A proteomic insight into the midgut proteome of Ornithodoros moubata females reveals novel information on blood digestion in argasid ticks

Abstract

BackgroundThe argasid tick Ornithodoros moubata is the main African vector of the human relapsing fever agent Borrelia duttoni and the African swine fever virus. Together with saliva, the tick midgut forms part of the host-tick-pathogen interface, and numerous midgut proteins play key functions in the blood digestion-related process and the infection and transmission of pathogens. This work explores the composition of the midgut proteome of unfed and fed O. moubata females with the aim to complete the biological information already obtained from the midgut transcriptome and provide a more robust and comprehensive perspective of this biological system.MethodsMidgut tissues taken from females before feeding and 48 h after feeding were subjected to LC/MS-MS analysis. After functional characterization and classification of the proteins identified, the differences in the proteome between unfed and fed females were analysed and discussed. Additionally, a detailed analysis of particular groups of proteins that are involved in the processes of nutrient digestion and responses to the oxidative stress was carried out.Results1491 non-redundant tick proteins were identified: 1132 of them in the midgut of unfed ticks, 1138 in the midgut of fed ticks, and up to 779 shared by both physiological conditions. Overall, the comparative analysis of the midgut proteomes of O. moubata females before and after feeding did not reveal great differences in the number or class of proteins expressed, enzymatic composition or functional classification.ConclusionsThe hemoglobinolytic system in ixodids and argasids is very similar in spite of the fact that they display very different feeding and reproductive strategies. Although the main source of nutrients in ticks are proteins, lipids and carbohydrates also constitute significant nutritional sources and play an important part in the process of blood digestion. The genes and proteins involved in intracellular transport mechanisms, defensive responses, detoxifying responses and stress responses seem to be closely regulated, highlighting the complexity and importance of these processes in tick biology, which in turn assigns them a great interest as targets for therapeutic and immunological interventions.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2300-8) contains supplementary material, which is available to authorized users.

Gene Expression in the Salivary Gland of Rhipicephalus (Boophilus) microplus Fed on Tick-Susceptible and Tick-Resistant Hosts

“…In Schyzosaccharomyces pombe, calnexin overexpression is involved in the induction of apoptosis triggered by endoplasmic reticulum stress (Guérin et al, 2008). In the midgut of the argasid tick Ornithodoros moubata female, a calnexin protein has been identified and determined to be involved with the stress responses associated with blood digestion (Oleaga et al, 2017). A calnexin transcript was upregulated in the Ixodes ricinus-derived cell line IRE/CTVM19 at day 2 post-infection with the flavivirus tickborne encephalitis virus (TBEV), which may have an important role in the response of tick cells to virus infection (Weisheit et al, 2015).…”

“…Four phosphate-adaptor proteins 1 and 2 (FAPP1 and FAPP2) are proteins that localize to the trans-Golgi network (TGN) on nascent carriers and interact with phosphatidylinositol-4-phosphate and the small GTPase ADPribosylation factor (ARF) through their plekstrin homology domain (Godi et al, 2004). Phosphoinositol 4-phosphate adaptor proteins are involved in lipid transport (Oleaga et al, 2017) and control the formation and fission of post-Golgi vesicles and regulate secretory transport from the TGN to the plasma membrane, and displacement or knockdown of FAPPs inhibits cargo transfer to the plasma membrane (Godi et al, 2004). In Ornithodoros moubata ticks, phosphoinositol 4-phosphate adaptor protein transcripts were upregulated in the midgut after blood feeding in comparison with non-fed ticks (Oleaga et al, 2017).…”

“…Phosphoinositol 4-phosphate adaptor proteins are involved in lipid transport (Oleaga et al, 2017) and control the formation and fission of post-Golgi vesicles and regulate secretory transport from the TGN to the plasma membrane, and displacement or knockdown of FAPPs inhibits cargo transfer to the plasma membrane (Godi et al, 2004). In Ornithodoros moubata ticks, phosphoinositol 4-phosphate adaptor protein transcripts were upregulated in the midgut after blood feeding in comparison with non-fed ticks (Oleaga et al, 2017). The phosphatidylinositol-4-phosphate, in turn, is a minor plasma membrane phospholipid component of a signal transduction pathway in tick salivary glands (McSwain et al, 1989), a key regulator of membrane transport required for the formation of transport carriers from the TGN.…”

The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles

“…Choice of 'shot-gun' technology will be important. Use of liquid chromatography and tandem mass spectrometry analysis (LC/MS-MS) of the mid-gut proteome of O. moubata females failed to find great differences in the number or class of proteins expressed, enzymatic composition or functional classification before and after blood feeding- Oleaga et al (2017). This was despite a detailed analysis of particular groups of proteins that are involved in the processes of nutrient digestion and responses to the oxidative stress being carried out.…”

The relapsing fever spirochete Borrelia turicatae persists in the highly oxidative environment of its soft‐bodied tick vector

“…ROS and RNS appear to be substantial environmental challenges for B. burgdorferi during both blood meal acquisition and during starvation in I. scapularis nymphs, as ROS‐sensitive and RNS‐sensitive B. burgdorferi strains harbouring mutations in antioxidant defence genes show poor survival compared with their wild‐type counterparts (Bourret et al, ; Eggers et al, ; Li et al, ). To the best of our knowledge, the production of ROS and RNS in Ornithodoros ticks has not been reported; however, transcriptomic and proteomic studies have identified a variety of oxidant metabolism and antioxidant defence genes expressed in soft‐bodied ticks that transmit RF Borrelia (Francischetti, Mans, et al, ; Francischetti, Meng, et al, ; Landulfo et al, ; Oleaga, Obolo‐Mvoulouga, Manzano‐Roman, & Perez‐Sanchez, ; Oleaga, Obolo‐Mvoulouga, Manzano‐Roman, & Perez‐Sanchez, ; Oleaga, Obolo‐Mvoulouga, Manzano‐Roman, & Perez‐Sanchez, ).…”