Abstract
Babesia bovis, a tick-transmitted apicomplexan protozoon, infects cattle in tropical and subtropical regions around the world. In the apicomplexans Toxoplasma gondii and Plasmodium falciparum, rhomboid serine protease 4 (ROM4) fulfills an essential role in host cell invasion. We thus investigated B. bovis ROM4 coding genes; their genomic organization; their expression in in vitro cultured asexual (AS) and sexual stages (SS); and strain polymorphisms. B. bovis contains five rom4 paralogous genes in chromosome 2, which we have named rom4.1, 4.2, 4.3, 4.4 and 4.5. There are moderate degrees of sequence identity between them, except for rom4.3 and 4.4, which are almost identical. RT-qPCR analysis showed that rom4.1 and rom4.3/4.4, respectively, display 18-fold and 218-fold significantly higher (p < 0.01) levels of transcription in SS than in AS, suggesting a role in gametogenesis-related processes. In contrast, transcription of rom4.4 and 4.5 differed non-significantly between the stages. ROM4 polymorphisms among geographic isolates were essentially restricted to the number of tandem repeats of a 29-amino acid sequence in ROM4.5. This sequence repeat is highly conserved and predicted as antigenic. B. bovis ROMs likely participate in relevant host–pathogen interactions and are possibly useful targets for the development of new control strategies against this pathogen.
Highlights
Babesia bovis is a highly pathogenic tick-transmitted apicomplexan protozoon causing bovine babesiosis, which affects the welfare and productivity of cattle in vast tropical and subtropical regions of the world [1–3].The genus Babesia belongs to the order Piroplasmida, which is characterized by a dixenous life cycle, and alternating asexual reproduction in a vertebrate and sexual and asexual reproduction in an ixodid tick host
rhomboid serine proteases (ROMs) were first discovered in Drosophila melanogaster, in which they were shown to be involved in the epidermal growth receptor signaling pathway
The molecular mechanisms and functions where ROMs are involved are diverse, ranging from cell signaling in animals to quorum sensing in bacteria, and from flower development in plants to host cell invasion in apicomplexan protozoa [11,19]
Summary
Babesia bovis is a highly pathogenic tick-transmitted apicomplexan protozoon causing bovine babesiosis, which affects the welfare and productivity of cattle in vast tropical and subtropical regions of the world [1–3].The genus Babesia belongs to the order Piroplasmida, which is characterized by a dixenous life cycle, and alternating asexual reproduction in a vertebrate and sexual and asexual reproduction in an ixodid tick host. To other related apicomplexans, B. bovis is an obligate intracellular parasite, and the processes of invasion and egress from host cells are essential for its survival [4]. In the vertebrate bovine host, B. bovis, pertaining to Babesia sensu stricto (Clade VI) [2,3], thrives and divides exclusively within erythrocytes by merogony. The resulting zygotes migrate across the gut epithelium into the hemolymph, undergo meiosis and mature into kinetes, which invade different tick tissues where they propagate by sporogony. Upon kinete invasion of the epithelial cells of the tick salivary glands, additional sporogony results in the production of a large quantity of infective sporozoites. Sporozoites are injected with tick saliva into the bovine dermis upon a blood meal, reach the capillaries, invade erythrocytes and undergo asexual merogony, closing the cycle [3,4,6]
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