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Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses.

Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ - Elife (2015)

Bottom Line: Although arthropods are important viral vectors, the biodiversity of arthropod viruses, as well as the role that arthropods have played in viral origins and evolution, is unclear.We similarly documented a remarkable diversity of genome structures in arthropod viruses, including a putative circular form, that sheds new light on the evolution of genome organization.Hence, arthropods are a major reservoir of viral genetic diversity and have likely been central to viral evolution.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China.

ABSTRACT
Although arthropods are important viral vectors, the biodiversity of arthropod viruses, as well as the role that arthropods have played in viral origins and evolution, is unclear. Through RNA sequencing of 70 arthropod species we discovered 112 novel viruses that appear to be ancestral to much of the documented genetic diversity of negative-sense RNA viruses, a number of which are also present as endogenous genomic copies. With this greatly enriched diversity we revealed that arthropods contain viruses that fall basal to major virus groups, including the vertebrate-specific arenaviruses, filoviruses, hantaviruses, influenza viruses, lyssaviruses, and paramyxoviruses. We similarly documented a remarkable diversity of genome structures in arthropod viruses, including a putative circular form, that sheds new light on the evolution of genome organization. Hence, arthropods are a major reservoir of viral genetic diversity and have likely been central to viral evolution.

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Related in: MedlinePlus

Host component of each pool used in the RNA-seq library construction andsequencing.The taxonomic units in the tree correspond to the unit samples used in theRNA extraction. Species or genus information is marked to the left of thetree.DOI:http://dx.doi.org/10.7554/eLife.05378.004
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fig1: Host component of each pool used in the RNA-seq library construction andsequencing.The taxonomic units in the tree correspond to the unit samples used in theRNA extraction. Species or genus information is marked to the left of thetree.DOI:http://dx.doi.org/10.7554/eLife.05378.004

Mentions: We focused our study of virus biodiversity and evolution on 70 potential host speciesfrom four arthropod classes: Insecta, Arachnida, Chilopoda, and Malacostraca (Table 1 and Figure 1). From these samples, 16 separate cDNA libraries were constructedand sequenced, resulting in a total of 147.4 Gb of 100-base pair-end reads (Table 1). Blastx comparisons against proteinsequences of negative-sense RNA virus revealed 108 distinct types of complete ornearly complete large (L) proteins (or polymerase protein 1 (PB1) in the case oforthomyxoviruses) that encode the relatively conserved RdRp (Tables 2–4). Four additional types ofpreviously undescribed RdRp sequence (>1000 amino acids) were identified fromthe Transcriptome Shotgun Assembly (TSA) database. Together, these proteins exhibitedan enormous diversity in terms of sequence variation and structure. Most notably,this data set of RdRp sequences is distinct from both previously described sequencesand from each other, with the most divergent showing as little as 15.8% amino acidsequence identity to its closest relatives (Tables 2–4). Overall, these data provideevidence for at least 16 potentially new families and genera of negative-sense RNAviruses, defined as whose RdRp sequences shared less than 25% amino acid identitywith existing taxa.10.7554/eLife.05378.003Table 1.


Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses.

Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ - Elife (2015)

Host component of each pool used in the RNA-seq library construction andsequencing.The taxonomic units in the tree correspond to the unit samples used in theRNA extraction. Species or genus information is marked to the left of thetree.DOI:http://dx.doi.org/10.7554/eLife.05378.004
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4384744&req=5

fig1: Host component of each pool used in the RNA-seq library construction andsequencing.The taxonomic units in the tree correspond to the unit samples used in theRNA extraction. Species or genus information is marked to the left of thetree.DOI:http://dx.doi.org/10.7554/eLife.05378.004
Mentions: We focused our study of virus biodiversity and evolution on 70 potential host speciesfrom four arthropod classes: Insecta, Arachnida, Chilopoda, and Malacostraca (Table 1 and Figure 1). From these samples, 16 separate cDNA libraries were constructedand sequenced, resulting in a total of 147.4 Gb of 100-base pair-end reads (Table 1). Blastx comparisons against proteinsequences of negative-sense RNA virus revealed 108 distinct types of complete ornearly complete large (L) proteins (or polymerase protein 1 (PB1) in the case oforthomyxoviruses) that encode the relatively conserved RdRp (Tables 2–4). Four additional types ofpreviously undescribed RdRp sequence (>1000 amino acids) were identified fromthe Transcriptome Shotgun Assembly (TSA) database. Together, these proteins exhibitedan enormous diversity in terms of sequence variation and structure. Most notably,this data set of RdRp sequences is distinct from both previously described sequencesand from each other, with the most divergent showing as little as 15.8% amino acidsequence identity to its closest relatives (Tables 2–4). Overall, these data provideevidence for at least 16 potentially new families and genera of negative-sense RNAviruses, defined as whose RdRp sequences shared less than 25% amino acid identitywith existing taxa.10.7554/eLife.05378.003Table 1.

Bottom Line: Although arthropods are important viral vectors, the biodiversity of arthropod viruses, as well as the role that arthropods have played in viral origins and evolution, is unclear.We similarly documented a remarkable diversity of genome structures in arthropod viruses, including a putative circular form, that sheds new light on the evolution of genome organization.Hence, arthropods are a major reservoir of viral genetic diversity and have likely been central to viral evolution.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China.

ABSTRACT
Although arthropods are important viral vectors, the biodiversity of arthropod viruses, as well as the role that arthropods have played in viral origins and evolution, is unclear. Through RNA sequencing of 70 arthropod species we discovered 112 novel viruses that appear to be ancestral to much of the documented genetic diversity of negative-sense RNA viruses, a number of which are also present as endogenous genomic copies. With this greatly enriched diversity we revealed that arthropods contain viruses that fall basal to major virus groups, including the vertebrate-specific arenaviruses, filoviruses, hantaviruses, influenza viruses, lyssaviruses, and paramyxoviruses. We similarly documented a remarkable diversity of genome structures in arthropod viruses, including a putative circular form, that sheds new light on the evolution of genome organization. Hence, arthropods are a major reservoir of viral genetic diversity and have likely been central to viral evolution.

Show MeSH
Related in: MedlinePlus