Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements

Cristina M. Crava; Finny S. Varghese; Elisa Pischedda; Rebecca Halbach; Umberto Palatini; Michele Marconcini; Leila Gasmi; Seth Redmond; Yaw Afrane; Diego Ayala; Christophe Paupy; Rebeca Carballar-Lejarazu; Pascal Miesen; Ronald P. van Rij; Mariangela Bonizzoni

doi:10.1111/mec.15798

Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements

Cristina M. Crava, Finny S. Varghese, Elisa Pischedda, Rebecca Halbach, Umberto Palatini, Michele Marconcini, Leila Gasmi, Seth Redmond, Yaw Afrane, Diego Ayala, Christophe Paupy, Rebeca Carballar-Lejarazu, Pascal Miesen, Ronald P. van Rij, Mariangela Bonizzoni

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

21 Citations (Scopus)

Abstract

Horizontal gene transfer from viruses to eukaryotic cells is a pervasive phenomenon. Somatic viral integrations are linked to persistent viral infection whereas integrations into germline cells are maintained in host genomes by vertical transmission and may be co-opted for host functions. In the arboviral vector Aedes aegypti, an endogenous viral element from a nonretroviral RNA virus (nrEVE) was shown to produce PIWI-interacting RNAs (piRNAs) to limit infection with a cognate virus. Thus, nrEVEs may constitute a heritable, sequence-specific mechanism for antiviral immunity, analogous to piRNA-mediated silencing of transposable elements. Here, we combine population genomics and evolutionary approaches to analyse the genomic architecture of nrEVEs in A. aegypti. We conducted a genome-wide screen for adaptive nrEVEs and searched for novel population-specific nrEVEs in the genomes of 80 individual wild-caught mosquitoes from five geographical populations. We show a dynamic landscape of nrEVEs in mosquito genomes and identified five novel nrEVEs derived from two currently circulating viruses, providing evidence of the environmental-dependent modification of a piRNA cluster. Overall, our results show that virus endogenization events are complex with only a few nrEVEs contributing to adaptive evolution in A. aegypti.

Original language	English
Pages (from-to)	1594-1611
Number of pages	18
Journal	Molecular Ecology
Volume	30
Issue number	7
DOIs	https://doi.org/10.1111/mec.15798
Publication status	Published - Apr 2021

Keywords

Aedes aegypti
endogenous viral elements
mosquito genomes
piRNA cluster

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343106598-oaFinal published version, 1.79 MBLicence: CC BY-NC-ND

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Crava, C. M., Varghese, F. S., Pischedda, E., Halbach, R., Palatini, U., Marconcini, M., Gasmi, L., Redmond, S., Afrane, Y., Ayala, D., Paupy, C., Carballar-Lejarazu, R., Miesen, P., van Rij, R. P., & Bonizzoni, M. (2021). Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements. Molecular Ecology, 30(7), 1594-1611. https://doi.org/10.1111/mec.15798

@article{62bc6131c12a45bc8eca2d68acffc594,

title = "Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements",

abstract = "Horizontal gene transfer from viruses to eukaryotic cells is a pervasive phenomenon. Somatic viral integrations are linked to persistent viral infection whereas integrations into germline cells are maintained in host genomes by vertical transmission and may be co-opted for host functions. In the arboviral vector Aedes aegypti, an endogenous viral element from a nonretroviral RNA virus (nrEVE) was shown to produce PIWI-interacting RNAs (piRNAs) to limit infection with a cognate virus. Thus, nrEVEs may constitute a heritable, sequence-specific mechanism for antiviral immunity, analogous to piRNA-mediated silencing of transposable elements. Here, we combine population genomics and evolutionary approaches to analyse the genomic architecture of nrEVEs in A. aegypti. We conducted a genome-wide screen for adaptive nrEVEs and searched for novel population-specific nrEVEs in the genomes of 80 individual wild-caught mosquitoes from five geographical populations. We show a dynamic landscape of nrEVEs in mosquito genomes and identified five novel nrEVEs derived from two currently circulating viruses, providing evidence of the environmental-dependent modification of a piRNA cluster. Overall, our results show that virus endogenization events are complex with only a few nrEVEs contributing to adaptive evolution in A. aegypti.",

keywords = "Aedes aegypti, endogenous viral elements, mosquito genomes, piRNA cluster",

author = "Crava, {Cristina M.} and Varghese, {Finny S.} and Elisa Pischedda and Rebecca Halbach and Umberto Palatini and Michele Marconcini and Leila Gasmi and Seth Redmond and Yaw Afrane and Diego Ayala and Christophe Paupy and Rebeca Carballar-Lejarazu and Pascal Miesen and {van Rij}, {Ronald P.} and Mariangela Bonizzoni",

note = "Funding Information: This research was funded by a Human Frontier Science Program Research grant (RGP0007/2017) to R.v.R. and M.B.; by the Italian Ministry of Education, University and Research FARE‐MIUR project R1623HZAH5 to M.B.; by a European Research Council Consolidator Grant (ERC‐CoG) under the European Union{\textquoteright}s Horizon 2020 Programme (Grant No. ERC‐CoG 682394) to M.B.; by a European Research Council Consolidator Grant (ECR‐CoG) under the European Union{\textquoteright}s Seventh Framework Programme (ERC‐CoG 615680) to R.v.R.; by a VICI grant from the Netherlands Organization for Scientific Research (NWO, grant no. 016.VICI.170.090) to R.v.R.; and by the Italian Ministry of Education, University and Research (MIUR): Dipartimenti Eccellenza Program (2018–2022) to the Department of Biology and Biotechnology “L. Spallanzani,” University of Pavia. Publisher Copyright: {\textcopyright} 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = apr,

