Wolbachia and the insect immune system: what reactive oxygen species can tell us about the mechanisms of Wolbachia–host interactions

Abstract

Wolbachia are intracellular bacteria that infect a vast range of arthropod species, making them one of the most prevalent endosymbionts in the world. Wolbachia’s stunning evolutionary success is mostly due to their reproductive parasitism but also to mutualistic effects such as increased host fecundity or protection against pathogens. However, the mechanisms underlying Wolbachia phenotypes, both parasitic and mutualistic, are only poorly understood. Moreover, it is unclear how the insect immune system is involved in these phenotypes and why it is not more successful in eliminating the bacteria. Here we argue that reactive oxygen species (ROS) are likely to be key in elucidating these issues. ROS are essential players in the insect immune system, and Wolbachia infection can affect ROS levels in the host. Based on recent findings, we elaborate a hypothesis that considers the different effects of Wolbachia on the oxidative environment in novel vs. native hosts. We propose that newly introduced Wolbachia trigger an immune response and cause oxidative stress, whereas in coevolved symbioses, infection is not associated with oxidative stress, but rather with restored redox homeostasis. Redox homeostasis can be restored in different ways, depending on whether Wolbachia or the host is in charge. This hypothesis offers a mechanistic explanation for several of the observed Wolbachia phenotypes.

Infections with the Sexually Transmitted Pathogen Nosema apis Trigger an Immune Response in the Seminal Fluid of Honey Bees (Apis mellifera)

“…Many of these proteins have previously been reported as molecular components of a humoral immune response in insects. Furthermore, they have been detected to be secreted into other fluids such as venom 86,89,90 .…”

“…gene expression is activated by two distinct signalling pathways, the Toll pathway and the IMD pathway (Figure 2).Humoral immune responses are also controlled by proteins involved in reaction to oxidative stress (ROS) defence 57 , because ROS are produced in the midgut cells and act at sites of infections to directly kill pathogens or as signals of cellular stress to activate humoral immune responses such as encapsulation and melanisation86,89,90,104,105 . We detected abundance changes in a number of…”

Diversity of bacteriome associated with Phlebotomus chinensis (Diptera: Psychodidae) sand flies in two wild populations from China

“…chinensis sand flies. Endosymbionts have complex interactions with their hosts, such as parthenogenesis, male killing, cytoplasm incompatibility, and host defence4150515253. Although most of Rickettsiella spp.…”

Impact of ERK activation on fly survival and Wolbachia-mediated protection during virus infection

“…Both ROS and antimicrobial peptides (AMPs) are important immune effectors in insect gut epithelia [reviewed in Zug & Hammerstein, (2015)]. In Drosophila, elevated ROS levels are associated with delayed virusinduced mortality following systemic viral infection (Wong et al, 2015).…”

“…It is therefore unlikely that induction of ROS upon Wolbachia infection correlates with Toll pathway activation in Drosophila. Although the mechanistic involvement of ROS in the insect antiviral response remains to be elucidated, and a recent study has reported that Wolbachia do not induce ROS in Aedes albopictus (Molloy & Sinkins, 2015), ROSrelated responses may constitute a promising area for future research in understanding Wolbachia-mediated antiviral effects (Zug & Hammerstein, 2015).…”