and co-infection. We corroborated our findings using several independent molecular and virologic approaches, including Sanger sequencing of 197 genome segments, and plaque isolation of viruses from putative co-infected virus stocks. This study contributes to the described genetic diversity of bunyaviruses and will enhance the capacity to characterize emerging human pathogenic bunyaviruses.Bunyaviruses (Negarnaviricota: Bunyavirales) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid characterization of known and new emerging pathogens depends on the availability of comprehensive reference sequence databases that can be used to match unknowns, infer evolutionary relationships and pathogenic potential, and make response decisions in an evidence-based manner. In this study, we determined the coding-complete genome sequences of 99 bunyaviruses in the Centers for Disease Control and Prevention's Arbovirus Reference Collection, focusing on orthonairoviruses (family Nairoviridae), orthobunyaviruses (Peribunyaviridae), and phleboviruses (Phenuiviridae) that either completely or partially lacked genome sequences. These viruses had been collected over 66 years from 27 countries from vertebrates and arthropods representing 37 genera. Many of the viruses had been characterized serologically and through experimental infection of animals but were isolated in the pre-sequencing era. We took advantage of our unusually large sample size to systematically evaluate genomic characteristics of these viruses, including reassortment, and co-infection. We corroborated our findings using several independent molecular and virologic approaches, including Sanger sequencing of 197 genome segments, and plaque isolation of viruses from putative co-infected virus stocks. This study contributes to the described genetic diversity of bunyaviruses and will enhance the capacity to characterize emerging human pathogenic bunyaviruses.
Iquitos and Itaya viruses are emerging reassortant viruses (Peribunyaviridae: Orthobunyavirus) that have both been associated with human illness in Peru [9,13]; an intra-lineage reassortant strain of Rift Valley fever virus (Phenuiviridae: Phlebovirus) was recently isolated from an ill traveler returning home to China [20]; and severe fever with thrombocytopenia syndrome virus (SFTSV) is a newly-recognized, tick-borne phenuivirus that causes severe human disease and for which reassortment has been recognized in strains detected in human patients [21]. The US Center for Disease Control and Prevention’s (CDC) Division of Vector-borne Diseases (DVBD), Arboviral Diseases Branch (ADB), maintains an Arbovirus Reference Collection (ARC). Genetic characterization of the viruses in the ARC would expand the value and impact of this collection even further as a scientific and public health resource and infuse a significant amount of novel and important molecular data into the public domain for actionable use. [...]the objective of this project was to generate additional and novel genome sequence and phylogenetic data for a large group of bunyaviruses lacking genetic characterization to facilitate the rapid identification and characterization of emerging bunyaviruses. Nucleic acids were eluted in 100 μl AVE elution buffer supplied with the extraction kit, and stored at -20°C. Amplification of viral RNA was performed in both forward and reverse directions using the Qiagen OneStep RT-PCR kit (Qiagen, Valencia, CA, USA) according to manufacturer’s instructions and using the appropriate primer pair listed in S1 Table.
Audience Academic
Author Bergren, Nicholas A.
Russell, Brandy J.
Kading, Rebekah C.
Burkhalter, Kristen L.
King, David C.
Stenglein, Mark D.
Hughes, Holly R.
Kapuscinski, Marylee L.
Lee, Justin S.
Borland, Erin M.
Hartman, Daniel A.
AuthorAffiliation Division of Clinical Research, UNITED STATES
1 Department of Microbiology, Immunology, and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado, United States of America
2 Arboviral Diseases Branch, Division of Vector Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado, United States of America
AuthorAffiliation_xml – name: 1 Department of Microbiology, Immunology, and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado, United States of America
– name: 2 Arboviral Diseases Branch, Division of Vector Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado, United States of America
– name: Division of Clinical Research, UNITED STATES
Author_xml – sequence: 1
  givenname: Marylee L.
  orcidid: 0000-0002-8616-4115
  surname: Kapuscinski
  fullname: Kapuscinski, Marylee L.
– sequence: 2
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  orcidid: 0000-0003-4496-447X
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  fullname: Bergren, Nicholas A.
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  fullname: Burkhalter, Kristen L.
– sequence: 10
  givenname: Rebekah C.
  orcidid: 0000-0002-4996-915X
  surname: Kading
  fullname: Kading, Rebekah C.
– sequence: 11
  givenname: Mark D.
  orcidid: 0000-0002-0993-813X
  surname: Stenglein
  fullname: Stenglein, Mark D.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33647063$$D View this record in MEDLINE/PubMed
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Snippet Bunyaviruses ( Negarnaviricota : Bunyavirales ) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The...
Bunyaviruses (Negarnaviricota: Bunyavirales) are a large and diverse group of viruses that include important human, veterinary, and plant pathogens. The rapid...
Iquitos and Itaya viruses are emerging reassortant viruses (Peribunyaviridae: Orthobunyavirus) that have both been associated with human illness in Peru...
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StartPage e1009315
SubjectTerms Animals
Arboviruses - genetics
Arthropods - genetics
Base Sequence
Biology and life sciences
Bunyaviruses
Coccidioidomycosis
Computer and Information Sciences
Disease
Disease control
Fever
Genetic aspects
Genome, Viral - genetics
Genomes
Genomics
Glycoproteins
Humans
Identification and classification
Infectious diseases
Medicine and Health Sciences
Nairovirus - genetics
Nucleic acids
Nucleotide sequence
Orthobunyavirus - genetics
Pathogens
Phenuiviridae
Phylogenetics
Phylogeny
Polymerase chain reaction
Proteins
Public domain
Public health
Research and Analysis Methods
Rift Valley fever
RNA polymerase
RNA Viruses - genetics
Thrombocytopenia
Vector-borne diseases
Vectors (Biology)
Viral diseases
Viruses
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Title Genomic characterization of 99 viruses from the bunyavirus families Nairoviridae, Peribunyaviridae, and Phenuiviridae, including 35 previously unsequenced viruses
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http://dx.doi.org/10.1371/journal.ppat.1009315
Volume 17
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