Document Type : Original Article

Authors

1 National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), NHC Key Laboratory of Parasite and Vector Biology, WHO Collaborating Center for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai, China

2 Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Xi'an Jiaotong University, Xi'an, China

3 Key Laboratory of Tropical Translational Medicine of Ministry of Education, NHC Key Laboratory of Tropical Disease Control, School of Tropical Medicine, Hainan Medical University, Haikou, China

Abstract

Rhipicephalus sanguineus, a repulsive obligate blood feeder, is a three-host tick inflicting tremendous damage. Blood-sucking initiates tick-pathogen-host interactions along with alterations in the expression levels of numerous bioactive ingredients. Key molecules regulating blood meals were identified using the transcriptomic approach. A total number of 744 transcripts showed statistically significantly differential expression including 309 significantly upregulated transcripts and 435 significantly downregulated transcripts in semiengorged female ticks compared to unfed ticks, all collected in 2021. The top 10 differentially upregulated transcripts with explicit functional annotations included turripeptide OL55-like protein, valine tRNA ligase-like protein and ice-structuring glycoprotein-like protein. The top 10 differentially down-regulated transcripts were uncharacterized proteins. Gene Ontology (GO) enrichment analysis revealed four associated terms in the cellular component category and 16 in the molecular function category among the top 20 terms. Differentially expressed genes (DEGs) were enriched in GO terms ID 0000323 (lytic vacuole) and ID 0005773 (vacuole).  The top 20 enriched Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways included metabolism, cellular processes, organismal systems and human diseases. The DEGs were enriched in the KEGG term ID: ko-04142 (lysosome pathway) associated with intracellular digestion in the tick midgut epithelium. Molecular markers annotated via comparative transcriptomic profiling were expected to be candidate markers for the purpose of tick control.

