Midgut proteome of an argasid tick, Ornithodoros erraticus: a comparison between unfed and engorged females

Abstract

BackgroundThe argasid tick Ornithodoros erraticus is the vector of African swine fever virus and of several Borrelia species that cause human relapsing fever in the Iberian Peninsula. The tick midgut is part of the ectoparasite-host interface and expresses proteins that are vital for the survival of the tick. Midgut proteins are therefore potential targets for drug and/or vaccine design aimed at the development of new strategies for tick control. Thus, the aim of this work was the characterization of the proteome of the O. erraticus midgut before and after a blood meal trying to elucidate the induced changes upon blood feeding.MethodsMidgut tissues from unfed and engorged O. erraticus females were dissected and proteins were fractionated by centrifugation and SDS-PAGE, and the corresponding gel pieces analysed by LC–MS/MS. The identified proteins were classified according to their Protein Class and Molecular Function and the differences between fed and unfed specimens were analysed.ResultsOverall 555 tick proteins were identified: 414 in the midgut of the unfed specimens and 376 in the fed specimens, of which 235 were present in both groups. The proteins with catalytic, binding and structural functions were the most numerous and abundant, consistent with their role in the intracellular processing of the blood meal. The analysis of some groups of proteins putatively involved directly in blood meal digestion, including protein digestion (peptidase activity), iron metabolism, enzymes involved in oxidative stress and detoxification and membrane traffic and transport proteins, detected some differences between the fed and unfed ticksConclusionsThis work reports for the first time the collection and analysis of the midgut proteome of an argasid tick species and provides molecular information about the argasid machinery involved in blood digestion. This information represents a starting point for the identification and selection of new targets for the development of alternative control strategies.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-015-1148-z) contains supplementary material, which is available to authorized users.

High-Throughput Identification of the Rhodnius prolixus Midgut Proteome Unravels a Sophisticated Hematophagic Machinery

“…This category is followed by proteins with binding activities representing 37% in both the AM and PM, structural functions (7% in the AM and 8% in the PM), regulators (4% in the AM and PM), transporters (2% in the AM and 3% in the PM), and translation and transcription regulators (3% in the AM and 1% in the PM). These same functional categories have also been identified in other insect midgut proteomes, such as the Glossina palpalis gambiensis tsetse fly [ 20 ] and in ticks Ornithodoros moubata [ 21 ] and Ornithodoros erraticus [ 22 ]. As observed in other proteomics studies [ 23 ], proteins of unknown functions are highly represented, with 35% of all proteins identified in the AM and 32% of those identified in the PM.…”

“…The expression of a large number of HSPs in R. prolixus midgut might be correlated with the arrival of a large amount of warm blood, which induces an increase in the body temperature of the insect. Indeed, members of HSPs were shown to be overexpressed in the midgut of several hematophagous species after a blood meal such as Aedes aegypti [ 26 ], Rhipicephalus microplus [ 27 ], and Ornithodoros erraticus [ 22 ]. In that respect, Hsp70 is the most widely studied HSP as a response to heat and many other stresses [ 24 , 28 ].…”

“…Comparing these findings to other antioxidant machinery identified by proteomic analyses of hematophagous insects show that R. prolixus has the most diversified and sophisticated antioxidant enzymatic machinery. Indeed, only 29 proteins implicated in the antioxidant process and detoxification were identified in Ornithodoros erraticus [ 22 ] and only thirteen in Ornithodoros moubata [ 21 ].…”

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, ).…”

Serine Protease Inhibitors in Ticks: An Overview of Their Role in Tick Biology and Tick-Borne Pathogen Transmission

“…Several comprehensive protein catalogs describing protein diversity in various tick fluids such as saliva (Madden et al, 2004; Cotté et al, 2014; Radulovic et al, 2014; Tirloni et al, 2014a, 2015) or hemolymph (Gudderra et al, 2002; Stopforth et al, 2010), as well as in midgut during feeding (Schwarz et al, 2014; Oleaga et al, 2015), have been compiled, vital to understanding mechanisms implicated in different biological processes such as tick feeding or tick immunity.…”