4.7 Article

A mosquito small RNA genomics resource reveals dynamic evolution and host responses to viruses and transposons

Journal

GENOME RESEARCH
Volume 31, Issue 3, Pages 512-528

Publisher

COLD SPRING HARBOR LAB PRESS, PUBLICATIONS DEPT
DOI: 10.1101/gr.265157.120

Keywords

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Funding

  1. NIH [R01AG052465, R21-HD088792, R01-GM135215, R01-AI128201, R01-AI116636, R01-AI150251]
  2. Defense Advanced Research Project Agency (DARPA) Safe Genes Program [HR0011-17-2-0047]
  3. NIH New Innovator Award [1DP2AI152071-01]
  4. Office of Extramural Research, NIH [R21AI129881]
  5. Liverpool School of Tropical Medicine Director's Catalyst Fund
  6. Biotechnology and Biological Sciences Research Council (BBSRC) [BB/T001240/1]
  7. Royal Society Wolfson Fellowship [RSWF\R1\180013]
  8. BBSRC Network Grant ANTI-VeC [AV/PP0020/1]
  9. Bill & Melinda Gates Foundation [U01CK000509]
  10. Centers for Disease Control and Prevention
  11. BBSRC [BB/T001240/1, BB/R005338/1] Funding Source: UKRI

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Mosquitoes exhibit little impact of viral infection on their health due to the RNA interference pathways generating antiviral siRNAs and piRNAs. An integrated mosquito small RNA genomics resource was developed to analyze viral and transposon small RNA profiles across different mosquito species, revealing a novel piRNA cluster locus and regular periodicity in piRNA biogenesis patterns coinciding with the expansion of Piwi pathway genes. The resource enables detection of cross talk between piRNA and siRNA populations in mosquito cells during virus infection.
Although mosquitoes are major transmission vectors for pathogenic arboviruses, viral infection has little impact on mosquito health. This immunity is caused in part by mosquito RNA interference (RNAi) pathways that generate antiviral small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). RNAi also maintains genome integrity by potently re pressing mosquito transposon activity in the germline and soma. However, viral and transposon small RNA regulatory pathways have not been systematically examined together in mosquitoes. Therefore, we developed an integrated mosquito small RNA genomics (MSRG) resource that analyzes the transposon and virus small RNA profiles in mosquito cell cultures and somatic and gonadal tissues across four medically important mosquito species. Our resource captures both somatic and gonadal small RNA expression profiles within mosquito cell cultures, and we report the evolutionary dynamics of a novel Mosquito-Conserved piRNA Cluster Locus (MCpiRCL) made up of satellite DNA repeats. In the larger culicine mosquito genomes we detected highly regular periodicity in piRNA biogenesis patterns coinciding with the expansion of Piwi pathway genes. Finally, our resource enables detection of cross talk between piRNA and siRNA populations in mosquito cells during a response to virus infection. The MSRG resource will aid efforts to dissect and combat the capacity of mosquitoes to

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