Mechanistic underpinnings of dehydration stress in the American dog tick revealed through RNA-Seq and metabolomics

Abstract

Ticks are obligate blood feeders but spend the majority of their lifetime off-host where they must contend with a multitude of environmental stresses. Survival under desiccating conditions is a determinant for habitats where ticks can become established, and water-balance characteristics of ticks have been extensively studied. However, little is known about the underlying aspects associated with dehydration stress in ticks. In this study, we examined the response of male American dog ticks, Dermacentor variabilis, to dehydration using a combined transcriptomics and metabolomics approach. During dehydration, 497 genes were differentially expressed, including an up-regulation of stress-response and protein-catabolism genes and concurrent down-regulation of several energetically expensive biological processes. Accumulation of several metabolites, including specific amino acids, glycerol and gamma aminobutyric acid (GABA), and transcript shifts in the associated pathways for generating these metabolites indicated congruence between changes in the metabolome and gene expression. Ticks treated with exogenous glycerol and GABA demonstrated altered water-balance characteristics; specifically, increased water absorption at high relative humidity. Finally, we observed changes in locomotor activity in response to dehydration, but this change was not influenced by the accumulation of GABA. Overall, the responses to dehydration by these ticks were similar to those observed in other dehydrationtolerant arthropods, but several molecular and behavioral responses are distinct from those associated with other taxa.

Progressive behavioural, physiological and transcriptomic shifts over the course of prolonged starvation in ticks

“…Although protein usage in starved ticks has received little attention, it seems to be an important source of energy, particularly during extended starvation and environmental stress (Jaworski et al., ; Rosendale, Romick‐Rosendale, Watanabe, Dunlevy, & Benoit, ; Rosendale et al., ). In our ticks, the utilization of protein stores was facilitated by changes in metabolic pathways related to protein degradation during starvation, including an upregulation of proteolysis‐related genes and a downregulation of peptidase inhibitors (Figure ).…”

Chemical Isotope Labeling LC-MS for Monitoring Disease Progression and Treatment in Animal Models: Plasma Metabolomics Study of Osteoarthritis Rat Model

“…GABA is considered to be effective immunomoldulatory molecule and plays an important role in autoimmune diseases such as type 1 diabetes and rheumatoid arthritis57. A recent study of mechanistic aspects of dehydration stress in the American dog tick showed accumulation of GABA in ticks, although its specific role is unknown58. Another work of relating stress with GABA level was reported in a metabolomic study of soybean leaves with iron deficiency.…”

Mechanisms underlying insect freeze tolerance

“…via CRISPR/Cas9 technology (Gratz et al, 2013) or RNA interference (RNAi; Scott et al, 2013)] or increasing cryoprotectant abundance [e.g. Generate knockout mutants Gratz et al (2013) by feeding (Koštál et al, 2016) or injection Rosendale et al, 2016)]. If cryoprotectant manipulations reduce or enhance freeze tolerance (loss-and gain-of-function, respectively), we can conclude that they contribute to the mechanisms underlying freeze tolerance.…”