The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster

Abstract

Wolbachia are vertically transmitted, obligatory intracellular bacteria that infect a great number of species of arthropods and nematodes. In insects, they are mainly known for disrupting the reproductive biology of their hosts in order to increase their transmission through the female germline. In Drosophila melanogaster, however, a strong and consistent effect of Wolbachia infection has not been found. Here we report that a bacterial infection renders D. melanogaster more resistant to Drosophila C virus, reducing the load of viruses in infected flies. We identify these resistance-inducing bacteria as Wolbachia. Furthermore, we show that Wolbachia also increases resistance of Drosophila to two other RNA virus infections (Nora virus and Flock House virus) but not to a DNA virus infection (Insect Iridescent Virus 6). These results identify a new major factor regulating D. melanogaster resistance to infection by RNA viruses and contribute to the idea that the response of a host to a particular pathogen also depends on its interactions with other microorganisms. This is also, to our knowledge, the first report of a strong beneficial effect of Wolbachia infection in D. melanogaster. The induced resistance to natural viral pathogens may explain Wolbachia prevalence in natural populations and represents a novel Wolbachia–host interaction.

Disease tolerance and immunity in host protection against infection

“…A potential bias of this approach is that changes in pathogen behavior, such as reflected by variations in tissue tropism and accumulation are not account for. An alternative approach is to quantify pathogen load in "whole body", as performed routinely in flies 5,9,10,127 . This is more challenging in other species, including rodents, but can be achieved, for example, using transgenic pathogens expressing reporter probes quantified throughout the course of an infection by whole body imaging 29 .…”

“…This notion has been challenged over the past years by the (re)discovery of disease tolerance 5,6 . This evolutionarily conserved host defense strategy, which was first described in plants 7,8 , is fully operational in flies 9,10 and mammals, including rodents 11,12 and humans 13 , where it preserves host homeostasis in response to viral 14,15 , bacterial [15][16][17][18] , fungal 19 and protozoan 11,13,20,21 infections. In contrast to resistance to infection, disease tolerance does not exert a direct negative effect on these pathogens 6 .…”

Tissue damage control in disease tolerance

“…Contemporary with these studies is the finding that a symbiont of flies, i.e. the intracellular bacteria Wolbachia, regulates not only host resistance but also disease tolerance to viral infections 92 . In addition to demonstrating that disease tolerance is operational in flies, these studies revealed that host interaction with a given microbe can regulate disease tolerance and as such the pathologic impact of infection by other pathogens 92 .…”

“…the intracellular bacteria Wolbachia, regulates not only host resistance but also disease tolerance to viral infections 92 . In addition to demonstrating that disease tolerance is operational in flies, these studies revealed that host interaction with a given microbe can regulate disease tolerance and as such the pathologic impact of infection by other pathogens 92 . Again contemporary to these studies, is the finding that disease tolerance also occurs in animals, including worms 59 as well as mice 86,93 .…”

Endosymbionts and honey bee colony losses?

“…via providing protection against viruses or fungi [6]. For example, Wolbachia can protect the host against several vectored RNA viruses [9] and can be regarded as part of host immunity [6]. However, endosymbionts such as Spiroplasma and Hamiltonella can also be beneficial for their host's vectorial capacity, e.g.…”