Viromics of extant insect orders unveil the evolution of the flavi-like superfamily

Abstract Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such as the genus Flavivirus, are associated with insects; however, systematic studies on insect virus genetic diversity are lacking, li...

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Veröffentlicht in:Virus evolution Jg. 7; H. 1; S. veab030
Hauptverfasser: Paraskevopoulou, Sofia, Käfer, Simon, Zirkel, Florian, Donath, Alexander, Petersen, Malte, Liu, Shanlin, Zhou, Xin, Drosten, Christian, Misof, Bernhard, Junglen, Sandra
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Sprache:Englisch
Veröffentlicht: Oxford Oxford University Press 01.01.2021
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ISSN:2057-1577, 2057-1577
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Abstract Abstract Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such as the genus Flavivirus, are associated with insects; however, systematic studies on insect virus genetic diversity are lacking, limiting our understanding of the evolution of the flavi-like superfamily. Here, we examined the diversity of flavi-like viruses within the most complete and up-to-date insect transcriptome collection comprising 1,243 insect species by employing a Flaviviridae RdRp profile hidden Markov model search. We identified seventy-six viral sequences in sixty-one species belonging to seventeen insect, one entognathan, and one arachnidan orders. Phylogenetic analyses revealed that twenty-seven sequences fell within the Flaviviridae phylogeny but did not group with established genera. Despite the large diversity of insect hosts studied, we only detected one virus in a blood-feeding insect, which branched within the genus Flavivirus, indicating that this genus likely diversified only in hematophagous arthropods. Nine new jingmenviruses with novel host associations were identified. One of the jingmenviruses established a deep rooting lineage additional to the insect- and tick-associated clades. Segment co-segregation phylogenies support the separation of tick- and insect-associated groups within jingmenviruses, with evidence for segment reassortment. In addition, fourteen viruses grouped with unclassified flaviviruses encompassing genome length of up to 20 kb. Species-specific clades for Hymenopteran- and Orthopteran-associated viruses were identified. Forty-nine viruses populated three highly diversified clades in distant relationship to Tombusviridae, a plant-infecting virus family, suggesting the detection of three previously unknown insect-associated families that contributed to tombusvirus evolution.
AbstractList Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such as the genus Flavivirus, are associated with insects; however, systematic studies on insect virus genetic diversity are lacking, limiting our understanding of the evolution of the flavi-like superfamily. Here, we examined the diversity of flavi-like viruses within the most complete and up-to-date insect transcriptome collection comprising 1,243 insect species by employing a Flaviviridae RdRp profile hidden Markov model search. We identified seventy-six viral sequences in sixty-one species belonging to seventeen insect, one entognathan, and one arachnidan orders. Phylogenetic analyses revealed that twenty-seven sequences fell within the Flaviviridae phylogeny but did not group with established genera. Despite the large diversity of insect hosts studied, we only detected one virus in a blood-feeding insect, which branched within the genus Flavivirus, indicating that this genus likely diversified only in hematophagous arthropods. Nine new jingmenviruses with novel host associations were identified. One of the jingmenviruses established a deep rooting lineage additional to the insect- and tick-associated clades. Segment co-segregation phylogenies support the separation of tick- and insect-associated groups within jingmenviruses, with evidence for segment reassortment. In addition, fourteen viruses grouped with unclassified flaviviruses encompassing genome length of up to 20 kb. Species-specific clades for Hymenopteran- and Orthopteran-associated viruses were identified. Forty-nine viruses populated three highly diversified clades in distant relationship to Tombusviridae, a plant-infecting virus family, suggesting the detection of three previously unknown insect-associated families that contributed to tombusvirus evolution.
Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such as the genus Flavivirus, are associated with insects; however, systematic studies on insect virus genetic diversity are lacking, limiting our understanding of the evolution of the flavi-like superfamily. Here, we examined the diversity of flavi-like viruses within the most complete and up-to-date insect transcriptome collection comprising 1,243 insect species by employing a Flaviviridae RdRp profile hidden Markov model search. We identified seventy-six viral sequences in sixty-one species belonging to seventeen insect, one entognathan, and one arachnidan orders. Phylogenetic analyses revealed that twenty-seven sequences fell within the Flaviviridae phylogeny but did not group with established genera. Despite the large diversity of insect hosts studied, we only detected one virus in a blood-feeding insect, which branched within the genus Flavivirus, indicating that this genus likely diversified only in hematophagous arthropods. Nine new jingmenviruses with novel host associations were identified. One of the jingmenviruses established a deep rooting lineage additional to the insect- and tick-associated clades. Segment co-segregation phylogenies support the separation of tick- and insect-associated groups within jingmenviruses, with evidence for segment reassortment. In addition, fourteen viruses grouped with unclassified flaviviruses encompassing genome length of up to 20 kb. Species-specific clades for Hymenopteran- and Orthopteran-associated viruses were identified. Forty-nine viruses populated three highly diversified clades in distant relationship to Tombusviridae, a plant-infecting virus family, suggesting the detection of three previously unknown insect-associated families that contributed to tombusvirus evolution.Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such as the genus Flavivirus, are associated with insects; however, systematic studies on insect virus genetic diversity are lacking, limiting our understanding of the evolution of the flavi-like superfamily. Here, we examined the diversity of flavi-like viruses within the most complete and up-to-date insect transcriptome collection comprising 1,243 insect species by employing a Flaviviridae RdRp profile hidden Markov model search. We identified seventy-six viral sequences in sixty-one species belonging to seventeen insect, one entognathan, and one arachnidan orders. Phylogenetic analyses revealed that twenty-seven sequences fell within the Flaviviridae phylogeny but did not group with established genera. Despite the large diversity of insect hosts studied, we only detected one virus in a blood-feeding insect, which branched within the genus Flavivirus, indicating that this genus likely diversified only in hematophagous arthropods. Nine new jingmenviruses with novel host associations were identified. One of the jingmenviruses established a deep rooting lineage additional to the insect- and tick-associated clades. Segment co-segregation phylogenies support the separation of tick- and insect-associated groups within jingmenviruses, with evidence for segment reassortment. In addition, fourteen viruses grouped with unclassified flaviviruses encompassing genome length of up to 20 kb. Species-specific clades for Hymenopteran- and Orthopteran-associated viruses were identified. Forty-nine viruses populated three highly diversified clades in distant relationship to Tombusviridae, a plant-infecting virus family, suggesting the detection of three previously unknown insect-associated families that contributed to tombusvirus evolution.
Abstract Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such as the genus Flavivirus, are associated with insects; however, systematic studies on insect virus genetic diversity are lacking, limiting our understanding of the evolution of the flavi-like superfamily. Here, we examined the diversity of flavi-like viruses within the most complete and up-to-date insect transcriptome collection comprising 1,243 insect species by employing a Flaviviridae RdRp profile hidden Markov model search. We identified seventy-six viral sequences in sixty-one species belonging to seventeen insect, one entognathan, and one arachnidan orders. Phylogenetic analyses revealed that twenty-seven sequences fell within the Flaviviridae phylogeny but did not group with established genera. Despite the large diversity of insect hosts studied, we only detected one virus in a blood-feeding insect, which branched within the genus Flavivirus, indicating that this genus likely diversified only in hematophagous arthropods. Nine new jingmenviruses with novel host associations were identified. One of the jingmenviruses established a deep rooting lineage additional to the insect- and tick-associated clades. Segment co-segregation phylogenies support the separation of tick- and insect-associated groups within jingmenviruses, with evidence for segment reassortment. In addition, fourteen viruses grouped with unclassified flaviviruses encompassing genome length of up to 20 kb. Species-specific clades for Hymenopteran- and Orthopteran-associated viruses were identified. Forty-nine viruses populated three highly diversified clades in distant relationship to Tombusviridae, a plant-infecting virus family, suggesting the detection of three previously unknown insect-associated families that contributed to tombusvirus evolution.
