High Virulence of Wolbachia after Host Switching: When Autophagy Hurts

Abstract

Wolbachia are widespread endosymbionts found in a large variety of arthropods. While these bacteria are generally transmitted vertically and exhibit weak virulence in their native hosts, a growing number of studies suggests that horizontal transfers of Wolbachia to new host species also occur frequently in nature. In transfer situations, virulence variations can be predicted since hosts and symbionts are not adapted to each other. Here, we describe a situation where a Wolbachia strain (wVulC) becomes a pathogen when transfected from its native terrestrial isopod host species (Armadillidium vulgare) to another species (Porcellio d. dilatatus). Such transfer of wVulC kills all recipient animals within 75 days. Before death, animals suffer symptoms such as growth slowdown and nervous system disorders. Neither those symptoms nor mortalities were observed after injection of wVulC into its native host A. vulgare. Analyses of wVulC's densities in main organs including Central Nervous System (CNS) of both naturally infected A. vulgare and transfected P. d. dilatatus and A. vulgare individuals revealed a similar pattern of host colonization suggesting an overall similar resistance of both host species towards this bacterium. However, for only P. d. dilatatus, we observed drastic accumulations of autophagic vesicles and vacuoles in the nerve cells and adipocytes of the CNS from individuals infected by wVulC. The symptoms and mortalities could therefore be explained by this huge autophagic response against wVulC in P. d. dilatatus cells that is not triggered in A. vulgare. Our results show that Wolbachia (wVulC) can lead to a pathogenic interaction when transferred horizontally into species that are phylogenetically close to their native hosts. This change in virulence likely results from the autophagic response of the host, strongly altering its tolerance to the symbiont and turning it into a deadly pathogen.

Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells

“…There is evidence that multiple host mechanisms may be involved in inhibiting viral replication including synthesis of reactive oxygen and cholesterol and induction of host autophagy (Le Clec'h et al 2012;Pan et al 2012;Caragata et al 2013;Wong et al 2015). Our finding that Wolbachia dramatically alters host ER morphology and relies on the ERAD pathway to maintain titer suggests the involvement of a previously unsuspected mechanism in preventing the replication of positive-strand RNA viruses.…”

Wolbachia-Associated Bacterial Protection in the Mosquito Aedes aegypti

“…This constitutive aspect of immunity, defined early in development will continue to have real effects on the performance of phagocytosis in the adult [63]. Also, the recent transinfection of Wolbachia into new insect hosts has been associated with increases in autophagy [64] and the generation of reactive oxygen species [65], both of which may not be captured in transcriptional measures.…”

Symbiotic Bacteria Influence the Odor and Mating Preference of Their Hosts

“…This protocol was applied to inject three separate batches of individuals. Previous studies revealed that wVulC injections in A. vulgare females had no effect on different life history traits (Le Clec'h et al, 2012). The animals were then used for behavioral assays 6 months post-injection, leaving enough time for Wolbachia to spread and be incorporated into the host tissue, as is the case in naturally infected individuals (Juchault and Mocquard, 1989).…”

“…In general, Wolbachia are weakly virulent to their native hosts (Engelstädter and Hurst, 2009), probably as a result of the host/parasite coevolution of the vertical transmission process (Lipsitch et al, 1996;Engelstädter and Hurst, 2009), although the symbiotic bacteria may become pathogenic when bacterial levels get too high (Sachs and Simms, 2006;Le Clec'h et al, 2012). However, although Wolbachia affects the mating choice through CI of its host in some Drosophila (Moreau et al, 2001;Markov et al, 2009;Sharon et al, 2010), this is not always true for all Drosophila species (Jenkins et al, 1996;Sullivan and Jaenike, 2006).…”