Conserved virome diversity and structure in the mosquito vector Culex pipiens. P15
Patricia GilIgnace RakotoarivonyÉtienne LoireAlbane MarieBenoît FrancésGrégory L’AmbertNúria Busquets-MartíLotty BirnbergSandra TalaveraCarles ArandaMohamed BessatYehia OtifyGiuseppe MansiniMaria GoffredoEmna AyariSelma MejriErika MuthJustine ChevalLouise De VisserArnaud LamanyÉric CabannesCharles HébertMarc ÉloitSerafín Gutiérrez
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Recent epidemics caused by different mosquito‐borne viruses underline the viral diversity associated to mosquitoes. However, beyond human viral pathogens, we know little on other viruses of the mosquito virome. This unexplored diversity probably influences vector competence and other aspects of the mosquito biology, as shown for the mosquito bacteriome. We have analysed the virome of Culex pipiens, a mosquito vector of important arboviruses like Rift Valley fever virus or West Nile fever virus. To this end, we have coupled a metagenomics approach with a large sampling campaign involving different countries and habitats around the Mediterranean basin. Our results show for the first time conserved patterns in virus diversity among mosquito populations, as well as specificities probably linked to different environmental conditions. The discovery of a ubiquitous group of viruses strongly supports the existence of a core virome in Culex pipiens that is likely to influence mosquito physiology.Keywords:
Human virome
Culex pipiens
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Abstract Mosquitoes belonging to the genus Aedes can efficiently transmit many pathogenic arboviruses, placing a great burden on public health worldwide. In addition, they also carry a number of insect specific viruses (ISVs), and it was recently suggested that some of these ISVs might form a stable species-specific “core virome” in mosquito populations. However, little is known about such a core virome in laboratory colonies and if it is present across different developmental stages. In this study, we compared the viromes in eggs, larvae, pupae and adults of Aedes albopictus mosquitoes collected from the field as well as from a lab colony. The virome in lab-derived Ae. albopictus is very stable across all stages, consistent with a vertical transmission route of these viruses, forming a “vertically transmitted core virome”. The different stages of field collected Ae. albopictus mosquitoes also contains this stable vertically transmitted core virome as well as another set of viruses shared by mosquitoes across different stages, which might be an “environment derived core virome”. Both these vertically and environmentally transmitted core viromes in Ae. albopictus deserve more attention with respect to their effects on vector competence for important medically relevant arboviruses. To further study this core set of ISVs, we screened 46 publically available SRA viral metagenomic dataset of mosquitoes belonging to the genus Aedes . Some of the identified core ISVs are identified in the majority of SRAs. In addition, a novel virus, Aedes phasmavirus, is found to be distantly related to Yongsan bunyavirus 1, and the genomes of the core virus Phasi Charoen-like phasivirus is highly prevalent in the majority of the tested samples, with nucleotide identities ranging from 94% to 99%. Finally, Guadeloupe mosquito virus, and some related viruses formed three separated phylogenetic clades. How these core ISVs influence the biology of mosquito host, arboviruses infection and evolution deserve to be further explored.
Human virome
Aedes albopictus
Zika Virus
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Aedes mosquitoes can efficiently transmit many pathogenic arboviruses, placing a great burden on public health worldwide. In addition, they also carry a number of insect-specific viruses (ISVs), and it was recently suggested that some of these ISVs might form a stable species-specific "core virome" in mosquito populations. However, little is known about such a core virome in laboratory colonies and if it is present across different developmental stages. In this study, we compared the viromes in eggs, larvae, pupae, and adults of Aedes albopictus mosquitoes collected from a lab colony and compared each to the virome of different developmental stages collected in the field. The virome in lab-derived A. albopictus was very stable across all stages, consistent with a vertical transmission route of these viruses, and formed a possible "vertically transmitted core virome." The different stages of field-collected A. albopictus mosquitoes also contained this stable vertically transmitted core virome, as well as another set of viruses (e.g., viruses distantly related to Guadeloupe mosquito virus, Hubei virga-like virus 2, and Sarawak virus) shared by mosquitoes across different stages, which might represent an "environment-derived core virome." To further study this core set of ISVs, we screened 48 publicly available SRA viral metagenomic data sets of mosquitoes belonging to the genus Aedes, showing that some of the identified ISVs were identified in the majority of SRAs and providing further evidence supporting the core-virome concept.IMPORTANCE Our study revealed that the virome was very stable across all developmental stages of both lab-derived and field-collected Aedes albopictus The data representing the core virome in lab A. albopictus proved the vertical transmission route of these viruses, forming a "vertically transmitted core virome." Field mosquitoes also contained this stable vertically transmitted core virome as well as additional viruses, which probably represented "environment-derived core virome" and which therefore were less stable over time and geography. By further screening publicly available SRA viral metagenomic data sets from mosquitoes belonging to the genus Aedes, some of the identified core ISVs were shown to be present in the majority of SRAs, such as Phasi Charoen-like phasivirus and Guadeloupe mosquito virus. How these core ISVs influence the biology of the mosquito host and arbovirus infection and evolution deserves to be further explored.
