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

Originality-Significance StatementThis contribution provides a window into the study of a densovirus called CpDV infecting Culex pipiens mosquitoes. The originality of the study lies in the fact that CpDV, a DNA virus, was to date almost unstudied, its interaction with its hosts and its transmission mode were unknown. Considering that all Cx. pipiens are infected with Wolbachia, we studied the influence of this bacterial endosymbiont on CpDV density and transmission. Although Wolbachia-RNA virus interactions, especially in non-native Wolbachia-host associations have been widely studied, Wolbachia-DNA virus interactions were rarely investigated.\n\nIn this natural tripartite Cx. pipiens-Wolbachia-CpDV system: O_LIWe revealed the wide prevalence of CpDV, mostly at low densities, in Cx. pipiens laboratory lines.\nC_LIO_LIWe monitored CpDV presence in several cell types in ovaries including the oocytes where they co-exist with the bacterial endosymbiont Wolbachia.\nC_LIO_LIWe demonstrated that CpDV density in ovaries was influenced by Wolbachia presence and strain variations\nC_LIO_LIWe studied CpDV vertical transmission depending on Wolbachia presence and strain variations\nC_LI\n\nWe report for the first time the occurrence of widely distributed covert CpDV infections in Cx. pipiens laboratory colonies. CpDV is maintained by both vertical and horizontal transmission and under the influence of the vertically transmitted bacterial endosymbiont Wolbachia. Taken together our results suggest that CpDV could be very prevalent in nature putatively influencing natural Cx. pipiens populations dynamics.\n\nSUMMARYCulex 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 hosts 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 quantity significantly differed between mosquito lines harboring 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 also significantly affected 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.