Cargando…

Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae

In this study, many virus-like fragments were obtained from transcriptomes of three wasp species, including Anisopteromalus calandrae (8), Lariophagus distinguendus (3), and Theocolax elegans (18), which can parasitize and control rice weevil Sitophilus oryzae, a serious insect pest of farm-stored g...

Descripción completa

Detalles Bibliográficos
Autores principales: Wang, Fei, Yuan, Bo, Xiao, Shan, Zhang, Jiao, Jia, Wenxi, Fang, Qi, Wang, Fang, Song, Qisheng, Ye, Gongyin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8103988/
https://www.ncbi.nlm.nih.gov/pubmed/33952664
http://dx.doi.org/10.1128/mSphere.00331-21
_version_ 1783689401887358976
author Wang, Fei
Yuan, Bo
Xiao, Shan
Zhang, Jiao
Jia, Wenxi
Fang, Qi
Wang, Fang
Song, Qisheng
Ye, Gongyin
author_facet Wang, Fei
Yuan, Bo
Xiao, Shan
Zhang, Jiao
Jia, Wenxi
Fang, Qi
Wang, Fang
Song, Qisheng
Ye, Gongyin
author_sort Wang, Fei
collection PubMed
description In this study, many virus-like fragments were obtained from transcriptomes of three wasp species, including Anisopteromalus calandrae (8), Lariophagus distinguendus (3), and Theocolax elegans (18), which can parasitize and control rice weevil Sitophilus oryzae, a serious insect pest of farm-stored grains. By further bioinformatic analysis and sequencing, we identified six novel RNA viruses with complete genomes and named them WWPSRV-1, WWPSRV-2, AcPSRV-1, AcNSRV-1, AcNSRV-2, and LdNSRV-1. PCR-based detection revealed that WWPSRV-1 and WWPSRV-2 had the possibility of interspecies virus transmission, especially WWPSRV-2, which was also present in the rice weevil adults. Phylogenetically, three out of these six viruses appeared to be members of order Picornavirales: WWPSRV-1 belonged to unassigned virus families of this order, whereas WWPSRV-2 and AcPSRV-1 belonged to families Iflaviridae and Dicistroviridae, respectively. The conserved picornavirus-typical domains helicase, protease, and RNA-dependent RNA polymerase could be found in the nonstructural protein encoded by the three viruses, whose genomes consisted of the different numbers of open reading frames (ORFs). The other three RNA viruses could be classified to order Mononegavirales: AcNSRV-1 and AcNSRV-2 belonged to family Lispiviridae, whereas LdNSRV-1 belonged to a big family Rhabdoviridae. The genomes of the three viruses contained at least five ORFs, encoding deduced proteins in the following order: 3′-N-P-M-G-L-5′. All the ORFs were separated by conserved intergenic sequences which likely regulated the transcription termination and initiation. Our findings enhance the understanding of RNA viruses in weevil wasps and set the foundation for the future study of the association among weevils, weevil wasps, and RNA viruses. IMPORTANCE The enormous diversity of RNA viruses in insects is continuously validated. Parasitoid wasps, as biocontrol insects which are widely used against insect pests in agroecosystems, may also carry many “good” RNA viruses. Some RNA viruses in parasitoid wasps have been reported to affect the host wasps or the wasps’ host. Here, six novel RNA viruses with complete genomes were identified in three parasitoid wasps of the rice weevil. One of these viruses was also detected in the rice weevil adults. Phylogenetically, WWPSRV-1 was the first unambiguous detection of Nora-like virus in insect parasitoids. WWPSRV-2 and AcPSRV-1 belong to families Iflaviridae and Dicistroviridae, some viruses of which can result in lethal infections in silkworms and honeybees. The other three RNA viruses belong to order Mononegavirales, which comprises many well-known insect-associated viruses.
format Online
Article
Text
id pubmed-8103988
