A Proteomics Informed by Transcriptomics Insight Into the Proteome of Ornithodoros Erraticus Adult Tick Saliva
Abstract Background: The argasid tick Ornithodoros erraticus is the main vector of tick-borne human relapsing fever (TBRF) and African swine fever (ASF) in the Mediterranean Basin. The prevention and control of these diseases would greatly benefit from the elimination of O. erraticus populations, and anti-tick vaccines are envisaged as an effective and sustainable alternative to chemical acaricide usage for tick control. O. erraticus saliva contains bioactive proteins that play essential functions for tick feeding and host defence modulation, which may contribute to host infection by tick-borne pathogens. Hence, these proteins could be candidate antigen targets for the development of vaccines aimed at the control and prevention of O. erraticus infestations and the diseases it transmits. The objective of the present work was to obtain and characterise the proteome of the saliva of O. erraticus adult ticks as a means to identify and select novel salivary antigen targets.Methods: We have applied a proteomics informed by transcriptomics (PIT) approach to analyse samples of female and male saliva separately using the previously obtained O. erraticus sialotranscriptome as a reference database, and two different mass spectrometry techniques, namely, LC-MS/MS in data-dependent acquisition mode and sequential window acquisition of all theoretical fragment ion spectra mass spectrometry (SWATH-MS). Results: Up to 264 and 263 proteins were identified by LC-MS/MS in the saliva of O. erraticus female and male ticks, respectively, totalling 387 non-redundant proteins. Of them, 224 were further quantified by SWATH-MS in both male and female saliva. Quantified proteins were classified into 23 functional categories and their abundance compared between sexes. Heme/iron binding proteins, protease inhibitors, proteases, lipocalins and immune-related proteins were the categories most abundantly expressed in females, while glycolytic enzymes, protease inhibitors and lipocalins were the most abundantly expressed in males. Ninety-seven proteins were differentially expressed between the sexes: 37 were overexpressed in females and 60 in males. Conclusions: The PIT approach demonstrated its usefulness for proteomics studies of O. erraticus, a non-model organism without genomic sequences available, allowing the publication of the first comprehensive proteome of the saliva of O. erraticus reported to date. These findings confirm important quantitative differences between sexes in the O. erraticus saliva proteome, unveil novel salivary proteins and functions at the tick–host feeding interface and help to understand the physiology of feeding in O. erraticus ticks. The integration of O. erraticus sialoproteomic and sialotranscriptomic data will drive a more rational selection of salivary candidates as antigen targets for the development of vaccines aimed at the control of O. erraticus infestations and the diseases it transmits.