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

Qicheng Ma; Satyam P. Srivastav; Stephanie Gamez; Gargi Dayama; Fabiana Feitosa-Suntheimer; Ian Patterson; Rebecca M. Johnson; Erik M. Matson; Alexander S. Gold; Douglas E. Brackney; John H. Connor; Tonya M. Colpitts; Grant Hughes; Jason L. Rasgon; Tony Nolan; Omar S. Akbari; Nelson C. Lau

doi:10.1101/gr.265157.120

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

Qicheng Ma, Satyam P. Srivastav, Stephanie Gamez, Gargi Dayama, Fabiana Feitosa-Suntheimer, Ian Patterson, Rebecca M. Johnson, Erik M. Matson, Alexander S. Gold, Douglas E. Brackney, John H. Connor, Tonya M. Colpitts, Grant Hughes, Jason L. Rasgon, Tony Nolan, Omar S. Akbari, Nelson C. Lau

Research output: Contribution to journal › Article › peer-review

23 Citations (Scopus)

Abstract

Although mosquitoes are major transmission vectors for pathogenic arboviruses, viral infection has little impact on mosquito health. This immunity is due in part to 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) composed 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 crosstalk 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.

Original language	English
Pages (from-to)	512-528
Number of pages	17
Journal	Genome Research
Volume	31
Issue number	3
Early online date	8 Jan 2021
DOIs	https://doi.org/10.1101/gr.265157.120
Publication status	Published - 1 Apr 2021

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Genome ResAccepted author manuscript, 4.81 MBLicence: CC BY

23 Citations
1 Other contribution

Corrigendum: A mosquito small RNA genomics resource reveals dynamic evolution and host responses to viruses and transposons
Ma, Q., Srivastav, S. P., Gamez, S., Dayama, G., Feitosa-Suntheimer, F., Patterson, I., Johnson, R. M., Matson, E. M., Gold, A. S., Brackney, D. E., Connor, J. H., Colpitts, T. M., Hughes, G., Rasgon, J. L., Nolan, T., Akbari, O. S. & Lau, N. C., 7 Feb 2024, 1 p.
Research output: Other contribution

Open Access

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Ma, Q., Srivastav, S. P., Gamez, S., Dayama, G., Feitosa-Suntheimer, F., Patterson, I., Johnson, R. M., Matson, E. M., Gold, A. S., Brackney, D. E., Connor, J. H., Colpitts, T. M., Hughes, G., Rasgon, J. L., Nolan, T., Akbari, O. S., & Lau, N. C. (2021). A mosquito small RNA genomics resource reveals dynamic evolution and host responses to viruses and transposons. Genome Research, 31(3), 512-528. https://doi.org/10.1101/gr.265157.120

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abstract = "Although mosquitoes are major transmission vectors for pathogenic arboviruses, viral infection has little impact on mosquito health. This immunity is due in part to mosquito RNA interference (RNAi) pathways that generate antiviral small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). RNAi also maintains genomeintegrity 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 integratedMosquito 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) composed of satellite DNA repeats. In the larger culicine mosquito genomes we detected highly regular periodicity in piRNA biogenesis patterns coinciding with theexpansion of Piwi pathway genes. Finally, our resource enables detection of crosstalk 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 ofmosquitoes to tolerate and spread arboviruses.",

author = "Qicheng Ma and Srivastav, \{Satyam P.\} and Stephanie Gamez and Gargi Dayama and Fabiana Feitosa-Suntheimer and Ian Patterson and Johnson, \{Rebecca M.\} and Matson, \{Erik M.\} and Gold, \{Alexander S.\} and Brackney, \{Douglas E.\} and Connor, \{John H.\} and Colpitts, \{Tonya M.\} and Grant Hughes and Rasgon, \{Jason L.\} and Tony Nolan and Akbari, \{Omar S.\} and Lau, \{Nelson C.\}",

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Ma, Q, Srivastav, SP, Gamez, S, Dayama, G, Feitosa-Suntheimer, F, Patterson, I, Johnson, RM, Matson, EM, Gold, AS, Brackney, DE, Connor, JH, Colpitts, TM, Hughes, G, Rasgon, JL, Nolan, T, Akbari, OS & Lau, NC 2021, 'A mosquito small RNA genomics resource reveals dynamic evolution and host responses to viruses and transposons', Genome Research, vol. 31, no. 3, pp. 512-528. https://doi.org/10.1101/gr.265157.120

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AU - Ma, Qicheng

AU - Srivastav, Satyam P.

AU - Gamez, Stephanie

AU - Dayama, Gargi

AU - Feitosa-Suntheimer, Fabiana

AU - Patterson, Ian

AU - Johnson, Rebecca M.

AU - Matson, Erik M.

AU - Gold, Alexander S.

AU - Brackney, Douglas E.

AU - Connor, John H.

AU - Colpitts, Tonya M.

AU - Hughes, Grant

AU - Rasgon, Jason L.

AU - Nolan, Tony

AU - Akbari, Omar S.

AU - Lau, Nelson C.

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N2 - Although mosquitoes are major transmission vectors for pathogenic arboviruses, viral infection has little impact on mosquito health. This immunity is due in part to mosquito RNA interference (RNAi) pathways that generate antiviral small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). RNAi also maintains genomeintegrity 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 integratedMosquito 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) composed of satellite DNA repeats. In the larger culicine mosquito genomes we detected highly regular periodicity in piRNA biogenesis patterns coinciding with theexpansion of Piwi pathway genes. Finally, our resource enables detection of crosstalk 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 ofmosquitoes to tolerate and spread arboviruses.

AB - Although mosquitoes are major transmission vectors for pathogenic arboviruses, viral infection has little impact on mosquito health. This immunity is due in part to mosquito RNA interference (RNAi) pathways that generate antiviral small interfering RNAs (siRNAs) and Piwi-interacting RNAs (piRNAs). RNAi also maintains genomeintegrity 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 integratedMosquito 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) composed of satellite DNA repeats. In the larger culicine mosquito genomes we detected highly regular periodicity in piRNA biogenesis patterns coinciding with theexpansion of Piwi pathway genes. Finally, our resource enables detection of crosstalk 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 ofmosquitoes to tolerate and spread arboviruses.

U2 - 10.1101/gr.265157.120

DO - 10.1101/gr.265157.120

M3 - Article

SN - 1088-9051

VL - 31

SP - 512

EP - 528

JO - Genome Research

JF - Genome Research

IS - 3

ER -

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

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

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