An official website of the United States government
Abstract Ticks are important vectors of pathogenic viruses, bacteria, and protozoans to humans, wildlife, and domestic animals. Due to their life cycles, ticks face significant challenges related to water homeostasis. When blood‐feeding, they must excrete water and ions, but when off‐host (for stretches lasting several months), they must conserve water to avoid desiccation. Aquaporins (AQPs), a family of membrane‐bound water channels, are key players in osmoregulation in many animals but remain poorly characterized in ticks. Here, we bioinformatically identified AQP‐like genes from the deer tickIxodes scapularisand used phylogenetic approaches to map the evolution of the aquaporin gene family in arthropods. Most arachnid AQP‐like sequences (including those ofI. scapularis) formed a monophyletic group clustered within aquaglycerolporins (GLPs) from bacteria to vertebrates. This gene family is absent from insects, revealing divergent evolutionary paths for AQPs in different hematophagous arthropods. Next, we sequenced the full‐length cDNA ofI. scapularisaquaporin 1 (IsAQP1) and expressed it heterologously inXenopusoocytes to functionally characterize its permeability to water and solutes. Additionally, we examinedIsAQP1expression across different life stages and adult female organs. We foundIsAQP1is an efficient water channel with high expression in salivary glands prior to feeding, suggesting it plays a role in osmoregulation before or during blood feeding. Its functional properties are unique: unlike most GLPs,IsAQP1has low glycerol permeability, and unlike most AQPs, it is insensitive to mercury. Together, our results suggestIsAQP1plays an important role in tick water balance physiology and that it may hold promise as a target of novel vector control efforts.
more »
« less
Progressive behavioural, physiological and transcriptomic shifts over the course of prolonged starvation in ticks
Abstract Ticks are obligatorily hematophagous but spend the majority of their lives off host in an unfed state where they must resist starvation between bouts of blood feeding. Survival during these extended off‐host periods is critical to the success of these arthropods as vectors of disease; however, little is known about the underlying physiological and molecular mechanisms of starvation tolerance in ticks. We examined the bioenergetic, transcriptomic and behavioural changes of female American dog ticks,Dermacentor variabilis, throughout starvation (up to nine months post‐bloodmeal). As starvation progressed, ticks utilized glycogen and lipid, and later protein as energy reserves with proteolysis and autophagy facilitating the mobilization of endogenous nutrients. The metabolic rate of the ticks was expectedly low, but showed a slight increase as starvation progressed possibly reflecting the upregulation of several energetically costly processes such as transcription/translation and/or increases in host‐seeking behaviours. Starved ticks had higher activity levels, increased questing behaviour and augmented expression of genes related to chemosensing, immunity and salivary gland proteins. The shifts in gene expression and associated behavioural and physiological processes are critical to allowing these parasites to exploit their ecological niche as extreme sit‐and‐wait parasites. The overall responses of ticks to starvation were similar to other blood‐feeding arthropods, but we identified unique responses that could have epidemiological and ecological significance for ticks as ectoparasites that must be tolerant of sporadic feeding.
