A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium

Abstract

Wolbachia are maternally inherited intracellular bacterial symbionts that are estimated to infect more than 60% of all insect species. While Wolbachia is commonly found in many mosquitoes it is absent from the species that are considered to be of major importance for the transmission of human pathogens. The successful introduction of a life-shortening strain of Wolbachia into the dengue vector Aedes aegypti that halves adult lifespan has recently been reported. Here we show that this same Wolbachia infection also directly inhibits the ability of a range of pathogens to infect this mosquito species. The effect is Wolbachia strain specific and relates to Wolbachia priming of the mosquito innate immune system and potentially competition for limiting cellular resources required for pathogen replication. We suggest that this Wolbachia-mediated pathogen interference may work synergistically with the life-shortening strategy proposed previously to provide a powerful approach for the control of insect transmitted diseases.

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

“…In the past decade, studies have shown that certain microbes associated with insect vectors could be used to mediate the transmission of diseases including those transmitted by mosquitoes (Capone et al., 2013; Cirimotich et al., 2011; Dong, Manfredini, & Dimopoulos, 2009; Mourya, Pidiyar, Patole, Gokhale, & Shouche, 2002; Ramirez et al., 2014; Tchioffo et al., 2013; Xi, Ramirez, & Dimopoulos, 2008), tsetse flies (Pais, Lohs, Wu, Wang, & Aksoy, 2008; Wang, Wu, Yang, & Aksoy, 2009; Weiss, Wang, Maltz, Wu, & Aksoy, 2013), sand flies (Sant'Anna et al., 2014), and ticks (Gall et al., 2016; Narasimhan et al., 2014). The most striking example is the inhibition by bacterium Wolbachia pipientis of virus and parasite infection in mosquito vectors (Bian, Xu, Lu, Xie, & Xi, 2010; Blagrove, Arias‐Goeta, Di Genua, Failloux, & Sinkins, 2013; Frentiu et al., 2014; van den Hurk et al., 2012; Hussain et al., 2012; Moreira et al., 2009). Unfortunately, while studies on the application of microbes such as Wolbachia to control human disease have advanced, we still lack basic insight into the natural microbial communities associated with vectors, from viruses to bacteria to single‐celled eukaryotes.…”

Wolbachia enhances insect‐specific flavivirus infection in Aedes aegypti mosquitoes

“…These findings were unexpected given that Wolbachia has been extensively shown to inhibit flaviviruses of medical importance in Ae. aegypti (Bian et al., 2010; van den Hurk et al., 2012; Moreira et al., 2009; Walker et al., 2011). …”

“…aegypti populations. This sharply contrasts previous studies where Wolbachia infection significantly reduced the proportion of individuals infected with other flaviviruses such as DENV (Amuzu & McGraw, 2016; Amuzu, Simmons, & McGraw, 2015; Bian et al., 2013; Frentiu et al., 2014; Moreira et al., 2009; Walker et al., 2011), Zika (Aliota et al., 2016; Dutra et al., 2016), and YFV (van den Hurk et al., 2012). Our findings are, however, supported by studies performed in Cx.…”

“…albopictus (Xi, Dean, Khoo, & Dobson, 2005), and w Mel w AlbB (Joubert et al., 2016) that is a superinfection of w Mel and w AlbB. Wolbachia ‐mediated pathogen blocking has now been observed for arboviruses such as WNV (Glaser & Meola, 2010), YFV (van den Hurk et al., 2012), DENV (Bian et al., 2010; Frentiu, Robinson, Young, McGraw, & O'Neill, 2010; Moreira et al., 2009; Walker et al., 2011), ZIKV (Aliota, Peinado, Velez, & Osorio, 2016; Dutra et al., 2016), and Chikungunya virus (van den Hurk et al., 2012; Moreira et al., 2009). Wolbachia is currently being released into populations of Ae.…”

“…Wolbachia infections in Ae. aegypti differ significantly from those found in D. melanogaster however, exhibiting higher symbiont loads (McGraw, Merritt, Droller, & O'Neill, 2002; McMeniman et al., 2009; Moreira et al., 2009; Walker et al., 2011), broader tissue distributions (Moreira et al., 2009; Walker et al., 2011), greater activation of the immune response (McGraw et al., 2002; McMeniman et al., 2009; Moreira et al., 2009; Walker et al., 2011), and greater fitness costs (McMeniman, Hughes, & O'Neill, 2011; Min & Benzer, 1997). These discrepancies may result from different periods of association/evolutionary history, long (~5,000 years) in the case of D. melanogaster (Richardson et al., 2012) and short (<10 years) in the case of the newly infected Ae.…”