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-81039882021-05-21 Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae Wang, Fei Yuan, Bo Xiao, Shan Zhang, Jiao Jia, Wenxi Fang, Qi Wang, Fang Song, Qisheng Ye, Gongyin mSphere Research Article In this study, many virus-like fragments were obtained from transcriptomes of three wasp species, including Anisopteromalus calandrae (8), Lariophagus distinguendus (3), and Theocolax elegans (18), which can parasitize and control rice weevil Sitophilus oryzae, a serious insect pest of farm-stored grains. By further bioinformatic analysis and sequencing, we identified six novel RNA viruses with complete genomes and named them WWPSRV-1, WWPSRV-2, AcPSRV-1, AcNSRV-1, AcNSRV-2, and LdNSRV-1. PCR-based detection revealed that WWPSRV-1 and WWPSRV-2 had the possibility of interspecies virus transmission, especially WWPSRV-2, which was also present in the rice weevil adults. Phylogenetically, three out of these six viruses appeared to be members of order Picornavirales: WWPSRV-1 belonged to unassigned virus families of this order, whereas WWPSRV-2 and AcPSRV-1 belonged to families Iflaviridae and Dicistroviridae, respectively. The conserved picornavirus-typical domains helicase, protease, and RNA-dependent RNA polymerase could be found in the nonstructural protein encoded by the three viruses, whose genomes consisted of the different numbers of open reading frames (ORFs). The other three RNA viruses could be classified to order Mononegavirales: AcNSRV-1 and AcNSRV-2 belonged to family Lispiviridae, whereas LdNSRV-1 belonged to a big family Rhabdoviridae. The genomes of the three viruses contained at least five ORFs, encoding deduced proteins in the following order: 3′-N-P-M-G-L-5′. All the ORFs were separated by conserved intergenic sequences which likely regulated the transcription termination and initiation. Our findings enhance the understanding of RNA viruses in weevil wasps and set the foundation for the future study of the association among weevils, weevil wasps, and RNA viruses. IMPORTANCE The enormous diversity of RNA viruses in insects is continuously validated. Parasitoid wasps, as biocontrol insects which are widely used against insect pests in agroecosystems, may also carry many “good” RNA viruses. Some RNA viruses in parasitoid wasps have been reported to affect the host wasps or the wasps’ host. Here, six novel RNA viruses with complete genomes were identified in three parasitoid wasps of the rice weevil. One of these viruses was also detected in the rice weevil adults. Phylogenetically, WWPSRV-1 was the first unambiguous detection of Nora-like virus in insect parasitoids. WWPSRV-2 and AcPSRV-1 belong to families Iflaviridae and Dicistroviridae, some viruses of which can result in lethal infections in silkworms and honeybees. The other three RNA viruses belong to order Mononegavirales, which comprises many well-known insect-associated viruses. American Society for Microbiology 2021-05-05 /pmc/articles/PMC8103988/ /pubmed/33952664 http://dx.doi.org/10.1128/mSphere.00331-21 Text en Copyright © 2021 Wang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Wang, Fei
Yuan, Bo
Xiao, Shan
Zhang, Jiao
Jia, Wenxi
Fang, Qi
Wang, Fang
Song, Qisheng
Ye, Gongyin
Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae
title Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae
title_full Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae
title_fullStr Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae
title_full_unstemmed Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae
title_short Diverse RNA Viruses Discovered in Three Parasitoid Wasps of the Rice Weevil Sitophilus oryzae
title_sort diverse rna viruses discovered in three parasitoid wasps of the rice weevil sitophilus oryzae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8103988/
https://www.ncbi.nlm.nih.gov/pubmed/33952664
http://dx.doi.org/10.1128/mSphere.00331-21
work_keys_str_mv AT wangfei diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT yuanbo diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT xiaoshan diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT zhangjiao diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT jiawenxi diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT fangqi diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT wangfang diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT songqisheng diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae
AT yegongyin diversernavirusesdiscoveredinthreeparasitoidwaspsofthericeweevilsitophilusoryzae