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

Insect Mol Biol. 2015 Oct;24(5):570-81. doi: 10.1111/imb.12184. Epub 2015 Jul 17.

Abstract

Tick selenoproteins have been associated with antioxidant activity in ticks. Thioredoxin reductase (TrxR), also a selenoprotein, belongs to the pyridine nucleotide-disulphide oxidoreductase family of proteins and is an important antioxidant. Molecular interactions between native microbiota and tick hosts have barely been investigated to date. In this study, we determined the functional role of TrxR in tick feeding and in maintenance of the native microbial community. TrxR transcript levels remained high and microbial load was reduced throughout tick attachment to the vertebrate host. RNA interference (RNAi) showed that depletion of TrxR activity did not interfere with tick haematophagy 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 whereas the antioxidant genes Manganese superoxide dismutase (MnSOD), copper/zinc superoxide dismutase (Cu/Zn SOD) and selenoprotein M (SelM) were significantly down-regulated 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, we observed the altered bacterial profiles in TrxR-silenced tick tissues. Taken together, these results indicate an essential functional role for TrxR in maintaining the bacterial community associated with ticks.

Keywords: Amblyomma maculatum; Ixodidae ticks; RNA interference; caspases; microbiota; selenoprotein; superoxide dismutase; thioredoxin reductase; transcriptional expression.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antioxidants / metabolism
  • Bacterial Physiological Phenomena
  • Female
  • Ixodidae / enzymology*
  • Ixodidae / genetics
  • Ixodidae / microbiology*
  • Microbiota*
  • Oxidation-Reduction
  • RNA Interference
  • RNA, Double-Stranded
  • Salivary Glands / enzymology
  • Salivary Glands / microbiology
  • Selenoproteins / genetics
  • Selenoproteins / metabolism*
  • Sheep / parasitology
  • Superoxide Dismutase / metabolism
  • Thioredoxin-Disulfide Reductase / genetics
  • Thioredoxin-Disulfide Reductase / metabolism*
  • Transcriptional Activation

Substances

  • Antioxidants
  • RNA, Double-Stranded
  • Selenoproteins
  • Superoxide Dismutase
  • Thioredoxin-Disulfide Reductase