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

Abstract

SUMMARY 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.

Intestinal probiotics restore the ecological fitness decline of Bactrocera dorsalis by irradiation

“…For instance, in D. melanogaster , Lactobacillus plantarum is responsible for mating preference and the composition of the gut microbiota determines mating attractiveness: flies mated preferentially with individuals harbouring similar microbiota, and this preference was probably linked to microbiota‐dependent variation in the cuticle hydrocarbon profile (Sharon et al., ). Similarly, in Libellula pulchella , protozoan parasite infections that affect gut function can alter flight muscle development and decrease flight performance (Schilder & Marden, ). A study of C. capitata showed that feeding gut commensal Enterobacteriaceae bacteria extended host longevity (Behar et al., ).…”

A Novel, In-solution Separation of Endogenous Cardiac Sarcomeric Proteins and Identification of Distinct Charged Variants of Regulatory Light Chain

“…Muscle MHC exists as a heterogenous population (12) expressed as two unique isoforms, ␣ and ␤ (26), with post-translational modifications (27)(28)(29)(30)(31). MHC generates 150 tryptic peptides when unmodified and fully cleaved; therefore the endogenous number of MHC charge variants induced by isoforms and PTMs may be greater than 10 4 .…”

Influence of ageing and essential amino acids on quantitative patterns of troponin T alternative splicing in human skeletal muscle

“…The pre-mRNAs for all three genes are alternatively spliced, leading to the production of mRNAs encoding multiple protein variants that exhibit differential functional characteristics. Consequently, changes in the pattern of troponin T pre-mRNA alternative splicing results in variations in muscle force, power output, and calcium sensitivity in both insects (Fitzhugh et al 1997; Marden et al 2001; Schilder et al 2007) and mammals (Pan et al 1992; Briggs et al 1996; Chaudhuri et al 2005; Sancisi et al 2014). Although little is known about mechanisms involved in regulating alternative splicing of the troponin T pre-mRNA in general, the pattern of rodent Tnnt3 splice variant expression is rapidly altered in young rats in response to changes in effective body mass, e.g.…”