Author Petersen, Malte
Drosten, Christian
Liu, Shanlin
Paraskevopoulou, Sofia
Donath, Alexander
Zhou, Xin
Käfer, Simon
Misof, Bernhard
Junglen, Sandra
Zirkel, Florian
AuthorAffiliation 2 Institute of Virology, University of Bonn Medical Center , Venusberg-Campus 1, 53127 Bonn, Germany
4 Department of Entomology, China Agricultural University , 17 Qinghua E Rd, Haidian District, Beijing, China
5 German Center for Infection Research (DZIF), partner site Charité , Chariteplatz 1, 10117 Berlin, Germany
1 Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health , Chariteplatz 1, 10117 Berlin, Germany
3 Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig , Adenauerallee 160, 53113 Bonn, Germany
AuthorAffiliation_xml – name: 2 Institute of Virology, University of Bonn Medical Center , Venusberg-Campus 1, 53127 Bonn, Germany
– name: 3 Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig , Adenauerallee 160, 53113 Bonn, Germany
– name: 5 German Center for Infection Research (DZIF), partner site Charité , Chariteplatz 1, 10117 Berlin, Germany
– name: 4 Department of Entomology, China Agricultural University , 17 Qinghua E Rd, Haidian District, Beijing, China
– name: 1 Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health , Chariteplatz 1, 10117 Berlin, Germany
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  givenname: Sofia
  surname: Paraskevopoulou
  fullname: Paraskevopoulou, Sofia
  organization: Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Chariteplatz 1, 10117 Berlin, Germany
– sequence: 2
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  surname: Käfer
  fullname: Käfer, Simon
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  organization: Institute of Virology, University of Bonn Medical Center, Venusberg-Campus 1, 53127 Bonn, Germany
– sequence: 4
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  surname: Donath
  fullname: Donath, Alexander
  organization: Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany
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  surname: Petersen
  fullname: Petersen, Malte
  organization: Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany
– sequence: 6
  givenname: Shanlin
  surname: Liu
  fullname: Liu, Shanlin
  organization: Department of Entomology, China Agricultural University, 17 Qinghua E Rd, Haidian District, Beijing, China
– sequence: 7
  givenname: Xin
  surname: Zhou
  fullname: Zhou, Xin
  organization: Department of Entomology, China Agricultural University, 17 Qinghua E Rd, Haidian District, Beijing, China
– sequence: 8
  givenname: Christian
  surname: Drosten
  fullname: Drosten, Christian
  organization: Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Chariteplatz 1, 10117 Berlin, Germany
– sequence: 9
  givenname: Bernhard
  surname: Misof
  fullname: Misof, Bernhard
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  organization: Centre for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany
– sequence: 10
  givenname: Sandra
  surname: Junglen
  fullname: Junglen, Sandra
  email: sandra.junglen@charite.de
  organization: Institute of Virology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Chariteplatz 1, 10117 Berlin, Germany
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Keywords phylogeny
tombusvirus
flavi-like virus
insect virus
positive-sense RNA
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  doi: 10.1038/nbt.4306
– volume: 9
  start-page: 154
  year: 2017
  ident: 2021070821242146400_veab030-B3
  article-title: A Review of Flaviviruses That Have No Known Arthropod Vector
  publication-title: Viruses
  doi: 10.3390/v9060154
– volume: 15
  start-page: e1008224
  year: 2019
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  article-title: Re-Assessing the Diversity of Negative Strand RNA Viruses in Insects
  publication-title: PLoS Pathogens
  doi: 10.1371/journal.ppat.1008224
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Snippet Abstract Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like...
Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such...
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SubjectTerms Viruses
Title Viromics of extant insect orders unveil the evolution of the flavi-like superfamily
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https://pubmed.ncbi.nlm.nih.gov/PMC8129625
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