Protein regulation mechanism of cold tolerance in Haemaphysalis longicornis

Abstract

Ticks are external parasitic arthropods that can transmit a variety of pathogens by sucking blood. Low‐temperature tolerance is essential for ticks to survive during the cold winter. Exploring the protein regulation mechanism of low‐temperature tolerance of Haemaphysalis longicornis could help to explain how ticks survive in winter. In this study, the quantitative proteomics of several tissues of H. longicornis exposed to low temperature were studied by data independent acquisition technology. Totals of 3 699, 3 422, and 1 958 proteins were identified in the salivary gland, midgut, and ovary, respectively. The proteins involved in energy metabolism, cell signal transduction, protein synthesis and repair, and cytoskeleton synthesis changed under low‐temperature stress. The comprehensive analysis of the protein regulation of multiple tissues of female ticks exposed to low temperature showed that maintaining cell homeostasis, maintaining cell viability, and enhancing cell tolerance were the most important means for ticks to maintain vital signs under low temperature. The expression of proteins involved in and regulating the above cell activities was the key to the survival of ticks under low temperatures. Through the analysis of a large amount of data, we found that the expression levels of arylamine N‐acetyltransferase, inositol polyphosphate multikinase, and dual‐specificity phosphatase were up‐regulated under low temperature. We speculated that they might have important significance in low‐temperature tolerance. Then, we performed RNA interference on the mRNA of these 3 proteins, and the results showed that the ability of female ticks to tolerate low temperatures decreased significantly.

Comparative Transcriptome Analysis of Galeruca daurica Reveals Cold Tolerance Mechanisms

“…Cold stress is diverse, and different insect species have evolved different metabolic and physiological adaptations [53]. Maintaining cellular homeostasis, preserving cell viability and enhancing cellular tolerance by adjusting their metabolic status are the most important means of maintaining vital signs in insects at low temperatures [54]. Fatty acid biosynthesis plays a key role in the development of insects, not only in resisting environmental stresses in harsh environments but also in acting as an important antifreeze in low-temperature conditions [55], which is helpful in maintaining the stability of cell membranes, prevent cell freezing and rupture.…”

Female ticks (Ixodes scapularis) infected with Borrelia burgdorferi have increased overwintering survival, with implications for tick population growth

“…, 2022], H. longicornis [Wang et al. , 2022b]). These protective mechanisms provide ticks with the tools to successfully overwinter, but they require an investment of resources during a time when resources are limited.…”

“…I. scapularis, like other ticks, have physiological adaptations (e.g., autophagy) that allow them to survive extended nonfeeding periods (Wang & Cull, 2022). Similarly, ticks also have physiological adaptations that help them survive cold temperatures, such as the production of cryoprotectant molecules (e.g., I. scapularis [Neelakanta et al, 2010], D. variabilis [Rosendale et al, 2022], H. longicornis [Wang et al, 2022b]). These protective mechanisms provide ticks with the tools to successfully overwinter, but they require an investment of resources during a time when resources are limited.…”

“…I. scapularis infected with B. burgdorferi do not appear to upregulate IAFGP, but they do show increased gene expression for other molecules (Narasimhan et al, 2017) known to increase cold tolerance in arthropods (Overgaard & MacMillan, 2017). Similarly, exposure to cold (D. variabilis; Rosendale et al, 2022), infection with B. burgdorfori (I. scapularis; Hart et al, 2022) or a lack of food (H. longicornis; Wang et al, 2022b) induce the production of protective molecules such as heat shock proteins. These molecules can protect organisms from a range of stressors, including pathogens, starvation (King & MacRae, 2015), and cold temperatures (Overgaard & MacMillan, 2017), in a phenomenon known as cross-tolerance (Sinclair et al, 2013).…”

“…, 2022) or a lack of food ( H. longicornis ; Wang et al. , 2022b) induce the production of protective molecules such as heat shock proteins. These molecules can protect organisms from a range of stressors, including pathogens, starvation (King & MacRae, 2015), and cold temperatures (Overgaard & MacMillan, 2017), in a phenomenon known as cross‐tolerance (Sinclair et al.…”