Abstract
Mosquitoes transmit a diverse group of human flaviviruses including West Nile, dengue, yellow fever, and Zika viruses. Mosquitoes are also naturally infected with insect‐specific flaviviruses (ISFs), a subgroup of the family not capable of infecting vertebrates. Although ISFs are not medically important, they are capable of altering the mosquito's susceptibility to flaviviruses and may alter host fitness. Wolbachia is an endosymbiotic bacterium of insects that when present in mosquitoes limits the replication of co‐infecting pathogens, including flaviviruses. Artificially created Wolbachia‐infected Aedes aegypti mosquitoes are being released into the wild in a series of trials around the globe with the hope of interrupting dengue and Zika virus transmission from mosquitoes to humans. Our work investigated the effect of Wolbachia on ISF infection in wild‐caught Ae. aegypti mosquitoes from field release zones. All field mosquitoes were screened for the presence of ISFs using general degenerate flavivirus primers and their PCR amplicons sequenced. ISFs were found to be common and widely distributed in Ae. aegypti populations. Field mosquitoes consistently had higher ISF infection rates and viral loads compared to laboratory colony material indicating that environmental conditions may modulate ISF infection in Ae. aegypti. Surprisingly, higher ISF infection rates and loads were found in Wolbachia‐infected mosquitoes compared to the Wolbachia‐free mosquitoes. Our findings demonstrate that the symbiont is capable of manipulating the mosquito virome and that Wolbachia‐mediated viral inhibition is not universal for flaviviruses. This may have implications for the Wolbachia‐based DENV control strategy if ISFs confer fitness effects or alter mosquito susceptibility to other flaviviruses.
Highlights
Mosquitoes transmit a wide range of pathogens including viruses deemed arboviruses that cause widespread morbidity and mortality in humans and animals (Mackenzie, Gubler, & Petersen, 2004; Mackenzie et al, 1994)
Flaviviruses include Japanese encephalitis virus and Murray Valley encephalitis virus transmitted by Culex species (Erlanger, Weiss, Keiser, Utzinger, & Wiedenmayer, 2009; Kay, Fanning, & Carley, 1984), West Nile virus (WNV) transmitted by a diverse group of mosquitoes including Aedes and Culex species (Mackenzie et al, 2004) and yellow fever virus (YFV), Zika virus (ZIKV), and dengue virus (DENV) that are all transmitted by Aedes aegypti and Aedes albopictus (Black et al, 2002; Hall-Mendelin et al, 2016; Hayes, 2009)
Our findings suggest that insect-specific flaviviruses (ISFs) are a common feature of the mosquito virome and that Wolbachia may be enhancing the frequency of infection in the field
Summary
Mosquitoes transmit a wide range of pathogens including viruses deemed arboviruses that cause widespread morbidity and mortality in humans and animals (Mackenzie, Gubler, & Petersen, 2004; Mackenzie et al, 1994). Some studies have shown that ISFs suppress flaviviruses, including WNV by CxFV and Murray Valley virus by Palm creek virus (Bolling, Olea-P opelka, Eisen, Moore, & Blair, 2012; Hobson-P eters et al, 2013) This effect, known as superinfection exclusion (Billecocq, Vazeille-Falcoz, Rodhain, & Bouloy, 2000; Geib et al, 2003; Karpf, Lenches, Strauss, Strauss, & Brown, 1997; McAlister & Barrett, 1977; Nethe, Berkhout, & van der Kuyl, 2005; Pesko & Mores, 2009), was not observed in field mosquito populations where a positive association was found between WNV and CxFV. These findings may have implications for Wolbachia-DENV control if ISFs affect host fitness or play a role in mosquito susceptibility to flaviviruses
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