Anaplasma marginale multistrain infection in bovines under natural conditions correlates with transovarial transmission and vector competence in Rhipicephalus microplus ticks

Abstract

Background Anaplasma marginale, a gram-negative obligate intracellular microorganism, infects erythrocytes of ruminants and other host species from tropical and subtropical world regions. This pathogen of importance for cattle production, is known to be transmitted mechanically and through hematophagous parasites, mainly by Rhipicephalus microplus ticks. Even though transovarial transmission of A. marginale has been previously reported in R. microplus ticks, there is no evidence of A. marginale transmission from the resulting unfed larvae to a susceptible host. The aim of the present study was to evaluate the transovarial transmission of A. marginale in the R. microplus tick under natural conditions and to study the vector competence of the infected hatched larvae. Methods Engorged female R. microplus ticks were sampled from A. marginale positive bovines from an enzootic area in Argentina, and larvae were obtained from a subgroup of these females. After identifying A. marginale in the females and their larvae, selected ticks collected from a single bovine were used. After spawn, hatched larvae were seeded on a susceptible healthy bovine and another subgroup of engorged R. microplus ticks were subjected to dissection to recover the salivary glands and ovaries for A. marginale identification. Anaplasma marginale was detected by PCR and molecularly characterized by means of cloning and sequence all msp1α fragments while genotyping. Results A. marginale was detected in naturally infected bovines, in different organs of engorged R. microplus females that were parasitizing them, and in the larvae obtained from these females. A. marginale infection of the susceptible bovine was corroborated both from DNA detection and from compatible structures in a blood smear. The characterization of A. marginale msp1α genotypes involved throughout the infection process provided relevant information about the dynamics of the transmission process. Conclusions The results demonstrate the transovarial transmission of A. marginale in R. microplus ticks under natural conditions and, through an experimental infection assay, the vector competence of the infected R. microplus larvae to transmit A. marginale to a susceptible bovine. The high genetic diversity of A. marginale in natural transmission settings seems to be one of the key factors for the transovarial transmission to occur.

Dynamic nesting of Anaplasma marginale in the microbial communities of Rhipicephalus microplus

“…Rhipicephalus microplus, commonly known as the cattle tick or tropical cattle tick, is a significant ectoparasite that infests cattle and other livestock. This tick species holds great importance due to its capacity to transmit various pathogens, with A. marginale being one of the most notable (De La Fourniere et al, 2023;Pereira et al, 2022).…”