An insight into the functional role of thioredoxin reductase, a selenoprotein, in maintaining normal native microbiota in the Gulf Coast tick (Amblyomma maculatum)

Abstract

Tick selenoproteins have been associated with antioxidant activity in ticks. Thioredoxin reductase (TrxR), also a selenoprotein, belongs to the pyridine nucleotide-disulfide oxidoreductase family of proteins and is an important antioxidant protein. Molecular interaction between native microbiota and tick hosts are barely investigated. In this study, we have determined the functional role of TrxR in tick feeding, and maintenance of native microbial community. TrxR transcript levels remained high and microbial load was reduced throughout tick attachment to the vertebrate host. Results of RNA interference (RNAi) show that depletion of TrxR activity did not interfere with tick hematophagy or phenotype but did reduce the viability of the microbiome within the tick tissues, presumably by perturbing redox homeostasis. The transcriptional activity of various antioxidant genes remained unaffected while antioxidant genes MnSOD, Cu/ZnSOD and SelM were significantly downregulated in salivary glands of the ticks subjected to RNAi. The perturbed TrxR enzymatic activity in the knocked down tick tissues negatively affected the bacterial load as well. Furthermore, the bacterial profiles in all the tissues dominated by Rickettisiaceae family decreased in TrxR silenced tissues. Taken together, these results indicate an essential functional role for TrxR in maintaining the bacterial community associated with ticks.

Assessment of tick antioxidant responses to exogenous oxidative stressors and insight into the role of catalase in the reproductive fitness of the Gulf Coast tick, Amblyomma maculatum

“…maculatum to offset starvation stress and blood feeding‐related stress makes it likely that it possesses a proactive antioxidant system. Complete studies of the tick interactive antioxidant network are presently still lacking, but the available literature implicates the extensive arsenal of antioxidant and redox‐associated selenoproteins in the ability of the tick to tolerate extreme alterations in redox homeostasis associated with long periods of starvation off the host, and the acquisition and digestion of blood and bloodmeal‐related products on the host (Adamson et al ., ; Budachetri & Karim, ).…”

RNA Interference – A Powerful Functional Analysis Tool for Studying Tick Biology and its Control

“…In another study, silencing thioredoxin reductase, another selenoprotein, in A. maculatum did not have a negative impact on blood feeding and reproduction. Likewise, variations in transcriptional expression of some antioxidant enzymes were also observed, suggesting compensatory mechanism in the absence of thioredoxin reductase [139]. However, the more interesting finding in that study was the decreased microbiota population following thioredoxin reductase knockdown, possibly because of disturbed redox homeostasis balance.…”

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

“…The bacterial load in each tick tissue was estimated as described previously (Budachetri and Karim, 2015; Narasimhan et al, 2014). A slightly modified published protocol was used to estimate FLE (Dergousoff and Chilton, 2012) and CMM numbers (Sassera et al, 2006).…”

“…Therefore, to successfully feed and survive, ticks must somehow prevent the detrimental and promote the beneficial aspects of ROS release, which suggests that precise regulatory strategies must exist for maintaining appropriate ROS levels both within the tick and possibly at the tick—host interface. Our previous studies have revealed an adaptive co-evolutionary process that enables the survival of the tick-borne pathogen Rickettsia parkeri by manipulating an antioxidant defense system associated with selenium, which includes a full set of selenoproteins and other antioxidants (Adamson et al, 2014, 2013; Budachetri et al, 2017; Budachetri and Karim, 2015; Crispell et al, 2016; Karim et al, 2011; Karim and Ribeiro, 2015; Kumar et al, 2016). ROS generation is one of the first lines of host defense against invading microbes (Ha et al, 2005).…”

“…Interestingly, the role of selenoproteins in Drosophila does not appear to be critical for either lifespan or oxidative stress defense (Hirosawa-Takamori et al, 2004). In contrast, despite the lack of published research, there is evidence that the tick selenoproteome and antioxidant enzymes may play critical roles in detoxifying ROS and maintaining both vector microbiota and R. parkeri colonization (Adamson et al, 2013; Budachetri et al, 2017; Budachetri and Karim, 2015; Crispell et al, 2016; Kumar et al, 2016). …”