Amblyomma maculatum SECIS binding protein 2 and putative selenoprotein P are indispensable for pathogen replication and tick fecundity

Abstract

Selenium, a vital trace element, is incorporated into selenoproteins to produce selenocysteine. Our previous studies have revealed an adaptive co-evolutionary process that has enabled the spotted fever-causing tick-borne pathogen Rickettsia parkeri to survive by manipulating an antioxidant defense system associated with selenium, which includes a full set of selenoproteins and other antioxidants in ticks. Here, we conducted a systemic investigation of SECIS binding protein 2 (SBP2) and putative selenoprotein P (SELENOP) by transcript silencing in adult female Gulf-coast ticks (Amblyomma maculatum). Knockdown of the SBP2 and SELENOP genes depleted the respective transcript levels of these tick selenogenes, and caused differential regulation of other antioxidants. Importantly, the selenium level in the immature and mature tick stages increased significantly after a blood meal, but the selenium level decreased in ticks after the SBP2 and SELENOP knockdowns. Moreover, the SBP2 knockdown significantly impaired both transovarial transmission of R. parkeri to tick eggs and egg hatching. Overall, our data offer new insight into the relationship between the SBP2 selenoprotein synthesis gene and the putative tick SELENOP gene. It also augments our understanding of selenoprotein synthesis, selenium maintenance and utilization, and bacterial colonization of a tick vector.

Spotted Fever Group Rickettsia Infection and Transmission Dynamics in Amblyomma maculatum

“…parkeri-infected A. maculatum was established at the University of Southern Mississippi (14). The “ Ca .…”

Is selenoprotein K required for Borrelia burgdorferi infection within the tick vector Ixodes scapularis?

“…This is not surprising, since the genome of I. scapularis has 50% coverage. Based on bioinformatics analysis, I. scapularis contains most of the selenogenes which have already been characterized in A. maculatum [5–7, 9, 10]. Interestingly, I. scapularis selenoK has 77% amino acid identity with that of A. maculatum suggesting conserved functions.…”

“…Our recently published work showed the pathogen-induced expression of several tick selenoproteins [7, 9]. Several studies implicated the involvement of selenoK in mitigating endoplasmic reticulum (ER) stress generated upon microbial infection and elevated oxidative stress [38–40].…”

“…Some of the newer specific functions of selenoproteins involve removal of hydrogen peroxide, repair of oxidatively damaged proteins, control of cytoskeleton/actin assembly, protein folding and mitigating ER stress as part of the endoplasmic reticulum associated degradation (ERAD) complex [17], among others. Tick selenoproteins have been shown to play an important role in mitigating oxidative stress [3–12], pathogen colonization [5, 7–9, 11, 18–20] and microbiota maintenance [9, 10, 12].…”

A Peroxiredoxin From the Haemaphysalis longicornis Tick Affects Langat Virus Replication in a Hamster Cell Line

“…In addition, silencing of the catalase gene and inhibition of that protein resulted to the low transmission of Rickettsia parkeri to eggs of Amblyomma maculatum ticks (Budachetri et al, 2017b). Furthermore, the gene silencing of a selenocysteine insertion sequence (SECIS) binding protein (SBP2), involved in selenoprotein synthesis, significantly diminished the transovarial transmission of R. parkeri parasites to eggs in A. maculatum ticks (Budachetri et al, 2017a). Thus, these enzymes are also important to the vector competency of ticks with regard to horizontal transmission and transovarial transmission (Kusakisako et al, 2018a;Hernandez et al, 2019).…”