doi = "10.1111/mec.15798",

language = "English",

volume = "30",

pages = "1594--1611",

journal = "Molecular Ecology",

issn = "0962-1083",

publisher = "Wiley-Blackwell",

number = "7",

}

Crava, CM, Varghese, FS, Pischedda, E, Halbach, R, Palatini, U, Marconcini, M, Gasmi, L, Redmond, S, Afrane, Y, Ayala, D, Paupy, C, Carballar-Lejarazu, R, Miesen, P, van Rij, RP & Bonizzoni, M 2021, 'Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements', Molecular Ecology, vol. 30, no. 7, pp. 1594-1611. https://doi.org/10.1111/mec.15798

TY - JOUR

T1 - Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements

AU - Crava, Cristina M.

AU - Varghese, Finny S.

AU - Pischedda, Elisa

AU - Halbach, Rebecca

AU - Palatini, Umberto

AU - Marconcini, Michele

AU - Gasmi, Leila

AU - Redmond, Seth

AU - Afrane, Yaw

AU - Ayala, Diego

AU - Paupy, Christophe

AU - Carballar-Lejarazu, Rebeca

AU - Miesen, Pascal

AU - van Rij, Ronald P.

AU - Bonizzoni, Mariangela

N1 - Funding Information: This research was funded by a Human Frontier Science Program Research grant (RGP0007/2017) to R.v.R. and M.B.; by the Italian Ministry of Education, University and Research FARE‐MIUR project R1623HZAH5 to M.B.; by a European Research Council Consolidator Grant (ERC‐CoG) under the European Union’s Horizon 2020 Programme (Grant No. ERC‐CoG 682394) to M.B.; by a European Research Council Consolidator Grant (ECR‐CoG) under the European Union’s Seventh Framework Programme (ERC‐CoG 615680) to R.v.R.; by a VICI grant from the Netherlands Organization for Scientific Research (NWO, grant no. 016.VICI.170.090) to R.v.R.; and by the Italian Ministry of Education, University and Research (MIUR): Dipartimenti Eccellenza Program (2018–2022) to the Department of Biology and Biotechnology “L. Spallanzani,” University of Pavia. Publisher Copyright: © 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/4

Y1 - 2021/4

N2 - Horizontal gene transfer from viruses to eukaryotic cells is a pervasive phenomenon. Somatic viral integrations are linked to persistent viral infection whereas integrations into germline cells are maintained in host genomes by vertical transmission and may be co-opted for host functions. In the arboviral vector Aedes aegypti, an endogenous viral element from a nonretroviral RNA virus (nrEVE) was shown to produce PIWI-interacting RNAs (piRNAs) to limit infection with a cognate virus. Thus, nrEVEs may constitute a heritable, sequence-specific mechanism for antiviral immunity, analogous to piRNA-mediated silencing of transposable elements. Here, we combine population genomics and evolutionary approaches to analyse the genomic architecture of nrEVEs in A. aegypti. We conducted a genome-wide screen for adaptive nrEVEs and searched for novel population-specific nrEVEs in the genomes of 80 individual wild-caught mosquitoes from five geographical populations. We show a dynamic landscape of nrEVEs in mosquito genomes and identified five novel nrEVEs derived from two currently circulating viruses, providing evidence of the environmental-dependent modification of a piRNA cluster. Overall, our results show that virus endogenization events are complex with only a few nrEVEs contributing to adaptive evolution in A. aegypti.

AB - Horizontal gene transfer from viruses to eukaryotic cells is a pervasive phenomenon. Somatic viral integrations are linked to persistent viral infection whereas integrations into germline cells are maintained in host genomes by vertical transmission and may be co-opted for host functions. In the arboviral vector Aedes aegypti, an endogenous viral element from a nonretroviral RNA virus (nrEVE) was shown to produce PIWI-interacting RNAs (piRNAs) to limit infection with a cognate virus. Thus, nrEVEs may constitute a heritable, sequence-specific mechanism for antiviral immunity, analogous to piRNA-mediated silencing of transposable elements. Here, we combine population genomics and evolutionary approaches to analyse the genomic architecture of nrEVEs in A. aegypti. We conducted a genome-wide screen for adaptive nrEVEs and searched for novel population-specific nrEVEs in the genomes of 80 individual wild-caught mosquitoes from five geographical populations. We show a dynamic landscape of nrEVEs in mosquito genomes and identified five novel nrEVEs derived from two currently circulating viruses, providing evidence of the environmental-dependent modification of a piRNA cluster. Overall, our results show that virus endogenization events are complex with only a few nrEVEs contributing to adaptive evolution in A. aegypti.

KW - Aedes aegypti

KW - endogenous viral elements

KW - mosquito genomes

KW - piRNA cluster

UR - http://www.scopus.com/inward/record.url?scp=85101239473&partnerID=8YFLogxK

U2 - 10.1111/mec.15798

DO - 10.1111/mec.15798

M3 - Article

C2 - 33432714

AN - SCOPUS:85101239473

VL - 30

SP - 1594

EP - 1611

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 7

ER -

Population genomics in the arboviral vector Aedes aegypti reveals the genomic architecture and evolution of endogenous viral elements

Abstract

Keywords

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