Abstract
Wolbachia is an intracellular bacterium generally described as being a facultative reproductive parasite. However, Wolbachia is necessary for oogenesis completion in the wasp Asobara tabida. This dependence has evolved recently as a result of interference with apoptosis during oogenesis. Through comparative transcriptomics between symbiotic and aposymbiotic individuals, we observed a differential expression of ferritin, which forms a complex involved in iron storage. Iron is an essential element that is in limited supply in the cell. However, it is also a highly toxic precursor of Reactive Oxygen Species (ROS). Ferritin has also been shown to play a key role in host–pathogen interactions. Measuring ferritin by quantitative RT-PCR, we confirmed that ferritin was upregulated in aposymbiotic compared to symbiotic individuals. Manipulating the iron content in the diet, we showed that iron overload markedly affected wasp development and induced apoptotic processes during oogenesis in A. tabida, suggesting that the regulation of iron homeostasis may also be related to the obligate dependence of the wasp. Finally, we demonstrated that iron metabolism is influenced by the presence of Wolbachia not only in the obligate mutualism with A. tabida, but also in facultative parasitism involving Drosophila simulans and in Aedes aegypti cells. In these latter cases, the expression of Wolbachia bacterioferritin was also increased in the presence of iron, showing that Wolbachia responds to the concentration of iron. Our results indicate that Wolbachia may generally interfere with iron metabolism. The high affinity of Wolbachia for iron might be due to physiological requirement of the bacterium, but it could also be what allows the symbiont to persist in the organism by reducing the labile iron concentration, thus protecting the cell from oxidative stress and apoptosis. These findings also reinforce the idea that pathogenic, parasitic and mutualistic intracellular bacteria all use the same molecular mechanisms to survive and replicate within host cells. By impacting the general physiology of the host, the presence of a symbiont may select for host compensatory mechanisms, which extends the possible consequences of persistent endosymbiont on the evolution of their hosts.
Highlights
Symbiotic interactions, in which long-term interactions take place between two partners belonging to different species, are common in nature [1]
When we analyzed the genetic basis of this dependence, we found that ferritin, a protein involved in the regulation of iron homeostasis, was over-expressed in uninfected individuals
Among all the potential candidates for involvement in apoptotic processes, we focused on ferritin, a protein complex involved in iron storage, and composed of HCH and LCH subunits
Summary
In which long-term interactions take place between two partners belonging to different species, are common in nature [1]. These associations form a continuum ranging from parasitism to mutualism with respect to the outcome of the association (i.e. the cost or benefit for the host), and can be either facultative or obligate for the host. Increasing reports in the literature indicate that the same molecular mechanisms are used by both parasitic and mutualistic symbionts to interact with their host [4]. Common molecular mechanisms have been identified which are related to (i) communication processes, such as symbiosis/ virulence factors that encode genes classically involved in secretion systems [6] (ii) survival and replication processes, including the expression of colonization factors [7], evading host immune systems [8], and regulating bacterial growth, and (iii) physiological processes involved in environmental adaptation, such as pH modification, induction of specific metabolic pathways, development of iron uptake strategies [9] and induction of stress proteins [10]
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