Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatus
ABSTRACT Arboviruses and insect-specific viruses (ISVs) are two major types of viruses harbored by mosquitoes that are distinguished by the involvement of vertebrate hosts in their transmission cycles. While intensive studies have focused on the transmission, tissue tropism, and evolution of arbovir...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01344-22 |
| _version_ | 1811198131552911360 |
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| author | Yan-Jun Kang Guoding Zhu Yang Cheng Haitao Yang Jun Cao |
| author_facet | Yan-Jun Kang Guoding Zhu Yang Cheng Haitao Yang Jun Cao |
| author_sort | Yan-Jun Kang |
| collection | DOAJ |
| description | ABSTRACT Arboviruses and insect-specific viruses (ISVs) are two major types of viruses harbored by mosquitoes that are distinguished by the involvement of vertebrate hosts in their transmission cycles. While intensive studies have focused on the transmission, tissue tropism, and evolution of arboviruses, these characteristics are poorly investigated in ISVs, which dominate the mosquito virome. Therefore, in this study, we collected two mosquito species, Anopheles sinensis and Culex quinquefasciatus, in the field and used a metatranscriptomics approach to characterize their RNA viromes in different tissues, such as the midgut, legs, salivary gland, eggs, and the remainder of the carcass. Blood-engorged individuals of these species were captured in 3 locations, and 60 mosquitoes were pooled from each species and location. A total of 40 viral species from diverse viral taxa associated with all viral RNA genome types were identified, among which 19 were newly identified in this study. According to the current viral taxonomy, some of these viruses, such as Yancheng Anopheles associated virus 2 (Narnaviridae) and Jiangsu Anopheles-related virus (Ghabrivirales), were novel. The two investigated mosquito species generally harbored distinct viromes. Nevertheless, the viruses were generally shared among different tissue types to various degrees. Specifically, the eggs possessed a viral community with significantly lower diversity and abundance than those in other tissues, whereas the legs and salivary glands exhibited higher viral abundance. The compositions and distributions of the viromes of different mosquito tissues were demonstrated for the first time in our study, providing important insight into the virome dynamics within individual mosquitoes. IMPORTANCE ISVs are considered to be ancestral to arboviruses. Because of their medical importance, arboviruses have been well studied from the aspects of their transmission mode, evolution of dual-host tropism, and genetic dynamics within mosquito vectors. However, the mode of ISV maintenance is poorly understood, even though many novel ISVs have been identified with the emergence of sequencing technology. In our study, in addition to the identification of a diverse virus community, the tissue tropism of RNA viromes harbored by two field-collected mosquito species was demonstrated for the first time. According to the results, the virus communities of different tissues, such as the salivary glands, midguts, legs, and eggs, can help us understand the evolution, transmission routes, and maintenance modes of mosquito-specific viruses in nature. |
| first_indexed | 2024-04-12T01:26:34Z |
| format | Article |
| id | doaj.art-bd1b698a007e4e28911c788f1c5ca98b |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-12T01:26:34Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-bd1b698a007e4e28911c788f1c5ca98b2022-12-22T03:53:39ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.01344-22Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatusYan-Jun Kang0Guoding Zhu1Yang Cheng2Haitao Yang3Jun Cao4Department of Pediatric Laboratory, Wuxi Children's Hospital, Wuxi, ChinaNational Health Commission Key Laboratory of Parasitic Disease Control and Prevention, Jiangsu Provincial Key Laboratory on Parasite and Vector Control Technology, Jiangsu Institute of Parasitic Diseases, Wuxi, ChinaWuxi School of Medicine & Public Health Research Center, Jiangnan University, Wuxi, ChinaNational Health Commission Key Laboratory of Parasitic Disease Control and Prevention, Jiangsu Provincial Key Laboratory on Parasite and Vector Control Technology, Jiangsu Institute of Parasitic Diseases, Wuxi, ChinaNational Health Commission Key Laboratory of Parasitic Disease Control and Prevention, Jiangsu Provincial Key Laboratory on Parasite and Vector Control Technology, Jiangsu Institute of Parasitic Diseases, Wuxi, ChinaABSTRACT Arboviruses and insect-specific viruses (ISVs) are two major types of viruses harbored by mosquitoes that are distinguished by the involvement of vertebrate hosts in their transmission cycles. While intensive studies have focused on the transmission, tissue tropism, and evolution of arboviruses, these characteristics are poorly investigated in ISVs, which dominate the mosquito virome. Therefore, in this study, we collected two mosquito species, Anopheles sinensis and Culex quinquefasciatus, in the field and used a metatranscriptomics approach to characterize their RNA viromes in different tissues, such as the midgut, legs, salivary gland, eggs, and the remainder of the carcass. Blood-engorged individuals of these species were captured in 3 locations, and 60 mosquitoes were pooled from each species and location. A total of 40 viral species from diverse viral taxa associated with all viral RNA genome types were identified, among which 19 were newly identified in this study. According to the current viral taxonomy, some of these viruses, such as Yancheng Anopheles associated virus 2 (Narnaviridae) and Jiangsu Anopheles-related virus (Ghabrivirales), were novel. The two investigated mosquito species generally harbored distinct viromes. Nevertheless, the viruses were generally shared among different tissue types to various degrees. Specifically, the eggs possessed a viral community with significantly lower diversity and abundance than those in other tissues, whereas the legs and salivary glands exhibited higher viral abundance. The compositions and distributions of the viromes of different mosquito tissues were demonstrated for the first time in our study, providing important insight into the virome dynamics within individual mosquitoes. IMPORTANCE ISVs are considered to be ancestral to arboviruses. Because of their medical importance, arboviruses have been well studied from the aspects of their transmission mode, evolution of dual-host tropism, and genetic dynamics within mosquito vectors. However, the mode of ISV maintenance is poorly understood, even though many novel ISVs have been identified with the emergence of sequencing technology. In our study, in addition to the identification of a diverse virus community, the tissue tropism of RNA viromes harbored by two field-collected mosquito species was demonstrated for the first time. According to the results, the virus communities of different tissues, such as the salivary glands, midguts, legs, and eggs, can help us understand the evolution, transmission routes, and maintenance modes of mosquito-specific viruses in nature.https://journals.asm.org/doi/10.1128/spectrum.01344-22insect-specific virusesvirometissue tropismAnopheles sinensisCulex quinquefasciatus |
| spellingShingle | Yan-Jun Kang Guoding Zhu Yang Cheng Haitao Yang Jun Cao Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatus Microbiology Spectrum insect-specific viruses virome tissue tropism Anopheles sinensis Culex quinquefasciatus |
| title | Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatus |
| title_full | Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatus |
| title_fullStr | Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatus |
| title_full_unstemmed | Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatus |
| title_short | Deciphering the Tissue Tropism of the RNA Viromes Harbored by Field-Collected Anopheles sinensis and Culex quinquefasciatus |
| title_sort | deciphering the tissue tropism of the rna viromes harbored by field collected anopheles sinensis and culex quinquefasciatus |
| topic | insect-specific viruses virome tissue tropism Anopheles sinensis Culex quinquefasciatus |
| url | https://journals.asm.org/doi/10.1128/spectrum.01344-22 |
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