Cysteine cathepsins from C1 papain family are ubiquitous peptidases involved in lysosomal protein degradation as well as in specific physiological functions in many normal and pathological processes. One of specific functions of cysteine cathepsins was found in insects, where in selected taxonomic groups they act as major digestive enzymes. The emergence of new functions of the enzymes has led to variations in gene structure and accordingly the formation of new types of peptidases. We analyzed and compared C1 peptidases in 12 insect genomes from six orders, including those newly sequenced under the auspices of the i5k Project, and those deposited in GenBank. Different insect species contained from five cathepsins in parasitic Hymenoptera Orussus abietinus to 51 in the phytophagous beetle Leptinotarsa decemlineata. Based on phylogeny, we identified eight conserved groups of peptidase orthologs, and several species-specific non-conserved groups of peptidase genes. Conserved gene groups were represented by an ortholog in almost every species, and included cathepsins B, F, L, O, three new peptidase species similar but distinct from cathepsin L (cathepsins I, Ll and La). In species other than wasps, we find cathepsin B-like peptidase homologs with a substituted Cys/Ser in the active center, similar to TINAGL proteins. Species-specific groups of peptidase genes were found as sequential clusters of gene expansions in coleopterans L. decemlineata, Tribolium castaneum, Tenebrio molitor, a cockroach Blattella germanica, and a dipluran Catajapyx aquilonaris. These gene expansion groups contained cathepsin B-like and cathepsin L-like peptidase genes. The evolution of non-conserved peptidase groups presumably occurred by duplication of one or few peptidase genes independently in different organisms.
The work was supported by Russian Foundation for Basic Report (grants #14-04-91167-NSFC_а and #15-04-08689_a).