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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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The unrooted ML phylogeny based on RdRp showing the topological positionof segmented viruses within the genetic diversity of negative-sense RNAviruses.The segmented viruses are labeled with segment numbers and shaded red. Theunsegmented viruses are shaded green. The Chuviridae, which exhibit a widevariety of genome organizations, are shaded cyan. Three major types ofputative chuvirus genomes (circular, circular and segmented, and linear) areshown in the right panel and are annotated with predicted ORFs: putativeRdRp genes are shaded blue, putative glycoprotein genes are shaded orange,and the remaining ORFs are shaded gray.DOI:http://dx.doi.org/10.7554/eLife.05378.013
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fig4: The unrooted ML phylogeny based on RdRp showing the topological positionof segmented viruses within the genetic diversity of negative-sense RNAviruses.The segmented viruses are labeled with segment numbers and shaded red. Theunsegmented viruses are shaded green. The Chuviridae, which exhibit a widevariety of genome organizations, are shaded cyan. Three major types ofputative chuvirus genomes (circular, circular and segmented, and linear) areshown in the right panel and are annotated with predicted ORFs: putativeRdRp genes are shaded blue, putative glycoprotein genes are shaded orange,and the remaining ORFs are shaded gray.DOI:http://dx.doi.org/10.7554/eLife.05378.013

Mentions: With this highly diverse set of RdRp sequences in hand we re-examined the evolutionof all available negative-sense RNA viruses by phylogenetic analysis (Figure 3; Figure 3—figure supplement 3). These data greatly expand thedocumented diversity of four viral families/orders—theArenaviridae, Bunyaviridae,Orthomyxoviridae, and Mononegavirales—aswell as of three floating genera—Tenuivirus,Emaravirus, and Varicosavirus (King et al., 2012). Most of the newly describedarthropod viruses fell basal to the known genetic diversity in these taxa: theirdiversity either engulfed that of previously described viruses, as in the case ofphlebovirus, nairovirus, and dimarhabdovirus, or appeared as novel lineagessandwiched between existing genera or families, and hence filling in a number ofphylogenetic ‘gaps’ (Figure 3;Figure 3—figure supplement 3). Oneimportant example was a large monophyletic group of newly discovered viruses thatfell between the major groups of segmented and unsegmented viruses (Figure 4); we name this putative new virus familythe ‘Chuviridae’ reflecting the geographic location in China where mostof this family were identified (‘Chu’ is a historical term referring tolarge area of China encompassing the middle and lower reaches of the Yangzi River).Also of note was that some of the previously defined families no longer appear asmonophyletic. For example, although classified as distinct families, the familyArenaviridae fell within the genetic diversity of the familyBunyaviridae and as a sister group to viruses of the genusNairovirus. Furthermore, the floating genusTenuivirus was nested within the Phlebovirus-like clade, andanother floating genus, Emaravirus, formed a monophyletic group withthe Orthobunyavirus and Tospovirus genera (Figure 3C; Figure 3—figure supplement 2). Hence, there are importantinconsistencies between the current virus classification scheme and the underlyingevolutionary history of the RdRp revealed here.10.7554/eLife.05378.009Figure 3.Evolutionary history of negative-sense RNA viruses based onRdRp.


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)

The unrooted ML phylogeny based on RdRp showing the topological positionof segmented viruses within the genetic diversity of negative-sense RNAviruses.The segmented viruses are labeled with segment numbers and shaded red. Theunsegmented viruses are shaded green. The Chuviridae, which exhibit a widevariety of genome organizations, are shaded cyan. Three major types ofputative chuvirus genomes (circular, circular and segmented, and linear) areshown in the right panel and are annotated with predicted ORFs: putativeRdRp genes are shaded blue, putative glycoprotein genes are shaded orange,and the remaining ORFs are shaded gray.DOI:http://dx.doi.org/10.7554/eLife.05378.013
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Related In: Results  -  Collection

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fig4: The unrooted ML phylogeny based on RdRp showing the topological positionof segmented viruses within the genetic diversity of negative-sense RNAviruses.The segmented viruses are labeled with segment numbers and shaded red. Theunsegmented viruses are shaded green. The Chuviridae, which exhibit a widevariety of genome organizations, are shaded cyan. Three major types ofputative chuvirus genomes (circular, circular and segmented, and linear) areshown in the right panel and are annotated with predicted ORFs: putativeRdRp genes are shaded blue, putative glycoprotein genes are shaded orange,and the remaining ORFs are shaded gray.DOI:http://dx.doi.org/10.7554/eLife.05378.013
Mentions: With this highly diverse set of RdRp sequences in hand we re-examined the evolutionof all available negative-sense RNA viruses by phylogenetic analysis (Figure 3; Figure 3—figure supplement 3). These data greatly expand thedocumented diversity of four viral families/orders—theArenaviridae, Bunyaviridae,Orthomyxoviridae, and Mononegavirales—aswell as of three floating genera—Tenuivirus,Emaravirus, and Varicosavirus (King et al., 2012). Most of the newly describedarthropod viruses fell basal to the known genetic diversity in these taxa: theirdiversity either engulfed that of previously described viruses, as in the case ofphlebovirus, nairovirus, and dimarhabdovirus, or appeared as novel lineagessandwiched between existing genera or families, and hence filling in a number ofphylogenetic ‘gaps’ (Figure 3;Figure 3—figure supplement 3). Oneimportant example was a large monophyletic group of newly discovered viruses thatfell between the major groups of segmented and unsegmented viruses (Figure 4); we name this putative new virus familythe ‘Chuviridae’ reflecting the geographic location in China where mostof this family were identified (‘Chu’ is a historical term referring tolarge area of China encompassing the middle and lower reaches of the Yangzi River).Also of note was that some of the previously defined families no longer appear asmonophyletic. For example, although classified as distinct families, the familyArenaviridae fell within the genetic diversity of the familyBunyaviridae and as a sister group to viruses of the genusNairovirus. Furthermore, the floating genusTenuivirus was nested within the Phlebovirus-like clade, andanother floating genus, Emaravirus, formed a monophyletic group withthe Orthobunyavirus and Tospovirus genera (Figure 3C; Figure 3—figure supplement 2). Hence, there are importantinconsistencies between the current virus classification scheme and the underlyingevolutionary history of the RdRp revealed here.10.7554/eLife.05378.009Figure 3.Evolutionary history of negative-sense RNA viruses based onRdRp.

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