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Aedes albopictus
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Culex pipiens is a mosquito vector of West Nile virus (WNV), the causing agent of West Nile fever. Epizooties of WNV have taken place in France, mainly in French Camargue, and in some instances human cases have been diagnosed. However, beyond WNV, little is known on the viruses associated to Culex pipiens, above all on viruses non-pathogenic for humans or livestock. Such viruses could have a role in WNV epidemiology either limiting mosquito populations or modulating the chances of WNV infection of Culex pipiens. Since the human impact of an ecosystem usually has an influence on species diversity, we can imagine a negative impact of human activity on the diversity of viral communities. Here we describe the development of an effective methodology for exploring viral diversity using high-throughput sequencing. We present the first results of the virome of Culex pipiens from sites with two different level of human activity in Camargue, showing that our approach allows to identify new viruses and, in some cases, to obtain almost full-length viral genomes. (Texte integral)
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Culex pipiens
Flavivirus
West Nile virus
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Viral diversity is theorized to play a significant role during virus infections, particularly for arthropod-borne viruses (arboviruses) that must infect both vertebrate and invertebrate hosts. To determine how viral diversity influences mosquito infection and dissemination Culex taeniopus mosquitoes were infected with the Venezuelan equine encephalitis virus endemic strain 68U201. Bodies and legs/wings of the mosquitoes were collected individually and subjected to multi-parallel sequencing. Virus sequence diversity was calculated for each tissue. Greater diversity was seen in mosquitoes with successful dissemination versus those with no dissemination. Diversity across time revealed that bottlenecks influence diversity following dissemination to the legs/wings, but levels of diversity are restored by Day 12 post-dissemination. Specific minority variants were repeatedly identified across the mosquito cohort, some in nearly every tissue and time point, suggesting that certain variants are important in mosquito infection and dissemination. This study demonstrates that the interaction between the mosquito and the virus results in changes in diversity and the mutational spectrum and may be essential for successful transition of the bottlenecks associated with arbovirus infection.
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Mosquitoes are classified into approximately 3500 species and further grouped into 41 genera. Epidemiologically, they are considered to be among the most important disease vectors in the world and they can harbor a wide variety of viruses. Several mosquito viruses are considered to be of significant medical importance and can cause serious public health issues throughout the world. Such viruses are Japanese encephalitis virus (JEV), dengue virus (DENV), chikungunya virus (CHIKV), and Zika virus (ZIKV). Others are the newly recognized mosquito viruses such as Banna virus (BAV) and Yunnan orbivirus (YNOV) with unclear medical significance. The remaining mosquito viruses are those that naturally infect mosquitoes but do not appear to infect humans or other vertebrates. With the continuous development and improvement of mosquito and mosquito-associated virus surveillance systems in China, many novel mosquito-associated viruses have been discovered in recent years. This review aims to systematically outline the history, characteristics, distribution, and/or current epidemic status of mosquito-associated viruses in China.
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Anopheles gambiae are a major vector of malaria in sub-Saharan Africa. Viruses that naturally infect these mosquitoes may impact their physiology and ability to transmit pathogens. We therefore used metagenomics sequencing to search for viruses in adult Anopheles mosquitoes collected from Liberia, Senegal, and Burkina Faso. We identified a number of virus and virus-like sequences from mosquito midgut contents, including 14 coding-complete genome segments and 26 partial sequences. The coding-complete sequences define new viruses in the order Mononegavirales, and the families Flaviviridae, and Totiviridae. The identification of a flavivirus infecting Anopheles mosquitoes broadens our understanding of the evolution and host range of this virus family. This study increases our understanding of virus diversity in general, begins to define the virome of a medically important vector in its natural setting, and lays groundwork for future studies examining the potential impact of these viruses on anopheles biology and disease transmission.
