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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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Genome structures of segmented negative-sense RNA viruses.Predicted viral proteins homologous to known viral proteins are shown andcolored according to their putative functions. The numbers below each ORFbox give the predicted molecular mass.DOI:http://dx.doi.org/10.7554/eLife.05378.017
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fig8: Genome structures of segmented negative-sense RNA viruses.Predicted viral proteins homologous to known viral proteins are shown andcolored according to their putative functions. The numbers below each ORFbox give the predicted molecular mass.DOI:http://dx.doi.org/10.7554/eLife.05378.017

Mentions: Although our phylogenetic analysis focused on the relatively conserved RdRp, in thecase of segmented viruses we searched for other putative viral proteins from theassembled contigs. Accordingly, we were able to find the segments encoding matchingstructural proteins (mainly glycoproteins and nucleoproteins) for many of the viralRdRp sequences (Figure 8), although extensivesequence divergence prevented this in some cases. Surprisingly, M segments wereapparently absent in a group of tick phleboviruses whose RdRps and nucleoproteinsshowed relatively high sequence similarity to Uukuniemi virus (genusPhlebovirus; Table 3 andFigure 8). Genomes with missingglycoprotein genes were also found in the chuviruses (Changping Tick Viruses 3 and 5,Wuhan Louse Viruses 6 and 7, Figure 7) and theunsegmented dimarhabdovirus (Taishun Tick Virus, Wuhan Tick Virus 1, Tacheng TickVirus 6, Figure 9). Although it is possiblethat the glycoprotein gene may have been replaced with a highly divergent or evennon-homologous sequence, we failed to find any candidate G proteins within theno-Blastx-hit set of sequences under the following criteria: (i) structuralresemblance to G proteins, (ii) similar level of abundance to the corresponding RdRpand nucleoprotein genes, and (iii) comparable phylogenies or levels of divergence(among related viruses) to those of RdRps and nucleoproteins. The cause andbiological significance of these seemingly ‘incomplete’ virus genomesrequire further study. Finally, it was also of interest that a virus with foursegments was discovered in the horsefly pool. Although the predicted proteins of allfour segments showed sequence homology to their counterparts in Tenuivirus (Falk and Tsai, 1998), this virus lacked theambisense coding strategy of tenuiviruses (Figure10). While the capability of this virus to infect plants is unknown, it ispossible that it represents a transitional form between plant-infecting andarthropod-specific viruses.10.7554/eLife.05378.017Figure 8.Genome structures of segmented negative-sense RNA viruses.


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)

Genome structures of segmented negative-sense RNA viruses.Predicted viral proteins homologous to known viral proteins are shown andcolored according to their putative functions. The numbers below each ORFbox give the predicted molecular mass.DOI:http://dx.doi.org/10.7554/eLife.05378.017
© Copyright Policy
Related In: Results  -  Collection

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

fig8: Genome structures of segmented negative-sense RNA viruses.Predicted viral proteins homologous to known viral proteins are shown andcolored according to their putative functions. The numbers below each ORFbox give the predicted molecular mass.DOI:http://dx.doi.org/10.7554/eLife.05378.017
Mentions: Although our phylogenetic analysis focused on the relatively conserved RdRp, in thecase of segmented viruses we searched for other putative viral proteins from theassembled contigs. Accordingly, we were able to find the segments encoding matchingstructural proteins (mainly glycoproteins and nucleoproteins) for many of the viralRdRp sequences (Figure 8), although extensivesequence divergence prevented this in some cases. Surprisingly, M segments wereapparently absent in a group of tick phleboviruses whose RdRps and nucleoproteinsshowed relatively high sequence similarity to Uukuniemi virus (genusPhlebovirus; Table 3 andFigure 8). Genomes with missingglycoprotein genes were also found in the chuviruses (Changping Tick Viruses 3 and 5,Wuhan Louse Viruses 6 and 7, Figure 7) and theunsegmented dimarhabdovirus (Taishun Tick Virus, Wuhan Tick Virus 1, Tacheng TickVirus 6, Figure 9). Although it is possiblethat the glycoprotein gene may have been replaced with a highly divergent or evennon-homologous sequence, we failed to find any candidate G proteins within theno-Blastx-hit set of sequences under the following criteria: (i) structuralresemblance to G proteins, (ii) similar level of abundance to the corresponding RdRpand nucleoprotein genes, and (iii) comparable phylogenies or levels of divergence(among related viruses) to those of RdRps and nucleoproteins. The cause andbiological significance of these seemingly ‘incomplete’ virus genomesrequire further study. Finally, it was also of interest that a virus with foursegments was discovered in the horsefly pool. Although the predicted proteins of allfour segments showed sequence homology to their counterparts in Tenuivirus (Falk and Tsai, 1998), this virus lacked theambisense coding strategy of tenuiviruses (Figure10). While the capability of this virus to infect plants is unknown, it ispossible that it represents a transitional form between plant-infecting andarthropod-specific viruses.10.7554/eLife.05378.017Figure 8.Genome structures of segmented negative-sense RNA viruses.

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