Functional annotation and analysis of the Ornithodoros moubata midgut genes differentially expressed after blood feeding

Abstract

The argasid tick Ornithodoros moubata is the main vector of the African swine fever and the human relapsing fever in Africa. As part of the host-parasite-pathogen interface, the tick midgut expresses key proteins for tick survival and tick-borne pathogen transmission. Accordingly, midgut proteins are potential targets for the development of new drugs and vaccines aimed at tick control, and obtaining proteomic and transcriptomic data from the O. moubata midgut would facilitate the identification of such target candidates. With this aim, we have assembled and characterized the midgut transcriptome of O. moubata females before and 48h after a blood meal, and identified the genes that are differentially expressed in the midgut after feeding. Overall, 23,863 transcripts were obtained, and of them, 9,164 were identified and annotated. The most represented molecular functions were catalytic and binding activities, and the most represented biological processes were metabolic, cellular and single-organism processes. KEGG analysis of the annotated sequences assigned up to 3,053 of them to 130 active pathways, among which, the top 30 pathways were mostly metabolic routes. Differential expression analysis between unfed and fed ticks detected 8,026 Differentially Expressed Genes (DEGs), 4,093 up-regulated and 3,933 down-regulated, respectively. The biological significance of these DEGs was further investigated using the KEEG, Pfam and GO databases. The functional groups of the genes/proteins predicted to be involved in the processes of blood digestion, nutrient transport and metabolism, and in responses related to defence and oxidative stress are discussed in more detail. This work reports the first midgut transcriptome analysis of an argasid tick species, and provides a wealth of novel molecular information about the argasid machinery involved in blood feeding and digestion. This information represents a starting point for the development of alternative strategies for tick control.

De Novo Assembly and Analysis of Transcriptome of the Dermacentor Marginatus Genes Differentially Expressed After Blood Feeding and Long-term Starvation

“…Up regulated genes potentially involved in protein metabolism are listed in Table 2 and Supplementary Table 3. Protein families of proteases, such as cysteine peptidases, aspartic endopeptidases, metallopeptidases and serine peptidases were signi cantly up-regulated suggesting that the proteolytic system was active [41]. The results were quite similar with some of the transcriptome studies [31,47].…”

“…Up to 55 unigenes on carbohydrate metabolism were differentially expressed (35 in F tick group, 9 in H tick group and 11 in M tick group), covering biological process such as carbohydrate phosphorylation, protein glycosylation, glycogen catabolic process, galactose metabolic process. The results indicated that the up-regulated unigenes encoding carbohydrate-metabolizing enzymes were similar with the genes identi ed in the transcriptomes of Ixodes ricinus [67], Haemaphysalis ava [31], Dermacentor variabilis [68], and in Argasidae of Ornithodoros moubata [41] and Ornithodoros erraticus [60]. According to the annotations, the up-regulated unigenes were associated with the metabolism and transport of several carbohydrates including glucose, fructose, mannose, galactose, maltose, idose, malate and chitin (Table 4).…”

“…3). The remaining 20579 unigenes (61.6%) were classi ed as unknown because they did not produce matches within the searched databases, indicating that many new genes and noncoding RNA sequences had been identi ed [31,41]. The reason that most of hits matched with Ixodes rather than Dermacentor was probably because the only tick genomic information on Ixodes scapularis was available in the NCBI database [15], and rather few information on Dermacentor sequence was deposited.…”

African swine fever virus-like integrated elements in a soft tick genome – an ancient virus vector arms race?

“…Through the analysis of published transcriptome data from Ornithodoros ticks, we identified ASFLIspecific RNA in O. moubata ticks from laboratory colonies from Spain (18) and Japan (19) (Figure 4 and Supplementary Tables 1 and 2), while in pertinent data from O. erraticus (20) and Ornithodoros turicata (PRJNA447876) no ASFLI-specific RNA was detected ( Figure 4). Furthermore, we examined nine porcinus ticks, we detected ASFLI-specific reads or even contigs (Figure 4, Supplementary Table 6).…”

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, ).…”