Interactions of the intracellular bacterium Cardinium with its host, the house dust mite Dermatophagoides farinae, based on gene expression data

Authors: HUBERT, JAN - Crop Research Institute - Czech Republic; Scully, Erin; SOPKO, BRUNO - Crop Research Institute - Czech Republic; DOWD, SCOT - Molecular Research Lp (MR DNA); NESVOMA, MARTA - Crop Research Institute - Czech Republic; KLIMOV, PAVEL - Bangor University; ERBAN, THOMAS - Tyumen State University

Submitted to: mSystems
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/7/2021
Publication Date: 11/7/2021
Citation: Hubert, J., Scully, E.D., Sopko, B., Dowd, S.E., Nesvoma, M., Klimov, P., Erban, T. 2021. Interactions of the intracellular bacterium Cardinium with its host, the house dust mite Dermatophagoides farinae, based on gene expression data. mSystems. https://doi.org/10.1128/mSystems.00916-21.
DOI: https://doi.org/10.1128/mSystems.00916-21

Interpretive Summary: The house dust mite is a major source of indoor allergens for humans worldwide. Many populations of house dust mites harbor bacterial symbionts, that can have major influences on mite physiology and allergen production. The impacts of bacteria in the genus Cardinium on host dust mites are unknown. The expression of house dust mite and bacterial genes was evaluated and significant interactions that could be important for house dust mite biology were found. The bacteria Cardinium is capable of synthesizing essential nutrients, such as lipoic acid, which are important for survival of house dust mites and are lacking in their diet. Interactions between Cardinium with mite genes from pathways involved in the synthesis of pheromones were observed. Pheromone synthesis greatly influences mating and reproductive behaviors of mites, suggesting that Cardinium could influence reproduction in mites to facilitate its transmission to offspring. Correlations were observed between Cardinium and mite genes associated with energy production, suggesting that glucose and other sugars synthesized by the mite could be transferred to Cardinium. These results suggest that the interactions between house dust mites and Cardinium are mutually beneficial and potentially important for survival of house dust mites. This suggests that antibiotic treatments that reduce the abundance of this bacterium may be useful in controlling house dust mite populations.

Technical Abstract: The mite Dermatophagoides farinae is a medically important house dust mite species that is a major source of indoor allergens worldwide. European and North American populations of this mite species are inhabited by an intracellular bacterium belonging to Cardinium group A. This bacterium naturally occurs at very high abundances (up to 104 cells per mite), strongly suggesting that it is biologically significant for its mite host. However, the impacts of this symbiotic bacterium on mite biological processes and physiology are unknown. Using correlations between host and symbiont gene expression profiles, we identified several important molecular pathways that potentially regulate or facilitate interactions between the mite host and its endosymbiotic bacterium. Host-associated pathways for phagocytosis, apoptosis, the MAPK signaling cascade, endocytosis, the TNF pathway, the TGF-beta pathway, lysozyme, and the Toll/Imd pathway as the expression of Cardinium genes collectively explained 95% of the variation in the expression of mite genes assigned to these pathways. In addition, expression of mite genes explained 76% of the variability in Cardinium gene expression. In particular, the expression of the Cardinium genes encoding the signaling molecules bamD, lepA, symE, and virD4 was either positively or negatively correlated with the expression levels of mite genes involved in endocytosis, phagocytosis and apoptosis. We also found that Cardinium possesses a complete biosynthetic pathway for lipoic acid and may provide lipoate, but not biotin, to mites. Cardinium gene expression collectively explained 84% of the variation in expression related to several core mite metabolic pathways and, most notably, a negative correlation was observed between bacterial gene expression and expression of mite genes assigned to the glycolysis and the citric acid cycle pathways. Furthermore, we showed that Cardinium gene expression is correlated with expression levels of genes associated with terpenoid backbone biosynthesis. This pathway is important for the synthesis of pheromones, thus providing an opportunity for Cardinium to influence mite reproductive behavior to facilitate transmission of the bacterium. Overall, our study provided correlational gene expression data that can be useful for future research on mite–Cardinium interactions.