Parasites, proteomics and performance: Effects of gregarine gut parasites on dragonfly flight muscle composition and function

In previous work, we found that dragonflies infected with gregarine gut parasites have reduced muscle power output, loss of lipid oxidation in their flight muscles, and a suite of symptoms similar to mammalian metabolic syndrome. Here, we test the hypothesis that changes in muscle protein composition underlie the observed changes in contractile performance. We found that gregarine infection was associated with a 10-fold average reduction in abundance of a ∼155 kDa fragment of muscle myosin heavy chain (MHC; ∼206 kDa intact size). Insect MHC gene sequences contain evolutionarily conserved amino acid motifs predicted for calpain cleavage, and we found that calpain digestion of purified dragonfly MHC produced a peptide of ∼155 kDa. Thus, gut parasites in dragonflies are associated with what appears to be a reduction in proteolytic degradation of MHC. MHC155 abundance showed a strong negative relationship to muscle power output in healthy dragonflies but either no relationship or a weakly positive relationship in infected dragonflies. Troponin T (TnT) protein isoform profiles were not significantly different between healthy and infected dragonflies but whereas TnT isoform profile was correlated with power output in healthy dragonflies, there was no such correlation in infected dragonflies. Multivariate analyses of power output based on MHC155 abundance and a principal component of TnT protein isoform abundances explained 98% of the variation in muscle power output in healthy dragonflies but only 29% when data from healthy and infected dragonflies were pooled. These results indicate that important, yet largely unexplored, functional relationships exist between (pathways regulating) myofibrillar protein expression and (post-translational) protein processing. Moreover, infection by protozoan parasites of the midgut is associated with changes in muscle protein composition (i.e. across body compartments) that, either alone or in combination with other unmeasured changes, alter muscle contractile performance.