A mosquito small RNA genomics resource reveals dynamic evolution and host responses to viruses and transposons
- Qicheng Ma1,8,
- Satyam P. Srivastav1,8,
- Stephanie Gamez2,8,
- Gargi Dayama1,
- Fabiana Feitosa-Suntheimer3,
- Edward I. Patterson4,
- Rebecca M. Johnson5,
- Erik M. Matson1,
- Alexander S. Gold3,
- Douglas E. Brackney6,
- John H. Connor3,
- Tonya M. Colpitts3,
- Grant L. Hughes4,
- Jason L. Rasgon5,
- Tony Nolan4,
- Omar S. Akbari2 and
- Nelson C. Lau1,7
- 1Department of Biochemistry, Boston University School of Medicine, Boston, Massachusetts 02118, USA;
- 2Division of Biological Sciences, Section of Cell and Developmental Biology, University of California San Diego, La Jolla, California 92093, USA;
- 3Department of Microbiology and the National Emerging Infectious Disease Laboratory, Boston University School of Medicine, Boston, Massachusetts 02118, USA;
- 4Departments of Vector Biology and Tropical Disease Biology, Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Liverpool L3 5QA, United Kingdom;
- 5Department of Entomology, Center for Infectious Disease Dynamics, and the Huck Institutes for the Life Sciences, Pennsylvania State University, University Park, Pennsylvania 16802, USA;
- 6Department of Environmental Sciences, The Connecticut Agricultural Experiment Station, New Haven, Connecticut 06511, USA;
- 7Boston University Genome Science Institute and the National Emerging Infectious Disease Laboratory, Boston, Massachusetts 02118, USA
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↵8 These authors contributed equally to this work.
Abstract
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 repressing 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 tolerate and spread arboviruses.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.265157.120.
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Freely available online through the Genome Research Open Access option.
- Received April 25, 2020.
- Accepted January 6, 2021.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
