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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

Abundance level (transcripts per million—TPM) of the RdRp genesfrom the negative-sense RNA viruses detected in this study.Abundance is calculated after the removal of ribosomal RNA reads. As acomparison, we show the abundance of the two well characterized(positive-sense) RNA viruses: Japanese encephalitis virus andGill-associated virus found in the Mosquito-Hubei and Shrimp libraries,respectively, as well as the range of abundance of host mitochondrial COIgenes in these same multi-host libraries.DOI:http://dx.doi.org/10.7554/eLife.05378.008
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fig2: Abundance level (transcripts per million—TPM) of the RdRp genesfrom the negative-sense RNA viruses detected in this study.Abundance is calculated after the removal of ribosomal RNA reads. As acomparison, we show the abundance of the two well characterized(positive-sense) RNA viruses: Japanese encephalitis virus andGill-associated virus found in the Mosquito-Hubei and Shrimp libraries,respectively, as well as the range of abundance of host mitochondrial COIgenes in these same multi-host libraries.DOI:http://dx.doi.org/10.7554/eLife.05378.008

Mentions: Next, we measured the abundance of these sequences as the number transcripts permillion (TPM) within each library after the removal of rRNA reads. The abundance ofviral transcripts calculated in this manner exhibited substantial variation (Figure 2, Tables 2–4): while the least abundant L segment(Shayang Spider Virus 3) contributed to less than 0.001% to the total non-ribosomalRNA content, the most abundant (Sanxia Water Strider Virus 1) was at a frequency of21.2%, and up to 43.9% if we include the matching M and S segments of the virus. Theremaining viral RdRp sequences fell within a range (10–1000 TPM) that matchedthe abundance level of highly expressed host mitochondrial genes (Figure 2).10.7554/eLife.05378.008Figure 2.Abundance level (transcripts per million—TPM) of the RdRp genesfrom the negative-sense RNA viruses detected in this study.


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)

Abundance level (transcripts per million—TPM) of the RdRp genesfrom the negative-sense RNA viruses detected in this study.Abundance is calculated after the removal of ribosomal RNA reads. As acomparison, we show the abundance of the two well characterized(positive-sense) RNA viruses: Japanese encephalitis virus andGill-associated virus found in the Mosquito-Hubei and Shrimp libraries,respectively, as well as the range of abundance of host mitochondrial COIgenes in these same multi-host libraries.DOI:http://dx.doi.org/10.7554/eLife.05378.008
© Copyright Policy
Related In: Results  -  Collection

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

fig2: Abundance level (transcripts per million—TPM) of the RdRp genesfrom the negative-sense RNA viruses detected in this study.Abundance is calculated after the removal of ribosomal RNA reads. As acomparison, we show the abundance of the two well characterized(positive-sense) RNA viruses: Japanese encephalitis virus andGill-associated virus found in the Mosquito-Hubei and Shrimp libraries,respectively, as well as the range of abundance of host mitochondrial COIgenes in these same multi-host libraries.DOI:http://dx.doi.org/10.7554/eLife.05378.008
Mentions: Next, we measured the abundance of these sequences as the number transcripts permillion (TPM) within each library after the removal of rRNA reads. The abundance ofviral transcripts calculated in this manner exhibited substantial variation (Figure 2, Tables 2–4): while the least abundant L segment(Shayang Spider Virus 3) contributed to less than 0.001% to the total non-ribosomalRNA content, the most abundant (Sanxia Water Strider Virus 1) was at a frequency of21.2%, and up to 43.9% if we include the matching M and S segments of the virus. Theremaining viral RdRp sequences fell within a range (10–1000 TPM) that matchedthe abundance level of highly expressed host mitochondrial genes (Figure 2).10.7554/eLife.05378.008Figure 2.Abundance level (transcripts per million—TPM) of the RdRp genesfrom the negative-sense RNA viruses detected in this study.

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