Keywords

Main Subjects

  1. Brophy M, Walker KR, Adamson JE, et al. Tropical and temperate lineages of Rhipicephalus sanguineus s.l. ticks (Acari: Ixodidae) host different strains of Coxiella-like endosymbionts. J Med Entomol 2022; 59(6): 2022-2029.
  2. Garcia-Rosales L, Escarcega-Avila A, Ramirez-Lopez M, et al. Immune monitoring of paediatric patients infected with Rickettsia rickettsii, Ehrlichia canis and coinfected. Pathogens 2022; 11(11): 1351. doi: 10.3390/pathogens11111351.
  3. Walker DH, Blanton LS, Laroche M, et al. A vaccine for canine Rocky Mountain spotted fever: an unmet one health need. Vaccines (Basel) 2022; 10(10): 1626. doi: 10.3390/vaccines10101626.
  4. Namina A, Capligina V, Seleznova M, et al. Tick-borne pathogens in ticks collected from dogs, Latvia, 2011-2016. BMC Vet Res 2019; 15: 398. doi: 10.1186/s12917-019-2149-5.
  5. Hazelrig CM, Gettings JR, Cleveland CA, et al. Spatial and risk factor analyses of vector-borne pathogens among shelter dogs in the Eastern United States. Parasit Vectors 2023; 16(1): 197. doi: 10.1186/ s13071-023-05813-1.
  6. Phiri BSJ, Kattner S, Chitimia-Dobler L, et al. Rickettsia in ticks of South Luangwa Valley, Eastern Province, Zambia. Microorganisms 2023; 11(1): 167. doi: 10.3390/microorganisms11010167.
  7. Springer A, Glass A, Probst J, et al. Tick-borne zoonoses and commonly used diagnostic methods in human and veterinary medicine. Parasitol Res 2021; 120(12): 4075-4090.
  8. Burgio F, Meyer L, Armstrong R. A comparative laboratory trial evaluating the immediate efficacy of fluralaner, afoxolaner, sarolaner and imidacloprid + permethrin against adult Rhipicephalus sanguineus (sensu lato) ticks attached to dogs. Parasit Vectors 2016; 9(1): 626. doi: 10.1186/s13071-016-1900-z.
  9. Ebani VV, Mancianti F. Entomopathogenic fungi and bacteria in a veterinary perspective. Biology (Basel) 2021; 10(6): 479. doi: 10.3390/biology10060479.
  10. Oskam CL, Gofton AW, Greay TL, et al. Molecular investigation into the presence of a Coxiella in Rhipicephalus sanguineus ticks in Australia. Vet Microbiol 2017; 201: 141-145.
  11. Guccione C, Colomba C, Tolomeo M, et al. Rickettsiales in Italy. Pathogens 2021; 10(2): 181. doi: 10.3390/pathogens10020181.
  12. Cardenas-Cadena SA, Castañeda-Lopez ME, Mollinedo-Montaño FE, et al. Tick-borne pathogens screening using a multiplex real-time polymerase chain reaction-based method. Acta Parasitol 2023; 68(3): 705-710.
  13. Kidd L, Hamilton H, Stine L, et al. Vector-borne disease and its relationship to hematologic abnormalities and microalbuminuria in retired racing and show-bred greyhounds. J Vet Intern Med 2022; 36(4): 1287-1294.
  14. Oleaga A, Carnero-Morán A, Valero ML, et al. Proteomics informed by transcriptomics for a qualitative and quantitative analysis of the sialoproteome of adult Ornithodoros moubata Parasit Vectors 2021; 14: 396. doi: 10.1186/s13071-021-04892-2.
  15. Stewart PE, Bloom ME. Sharing the ride: Ixodes scapularis symbionts and their interactions. Front Cell Infect Microbiol 2020; 10: 142. doi: 10.3389/ fcimb.2020.00142.
  16. Li Z, Macaluso KR, Foil LD, et al. Inward rectifier potassium (Kir) channels mediate salivary gland function and blood feeding in the lone star tick, Amblyomma americanum. PLoS Negl Trop Dis 2019; 13(2): e0007153. doi: 10.1371/journal.pntd.0007153.
  17. Sharma A, Pooraiiouby R, Guzman B, et al. Dynamics of insulin signaling in the black-legged tick, Ixodes scapularis. Front Endocrinol (Lausanne) 2019; 10: 292. doi: 10.3389/fendo.2019.00292.
  18. Budachetri K, Kumar D, Crispell G, et al. The tick endosymbiont Candidatus Midichloria mitochondrii and selenoproteins are essential for the growth of Rickettsia parkeri in the Gulf Coast tick vector. Microbiome 2018; 6(1): 141. doi: 10.1186/s40168-018-0524-2.
  19. Abbas MN, Chlastáková A, Jmel MA, et al. Serpins in tick physiology and tick-host interaction. Front Cell Infect Microbiol 2022; 12: 892770. doi: 10.3389/fcimb. 2022.892770.
  20. Gargili A, Estrada-Peña A, Spengler JR, et al. The role of ticks in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus: a review of published field and laboratory studies. Antiviral Res 2017; 144: 93-119.
  21. Hernandez EP, Kusakisako K, Talactac MR, et al. Characterization and expression analysis of a newly identified glutathione S-transferase of the hard tick Haemaphysalis longicornis during blood-feeding. Parasit Vectors 2018; 11(1): 91. doi: 10.1186/s13071-018-2667-1.22.
  22. Umemiya-Shirafuji R, Mihara R, Fujisaki K, et al. Intracellular localization of vitellogenin receptor mRNA and protein during oogenesis of a partheno-genetic tick, Haemaphysalis longicornis. Parasit Vectors 2019; 12: 205. doi: 10.1186/s13071-019-3469-9.
  23. Liu L, Yan F, Zhang L, et al. Protein profiling of hemolymph in Haemaphysalis flava Parasit Vectors 2022; 15: 179. doi: 10.1186/s13071-022-05287-7.
  24. Perner J, Hatalova T, Cabello-Donayre M, et al. Haem-responsive gene transporter enables mobilization of host haem in ticks. Open Biol 2021; 11(9): 210048. doi: 10.1098/rsob.210048.
  25. de la Fuente J, Villar M, Cabezas-Cruz A, et al. Tick-host-pathogen interactions: conflict and cooperation. PLoS Pathog 2016; 12(4): e1005488. doi: 10.1371/journal. ppat.1005488.
  26. Chen S, Zhou Y, Chen Y, et al. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34(17): i884-i890.
  27. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9(4): 357-359.
  28. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods 2015; 12(4): 357-360.
  29. Pertea M, Pertea GM, Antonescu CM, et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 2015; 33(3): 290-295.
  30. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15(12): 550. doi: 10.1186/s13059-014-0550-8.
  31. Dantas-Torres F, Otranto D. Rhipicephalus sanguineus (brown dog tick). Trends Parasitol 2022; 38(11): 993-994.
  32. Kim TK, Radulovic Z, Mulenga A. Target validation of highly conserved Amblyomma americanum tick saliva serine protease inhibitor 19. Ticks Tick Borne Dis 2016; 7(3): 405-414.
  33. Mulenga A, Kim TK, Ibelli AMG. Deorphanization and target validation of cross-tick species conserved novel Amblyomma americanum tick saliva protein. Int J Parasitol 2013; 43(6): 439-451.
  34. Xu Z, Lin Z, Wei N, et al. Immunomodulatory effects of Rhipicephalus haemaphysaloides serpin RHS2 on host immune responses. Parasit Vectors 2019; 12(1): 341. doi: 10.1186/s13071-019-3607-4.