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Anopheles gambiae
Flavivirus
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Mosquitoes are the most important vectors for arthropod-borne viral diseases. Mixed viral infections of mosquitoes allow genetic recombination or reassortment of diverse viruses, turning mosquitoes into potential virologic mixing bowls. In this study, we field-collected mosquitoes of different species (Aedes aegypti and Culex pipiens complex), from different geographic locations and environments (central Europe and the Caribbean) for highly sensitive next-generation sequencing-based virome characterization. We found a rich virus community associated with a great diversity of host species. Among those, we detected a large diversity of novel virus sequences that we could predominately assign to circular Rep-encoding single-stranded (CRESS) DNA viruses, including the full-length genome of a yet undescribed Gemykrogvirus species. Moreover, we report for the first time the detection of a potentially zoonotic CRESS-DNA virus (Cyclovirus VN) in mosquito vectors. This study expands the knowledge on virus diversity in medically important mosquito vectors, especially for CRESS-DNA viruses that have previously been shown to easily recombine and jump the species barrier.
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Culex pipiens
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DNA virus
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Metagenomic studies of mosquitoes have revealed that their virome is far more diverse and includes many more viruses than just the pathogenic arboviruses vectored by mosquitoes. In this study, the virome of 953 female mosquitoes collected in the summer of 2017, representing six mosquito species from two geographic locations in Mid-Eastern Sweden, were characterized. In addition, the near-complete genome of nine RNA viruses were characterized and phylogenetically analysed. These viruses showed association to the viral orders Bunyavirales, Picornavirales, Articulavirales, and Tymovirales, and to the realm Ribovira. Hence, through this study, we expand the knowledge of the virome composition of different mosquito species in Sweden. In addition, by providing viral reference genomes from wider geographic regions and different mosquito species, future in silico recognition and assembly of viral genomes in metagenomic datasets will be facilitated.
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Viral evolution
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There is a dramatic lack of data on the virome of arthropods transmitting pathogenic viruses for humans and livestock. For example, we do not yet know whether there is a group of virus species that are predominant and conserved in the virome of many important vectors no matter the environment. These putative core virome could influence vector competence and other aspects of vector biology, as observed in the bacteriome of mosquito vectors. The study of the virome can thus unveil unknown aspects of the vector lifecycle, a knowledge that could empower vector control strategies. We have analysed the virome of Culex pipiens, a mosquito vector of important arboviruses like Rift Valley fever virus or West Nile fever virus, coupling a metagenomics approach and a large sampling campaign around the Mediterranean Sea. Our results show for the first time conserved patterns in diversity and structure within the virome of an important mosquito vector as well as specificities probably linked to different environmental conditions. (Texte integral)
Human virome
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Summary In the last decade, virus hunting and discovery has gained pace. This achievement has been driven by three major factors: (a) advancements in sequencing technologies, (b) scaled‐up routine arbovirus surveillance strategies, and (c) the “hunt” for emerging pathogens and novel viruses. Many novel viruses have been discovered from a myriad of hosts, vectors, and environmental samples. To help promote understanding of the global diversity and distribution of mosquito‐associated viruses and facilitate future studies, we review mosquito‐associated viruses discovered between years 2007 and 2017, across the world. In the analyzed period, novel mosquito‐associated viruses belonging to 25 families and a general group of unclassified viruses were categorized. The top three discovered novel mosquito‐associated viruses belonged to families Flaviviridae (n=32), Rhabdoviridae (n=16), and Peribunyaviridae (n=14). Also, 67 unclassified viruses were reported. Majority of these novel viruses were identified from Culex spp, Anopheles spp, Aedes spp, and Mansonia spp mosquitoes, respectively. Notably, the number of these discovered novels is not representative of intercontinental virus diversity but rather is influenced by the number of studies done in the study period. Some of these newly discovered mosquito‐associated viruses have medical significance, either directly or indirectly. For instance, in the study period, 14 novel mosquito‐borne viruses that infect mammalian cells in vitro were reported. These viruses pose a danger to the global health security on emerging viral diseases. On the other hand, some of the newly discovered insect specific viruses described herein have potential application as future biocontrol and vaccine agents against known pathogenic arboviruses. Overall, this review outlines the crucial role played by mosquitoes as viral vectors in the global virosphere.
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