Defining Virus-Carrier Networks That Shape the Composition of the Mosquito Core Virome of an Ecosystem

Abstract

BackgroundMosquitoes are the most important vectors of emerging infectious diseases. During the past decade, our understanding of the diversity of viruses they carry has greatly expanded. Most of these viruses are considered mosquito-specific, while there is increasing evidence that these viruses may affect mosquito vector potential. Metagenomics approaches have focused on specific mosquito species for the identification of what is called core virome. However, in most ecosystems, multiple species may participate in virus emergence and circulation, while there is lack of understanding on the viruses-carrier/host network for both vector-borne and mosquito-specific viruses. Results Here, we studied the core mosquito virome in a diverse ecosystem comprised of 24 different mosquito species. Analysis of these 24 diverse viromes resulted in the discovery of 35 viruses with known genetic traits and 9 novel viruses. Comparison of the viromes of the 24 individual species revealed novel relationships between mosquito species and virus families, as most of the mosquito species had never been analysed in the past. Groups of related viruses and mosquito species from multiple genera formed a complex network in the ecosystem. Analyses of whole traps of mosquitoes of variable composition not only showed a stable core virome for each species but also a relationship between mosquito population and virome composition.ConclusionsOur study highlighted the importance of a holistic approach regarding mosquito viromes in rich and diverse ecosystems. Our data further supported the idea of a stable core virome, characteristic of each mosquito species. The remarkable stability of the core virome seemed to determine the composition of the total mosquito core virome of a habitat in the ecosystem.

Intrinsic variation in the vertically transmitted core virome of the mosquito Aedes aegypti

“…Our et al, 2016), Armigeres in China (Zhai et al, 2010), Culex in Belgium (Wang et al, 2020), Culex in California (Batson et al, 2021), Culex in Australia (Williams et al, 2020), Culex in Japan (Isawa et al, 2011), andMansonia in Brazil (de Lara Pinto et al, 2017), suggesting that toti-like viruses may be common components of core viromes among mosquito populations. Metagenomic analyses of mosquitoes from our Palmetto site collected in 2016 and 2017 also identified a totilike virus, as well as dsRNA virus environmental sample (Boyles et al, 2020), further supporting that A. aegypti mosquitoes with similar genetic backgrounds (here, representative of central Florida-based populations) share many of the same viruses, as previously reported (Konstantinidis et al, 2021;Öhlund et al, 2019;Shi et al, 2019;Wang et al, 2020). unclassified Orthomyxoviridae virus) (Figure 3) were solely found in the field samples.…”

“…Similarly, the Partitiviridae and partiti‐like viruses have been historically associated with plants and fungi (Nibert et al, 2014), and their associations with arthropods have only recently been discovered, largely from high‐throughput sequencing data. Partitiviridae and partiti‐like viruses have been reported across numerous mosquito genera ( Culex , Culiseta , Coquilettidia , Anopheles , Aedes ) with a nearly global distribution (North and South America, Africa, Asia, and Europe) (Konstantinidis et al, 2021; Öhlund et al, 2019; Shi et al, 2019; Wang et al, 2020). The low congruence between viral host phylogeny and host‐range for these partiti‐like viruses may suggest a recent host‐switching event (Dolja & Koonin, 2018; Grubaugh et al, 2016), as the Palmetto partiti‐like virus was highly divergent (<80% similarity) from other known partiti‐like viruses and probably represents a novel virus.…”

“…Similarly, the Partitiviridae and partiti-like viruses have been historically associated with plants and fungi (Nibert et al, 2014) global distribution (North and South America, Africa, Asia, and Europe) (Konstantinidis et al, 2021;Öhlund et al, 2019;Shi et al, 2019;Wang et al, 2020). The low congruence between viral host phylogeny and host-range for these partiti-like viruses may suggest a recent host-switching event (Dolja & Koonin, 2018;Grubaugh et al, 2016), as the Palmetto partiti-like virus was highly divergent (<80% similarity) from other known partiti-like viruses and probably represents a novel virus.…”

Symbiotic Interactions Between Mosquitoes and Mosquito Viruses

“…Nasonia bacterial microbiota and virome exhibited a pattern of phylosymbiosis, primarily driven by bacteriophages hosted by the bacterial microbiota ( Leigh et al., 2018 ). Recent studies in mosquitoes have described a distinct core virome in different species of mosquitoes that were collected in the same region and share the same larval habitat ( Pettersson et al., 2019 ; Shi et al., 2019 ; Konstantinidis et al., 2021 ). The potential evolutionary significance of this core virome and whether/how it is maintained by the host is unknown.…”

Accumulated metagenomic studies reveal recent migration, whole genome evolution, and undiscovered diversity of orthomyxoviruses

“…Puerto Rican segments were recovered by mapping reads from SRA entries SRR3168916, SRR3168920, SRR3168922, and SRR3168925 (Frey et al, 2016) to segments of Californian strain CMS001 038 Ra S22 using bwa v0.7.17 (Li and Durbin, 2009) but most segments except for NP did not have good coverage to be assembled with certainty. Greek segments were recovered by mapping reads from SRA entry SRR13450231 (Konstantinidis et al, 2021) using the same approach as described earlier. New Chinese segments from 2018 (He et al, 2021) were similarly recovered by mapping reads from China National GeneBank Sequence Archive accessions CNR0266076 and CNR0266075 using the same approach as described earlier.…”