Commensal Viruses of Mosquitoes: Host Restriction, Transmission, and Interaction with Arboviral Pathogens

Abstract

Recent advances in virus detection strategies and deep sequencing technologies have enabled the identification of a multitude of new viruses that persistently infect mosquitoes but do not infect vertebrates. These are usually referred to as insect-specific viruses (ISVs). These novel viruses have generated considerable interest in their modes of transmission, persistence in mosquito populations, the mechanisms that restrict their host range to mosquitoes, and their interactions with pathogens transmissible by the same mosquito. In this article, we discuss studies in our laboratory and others that demonstrate that many ISVs are efficiently transmitted directly from the female mosquito to their progeny via infected eggs, and, moreover, that persistent infection of mosquito cell cultures or whole mosquitoes with ISVs can restrict subsequent infection, replication, and transmission of some mosquito-borne viral pathogens. This suggests that some ISVs may act as natural regulators of arboviral transmission. We also discuss viral and host factors that may be responsible for their host restriction.

High-Resolution Metatranscriptomics Reveals the Ecological Dynamics of Mosquito-Associated RNA Viruses in Western Australia

“…As the viruses present in these different countries are very similar (95% to ϳ98% nucleotide identities), such limited genetic distance tentatively suggests that these viruses were introduced by windblown mosquitoes (36,37) or by cyclones from neighboring regions (38) or were inadvertently spread by humans, rather than the result of ancient mosquito dispersal. Conversely, based on current data, there appears to be relatively little overlap between the mosquito viromes sampled from Western Australia and those sampled from other parts of Australia (3,10), which may reflect the different mosquito species present in these localities. In addition, a previous survey of viruses in Eastern Australia was performed after the viruses were passaged in cell culture, which may eliminate some of the viruses present in the original sample (10).…”

“…However, in addition to their role as transmission vectors, mosquitoes harbor a far larger virome, including many viruses that are confined to these insects, such that they are "insect specific" (1,2). Although these insect-specific viruses have no direct impact on public health, they may modulate the transmission of viruses that are pathogenic to vertebrates (3). The development of metagenomic sequencing approaches has therefore led to a reevaluation of the mosquito virome, including the recent discovery of viruses of the families Bunyaviridae (4)(5)(6)(7)(8), Rhabdoviridae (6,(9)(10)(11), Orthomyxoviridae (6,12), Flaviviridae (13)(14)(15), Mesoniviridae (16), and Reoviridae (8,17) as well as of the unclassified Chuvirus (6) and Negevirus (18) groups.…”

“…It has been suggested that most of these newly discovered viruses share features that distinguish them from "classic" human pathogens, including (i) the inability to infect vertebrates or vertebrate cell lines, (ii) high prevalence, (iii) prolonged host infection, and (iv) vertical transmission (1,2,23). Based on these features, these mosquito viruses have been referred to as "commensal" microbes (3). In reality, however, little is known about their natural infection status (e.g., abundance and frequency of superinfection), host specificity in relation to different mosquito species, geographic distribution and movement, and interactions with hosts and other microbes that may be present within a specific host.…”

Meta-transcriptomics and the evolutionary biology of RNA viruses

“…For example, considerable effort has been directed toward isolating and culturing mosquito viruses that are relevant to humans, such as flaviviruses, alphaviruses and orthobunyaviruses. In reality, however, these disease agents represent a tiny fraction of the mosquito virome (Hall et al, 2017;Junglen and Drosten, 2013;Vasilakis and Tesh, 2015), which in fact comprises representatives from every major virus group, that are more prevalent in the mosquito population, have much higher abundance, and are often transmitted vertically (Cook et al, 2013;Vasilakis and Tesh, 2015;Shi et al, 2017).…”

Firefly genomes illuminate parallel origins of bioluminescence in beetles

“…The correlation of high prevalence, prolonged host infection, and vertical transmission observed in several new mosquito viruses has resulted in their classification as "commensal" microbes. A shared evolutionary history of viruses and host, based in strategies of immune evasion of the viruses and counter antiviral strategies of the host could occasionally result in a modulation of viral loads and a chronic but latent state of virus infection (276).…”