Arginine decarboxylase activity in the cattle tick Rhipicephalus microplus suggests an alternative polyamine biosynthetic pathway

Abstract

The cattle tick Rhipicephalus microplus may rely on an alternative polyamine biosynthesis pathway mediated by arginine decarboxylase activity. This hematophagous ectoparasite is a major constraint to livestock production in tropical and subtropical regions, and its control is increasingly compromised by the rapid emergence of acaricide resistance, highlighting the need for new molecular targets. Previous RNA-seq analyses of ovaries, whole males, and female carcasses identified two sex-enriched transcripts, odc1 and odc2, initially annotated as ornithine decarboxylases (ODCs), enzymes that catalyze the rate-limiting step in polyamine biosynthesis. Polyamines are essential for nucleic acid stabilization, cell growth, stress responses, and gametogenesis. Here, we validated using qPCR that expression of both genes is sexually dimorphic. Phylogenetic analysis across Animalia revealed that R. microplus Odc1 and Odc2 form two divergent tick-specific clades, distinct from canonical ODCs described in mammals and insects. Biochemical characterization of recombinant proteins showed that Odc2 lacked detectable activity under the conditions tested, whereas Odc1 exhibited moderate ornithine decarboxylase activity and robust arginine decarboxylase activity. These results suggests that R. microplus may produce putrescine through an alternative route involving agmatine, thereby bypassing the canonical ornithine decarboxylation pathway. To our knowledge, this represents the first biochemical evidence consistent with arginine decarboxylase activity in an animal enzyme. Together, these findings support the existence of a previously unrecognized branch of polyamine metabolism in ticks and identify Odc1 as a promising candidate target for the development of selective acaricides.