more »
« less
- Award ID(s):
- 1654417
- PAR ID:
- 10084065
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 28
- Issue:
- 1
- ISSN:
- 0962-1083
- Format(s):
- Medium: X Size: p. 49-65
- Size(s):
- p. 49-65
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT Ticks are blood-feeding ectoparasites but spend most of their life off-host where they may have to tolerate low winter temperatures. Rapid cold hardening (RCH) is a process commonly used by arthropods, including ticks, to improve survival of acute low temperature exposure. However, little is known about the underlying mechanisms in ticks associated with RCH, cold shock and recovery from these stresses. In the present study, we investigated the extent to which RCH influences gene expression and metabolism during recovery from cold stress in Dermacentor variabilis, the American dog tick, using a combined transcriptomics and metabolomics approach. Following recovery from RCH, 1860 genes were differentially expressed in ticks, whereas only 99 genes responded during recovery to direct cold shock. Recovery from RCH resulted in an upregulation of various pathways associated with ion binding, transport, metabolism and cellular structures seen in the response of other arthropods to cold. The accumulation of various metabolites, including several amino acids and betaine, corresponded to transcriptional shifts in the pathways associated with these molecules, suggesting congruent metabolome and transcriptome changes. Ticks, D. variabilis and Amblyomma maculatum, receiving exogenous betaine and valine demonstrated enhanced cold tolerance, suggesting cryoprotective effects of these metabolites. Overall, many of the responses during recovery from cold shock in ticks were similar to those observed in other arthropods, but several adjustments may be distinct from the responses in other currently examined taxa.more » « less
-
Rich, Stephen (Ed.)Abstract The ability to escape predation modulates predator–prey interactions and represents a crucial aspect of organismal life history, influencing feeding, mating success, and survival. Thanatosis, also known as death feigning or tonic immobility (TI), is taxonomically widespread, but understudied in blood-feeding vectors. Hematophagous arthropods, such as ticks, are unique among animals as their predators (birds, mice, lizards, frogs, and other invertebrates) may also be their source of food. Therefore, the trade-off between predator avoidance and host-seeking may shift as the time since the last bloodmeal increases. Because ticks are slow-moving and unable to fly, or otherwise escape, we predicted that they may use TI to avoid predation, but that TI would be influenced by time since the last bloodmeal (starvation). We therefore aimed to quantify this relationship, examining the effect of starvation, body mass, and ontogeny on TI for two tick species: Dermacentor variabilis (Say) (Acari: Ixodidae) and Rhipicephalus sanguineus (Latreille) (Acari: Ixodidae). As we predicted, the duration and use of TI decreased with time since feeding and emergence across species and life stages. Therefore, ticks may become more aggressive in their search for a bloodmeal as they continue to starve, opting to treat potential predators as hosts, rather than avoiding predation by feigning death. Antipredator behaviors such as TI may influence the intensity and amount of time ticks spend searching for hosts, driving patterns of tick-borne pathogen transmission. This identification and quantification of a novel antipredation strategy add a new component to our understanding of tick life history.more » « less
-
Skare, Jon T. (Ed.)Pathogens possess the ability to adapt and survive in some host species but not in others–an ecological trait known as host tropism. Transmitted through ticks and carried mainly by mammals and birds, the Lyme disease (LD) bacterium is a well-suited model to study such tropism. Three main causative agents of LD, Borrelia burgdorferi , B . afzelii , and B . garinii , vary in host ranges through mechanisms eluding characterization. By feeding ticks infected with different Borrelia species, utilizing feeding chambers and live mice and quail, we found species-level differences in bacterial transmission. These differences localize on the tick blood meal, and specifically complement, a defense in vertebrate blood, and a polymorphic bacterial protein, CspA, which inactivates complement by binding to a host complement inhibitor, Factor H (FH). CspA selectively confers bacterial transmission to vertebrates that produce FH capable of allele-specific recognition. CspA is the only member of the Pfam54 gene family to exhibit host-specific FH-binding. Phylogenetic analyses revealed convergent evolution as the driver of such uniqueness, and that FH-binding likely emerged during the last glacial maximum. Our results identify a determinant of host tropism in Lyme disease infection, thus defining an evolutionary mechanism that shapes host-pathogen associations.more » « less
-
null (Ed.)Abstract Parasites cause harm to their hosts and represent pervasive causal agents of natural selection. Understanding host proximate responses during interactions with parasites can help predict which genes and molecular pathways are targets of this selection. In the current study, we examined transcriptional changes arising from interactions between Drosophila melanogaster and their naturally occurring ectoparasitic mite, Gamasodes queenslandicus . Shifts in host transcript levels associated with behavioural avoidance revealed the involvement of genes underlying nutrient metabolism. These genetic responses were reflected in altered body lipid and glycogen levels in the flies. Mite infestation triggered a striking immune response, while male accessory gland protein transcript levels were simultaneously reduced, suggesting a trade-off between host immune responses to parasite challenge and reproduction. Comparison of transcriptional analyses during mite infestation to those during nematode and parasitoid attack identified host genes similarly expressed in flies during these interactions. Validation of the involvement of specific genes with RNA interference lines revealed candidates that may directly mediate fly–ectoparasite interactions. Our physiological and molecular characterization of the Drosophila – Gamasodes interface reveals new proximate mechanisms underlying host–parasite interactions, specifically host transcriptional shifts associated with behavioural avoidance and infestation. The results identify potential general mechanisms underlying host resistance and evolutionarily relevant trade-offs.more » « less
