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DNA Methyltransferases Contribute to Cold Tolerance in Ticks Dermacentor silvarum and Haemaphysalis longicornis (Acari: Ixodidae).

ABSTRACT: DNA methylation, mediated by DNA methyltransferases (Dnmts), is a typical epigenetic process that plays an important role in affecting organism acclimatization and adaptation to environmental changes. However, information about Dnmts and their associations with the cold tolerance of ticks remains meager. Hence, in the present study, the Dnmts in important vector ticks Dermacentor silvarum and Haemaphysalis longicornis were cloned and identified, and their functions in cold response were further explored. Results showed that the length of DsDnmt and DsDnmt1 in D. silvarum, and HlDnmt1 and HlDnmt in H. longicornis were 1,284, 549, 1,500, and 1,613 bp, respectively. Bioinformatics in protein analysis revealed that they were all unstable hydrophilic proteins and were mainly characterized with Dcm (DNA cytosine methyltransferase domain), Dnmt1-RFD (DNA methyltransferase replication foci domain), zf-CXXC (zinc finger-CXXC domain), and BAH (Bromo adjacent homology domain). The relative expression of these Dnmts was reduced after cold treatment for 3 days (P < 0.05), and increased with the extension of treatment. Western blot revealed that Dnmt1 decreased first and then increased significantly (P < 0.05) in both tick species, whereas other Dnmts fluctuated at varying degrees. RNA interference significantly silenced the genes Dnmts (P < 0.01), and mortality increased significantly (P < 0.05), when exposed to sub-lethal temperature, underscoring the important roles of Dnmts during the cold response of D. silvarum and H. longicornis. The above results lay the foundation for further understanding of the epigenetic regulation of DNA methylation in cold acclimatization and adaptation of ticks.

SUBMITTER: Agwunobi DO

PROVIDER: S-EPMC8426640 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundHistone acetylation is involved in the regulation of stress responses in multiple organisms. Dermacentor silvarum is an important vector tick species widely distributed in China, and low temperature is a crucial factor restricting the development of its population. However, knowledge of the histone acetyltransferases and epigenetic mechanisms underlying cold-stress responses in this tick species is limited.MethodsHistone acetyltransferase genes were characterized in D. silvarum, and their relative expressions were determined using qPCR during cold stress. The association and modulation of histone acetyltransferase genes were further explored using RNA interference, and both the H3K9 acetylation level and relative expression of KAT5 protein were evaluated using western blotting.ResultsThree histone acetyltransferase genes were identified and named as DsCREBBP, DsKAT6B, and DsKAT5. Bioinformatics analysis showed that they were unstable hydrophilic proteins, characterized by the conserved structures of CBP (ZnF_TAZ), PHA03247 super family, Creb_binding, and MYST(PLN00104) super family. Fluorescence quantitative PCR showed that the expression of DsCREBBP, DsKAT6B, and DsKAT5 increased after 3 days of cold treatment, with subsequent gradual decreases, and was lowest on day 9. Western blotting showed that both the H3K9 acetylation level and relative expression of KAT5 in D. silvarum increased after treatment at - 4, 4, and 8 °C for 3 and 6 days, whereas they decreased significantly after a 9-day treatment. RNA interference induced significant gene silencing, and the mortality rate of D. silvarum significantly increased at the respective semi-lethal temperatures.ConclusionThese results imply that histone acetyltransferases play an important role in tick adaptation to low temperatures and lay a foundation for further understanding of the epigenetic regulation of histone acetylation in cold-stressed ticks. Further research is needed to elucidate the mechanisms underlying histone acetylation during cold stress in ticks.

Project description:Ticks are important disease vectors, as they transmit a variety of human and animal pathogens worldwide. Symbionts that coevolved with ticks confer crucial benefits to their host in nutrition metabolism, fecundity, and vector competence. Although over 100 tick species have been identified in China, general information on tick symbiosis is limited. Here, we visualized the tissue distribution of Coxiella sp. and Rickettsia sp. in lab-reared Haemaphysalis longicornis and Rhipicephalus haemaphysaloides by fluorescent in situ hybridization. We found that Coxiella sp. colonized exclusively the Malpighian tubules and ovaries of H. longicornis, while Rickettsia sp. additionally colonized the midgut of R. haemaphysaloides We also investigated the population structure of microbiota in Dermacentor silvarum ticks collected from Inner Mongolia, China, and found that Coxiella, Rickettsia, and Pseudomonas are the three dominant genera. No significant difference in microbiota composition was found between male and female D. silvarum ticks. We again analyzed the tissue localization of Coxiella sp. and Rickettsia sp. and found that they displayed tissue tropisms similar to those in R. haemaphysaloides, except that Rickettsia sp. colonized the nuclei of spermatids instead of ovaries in D. silvarum Altogether, our results suggest that Coxiella sp. and Rickettsia sp. are the main symbionts in the three ticks and reside primarily in midgut, Malpighian tubules, and reproductive tissues, but their tissue distribution varies in association with species and sexes.IMPORTANCE Tick-borne diseases constitute a major public health burden, as they are increasing in frequency and severity worldwide. The presence of symbionts helps ticks to metabolize nutrients, promotes fecundity, and influences pathogen infections. Increasing numbers of tick-borne pathogens have been identified in China; however, knowledge of native ticks, especially tick symbiosis, is limited. In this study, we analyze the distribution of Coxiella sp. and Rickettsia sp. in tissues of laboratory-reared Haemaphysalis longicornis and Rhipicephalus haemaphysaloides and field-collected Dermacentor silvarum We found that the localization patterns of Coxiella sp. in three Chinese tick species were similar to those of other tick species. We also found a previously undefined intracellular localization of Rickettsia sp. in tick midgut and spermatids. In addition, we demonstrate that tissue tropisms of symbionts vary between species and sexes. Our findings provide new insights into the tissue localization of symbionts in native Chinese ticks and pave the way for further understanding of their functional capabilities and symbiotic interactions with ticks.

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DNA Methyltransferases Contribute to Cold Tolerance in Ticks Dermacentor silvarum and Haemaphysalis longicornis (Acari: Ixodidae).

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