Abstract

The production of reactive oxygen species (ROS) is a normal consequence of the aerobic cell metabolism. Despite their high and potentially detrimental reactivity with various biomolecules, the endogenous production of ROS is a vital part of physiological, immunological, and molecular processes that contribute to fitness. The role of ROS in host–parasite interactions is frequently defined by their contribution to innate immunity as effectors, promoting parasite death during infections. In vertebrates, ROS and antioxidant system enzymes, such as superoxide dismutase (SOD) are also involved in acquired immune memory, where they are responsible for T-cell signalling, activation, proliferation, and viability. Based on recent findings, ROS are now also assumed to play a role in immune priming, i.e., a form of memory in invertebrates. In this study, the potential involvement of Cu,Zn SODs in immunity of the red flour beetle Tribolium castaneum is described for the first time, applying an approach that combines an in silico gene characterisation with an in vivo immune priming experiment using the Gram-positive entomopathogen Bacillus thuringiensis. We identified an unusually high number of three different transcripts for extracellular SOD and found that priming leads to a fine-tuned modulation of SOD expression, highlighting the potential of physiological co-adaptations for immune phenotypes.

Highlights

  • Reactive oxygen species (ROS) are oxygen derivatives commonly produced in eukaryotic cells as a consequence of the aerobic metabolism

  • The combination of in silico and mRNA expression data demonstrates the presence of one gene coding for IC-superoxide dismutase (SOD) and two genes coding for EC-SOD

  • The two separated genomic regions containing tc-sodb and tc-sodc, might have resulted from a gene duplication event, that might have contributed to the functional specialisation of these two isoforms in T. castaneum, as previously demonstrated in unicellular eukaryotes for IC-SOD and others genes belonging to the antioxidant system [12, 52]

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Summary

Introduction

Reactive oxygen species (ROS) are oxygen derivatives commonly produced in eukaryotic cells as a consequence of the aerobic metabolism. The components of the antioxidant system can be classified in enzymatic molecules [e.g., superoxide dismutase (SOD), catalase, glutathione (GSH) peroxidases, peroxiredoxins, and methionine sulphoxide reductase] and non-enzymatic ones (e.g., GSH, vitamin C, vitamin E, phytochelatins, and metallothioneins) [1, 7, 10,11,12,13]. These molecular components of the cell have been conserved throughout deep evolutionary time in all eukaryotic organisms, from yeast to vertebrates [14,15,16,17]

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