Sharing cells with Wolbachia: the transovarian vertical transmission of Culex pipiens densovirus

Abstract

Summary Culex pipiens densovirus (CpDV), a single stranded DNA virus, has been isolated from Culex pipiens mosquitoes but differs from other mosquito densoviruses in terms of genome structure and sequence identity. Its transmission from host to host, the nature of its interactions with both its host and host's endosymbiotic bacteria Wolbachia are not known. Here, we report the presence of CpDV in the ovaries and eggs of Cx. pipiens mosquitoes in close encounters with Wolbachia. In the ovaries, CpDV amount significantly differed between mosquito lines harbouring different strains of Wolbachia and these differences were not linked to variations in Wolbachia densities. CpDV was vertically transmitted in all laboratory lines to 17%–20% of the offspring. For some females, however, the vertical transmission reached 90%. Antibiotic treatment that cured the host from Wolbachia significantly decreased both CpDV quantity and vertical transmission suggesting an impact of host microbiota, including Wolbachia, on CpDV transmission. Overall our results show that CpDV is transmitted vertically via transovarian path along with Wolbachia with which it shares the same cells. Our results are primordial to understand the dynamics of densovirus infection, their persistence and spread in populations considering their potential use in the regulation of mosquito vector populations.

Use of Microbiota to Fight Mosquito-Borne Disease

“…First, many commensal bacteria may not always stop pathogen development in the mosquito. For example, Serratia inhibits malaria parasite infection of mosquitoes (Gonzalez-Ceron et al, 2003;Bando et al, 2013;Wang et al, 2017), while it promotes dengue virus infection of a culicine mosquito (Wu et al, 2019); A Wolbachia species reduces arbovirus infection of A. aegypti mosquitoes (Moreira et al, 2009;van den Hurk et al, 2012;Dutra et al, 2016) whereas another species enhances vertical densovirus transmission by Culex pipiens (Altinli et al, 2018;King et al, 2018). These apparently contradictory observations will only be clarified when the mechanisms underlying the observed effects are understood.…”

“…Infection by the wMel strain of Wolbachia also can significantly reduce CHIKV and Yellow Fever virus (YFV) infection and dissemination rate (van den Hurk et al, 2012). However, a Wolbachia strain was reported to enhance vertical densovirus transmission by Culex pipiens (Altinli et al, 2018;King et al, 2018).…”

Variation in the susceptibility of urban Aedes mosquitoes infected with a densovirus

“…Adult mortality has not been evaluated in this work, but many studies have shown that DVs infection of mosquito larvae affects the life traits of infected adults 33 , 34 , 37 . Thus, the effects of sublethal infection of Ae.…”

“…pipiens and Culiseta annulata 19 . MDVs are thought to persist in nature by horizontal transmission from larvae to larvae in the wild aquatic environments, although transovarial and sexual transmission have also been recorded 3 , 20 , 27 , 33 – 37 . They are highly pathogenic for larvae at all stages, but mortality is higher when infection occurs at an early stage.…”

Spotlight on how microbes influence their host's behavior

“…Although usually applied to animals rather than plants or microbes, this definition of ‘behavior’ encompasses all types of organisms and their populations. Indeed, besides articles on animal hosts (Koehler et al ., ; Murfin et al ., ; Truitt et al ., ; Altinli et al ., ; Rothman et al ., ; Zhao et al ., ), this special issue contains a number of research papers devoted to understanding how plants respond to their microbial inhabitants. Among these studies on plant–symbiont interactions, several focus on plant responses to nitrogen‐fixing bacteria (Lamouche et al ., ; Baena et al ., ; Bañuelos‐Vazquez et al ., ; Pujic et al ., ; Songwattana et al ., ), while others investigate endophytes and their role in alleviating plant abiotic stress (Vigani et al ., ; Lanza et al ., ; Llorens et al ., ).…”