The transcriptional signatures of Sodalis glossinidius in the Glossina palpalis gambiensis flies negative for Trypanosoma brucei gambiense contrast with those of this symbiont in tsetse flies positive for the parasite: Possible involvement of a Sodalis-hosted prophage in fly Trypanosoma refractoriness?

Soumana, Illiassou Hamidou; Loriod, Béatrice; Ravel, Sophie; Tchicaya, Bernadette; Simo, Gustave; Rihet, Pascal; Geiger, Anne

doi:10.1016/j.meegid.2014.03.005

Cited by 25 publications

(37 citation statements)

References 63 publications

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“…These results are in line with those obtained previously when comparing refractory versus infected flies (Hamidou Soumana et al, 2014). Bacteriophage elements have also been identified in other symbiotic associations.…”

Section: Discussionsupporting

confidence: 93%

Identification of overexpressed genes in Sodalis glossinidius inhabiting trypanosome-infected self-cured tsetse flies

et al. 2014

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Sodalis glossinidius, one of the three tsetse fly maternally inherited symbionts, was previously shown to favor fly infection by trypanosomes, the parasites causing human sleeping sickness. Among a population of flies taking a trypanosome-infected blood meal, only a few individuals will acquire the parasite; the others will escape infection and be considered as refractory to trypanosome infection. The aim of the work was to investigate whether fly refractoriness could be associated with specific Sodalis gene expression. The transcriptome of S. glossinidius harbored by flies that were fed either with a non-infected blood meal (control) or with a trypanosome-infected meal but that did not develop infection were analyzed, using microarray technology, and compared. The analysis using the microarray procedure yielded 17 genes that were found to have a significant differential expression between the two groups. Interestingly, all these genes were overexpressed in self-cured (refractory) flies. Further analysis of functional annotation of these genes indicated that most associated biological process terms were related to metabolic and biosynthetic processes as well as to oxido-reduction mechanisms. These results evidence the occurrence of molecular crosstalk between the different partners, induced by the passage of the trypanosomes through the fly's gut even though the parasites were unable to establish in the gut and to develop a permanent infection.

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Section: Discussionsupporting

confidence: 93%

Identification of overexpressed genes in Sodalis glossinidius inhabiting trypanosome-infected self-cured tsetse flies

et al. 2014

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“…Anal drop analysis was selected in this study to determine fly contamination status since the whole midgut was later used for RNA extraction. The prevalence of midgut infection was less than 5% for 10-day flies and greater than 10% for 20-day flies, corresponding with recently recorded values from artificial infection experiments (Ravel et al, 2006; Hamidou Soumana et al, 2014). Using this procedure, flies were separated into infected and self-cured groups (i.e., flies that had ingested trypanosomes in their bloodmeal but had cleared the infection), and dissected according to the method described by Penchenier and Itard (1981).…”

Section: Methodssupporting

confidence: 87%

Midgut expression of immune-related genes in Glossina palpalis gambiensis challenged with Trypanosoma brucei gambiense

et al. 2014

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Tsetse flies from the subspecies Glossina morsitans morsitans and Glossina palpalis gambiensis, respectively, transmit Trypanosoma brucei rhodesiense and Trypanosoma brucei gambiense. The former causes the acute form of sleeping sickness, and the latter provokes the chronic form. Although several articles have reported G. m. morsitans gene expression following trypanosome infection, no comparable investigation has been performed for G. p. gambiensis. This report presents results on the differential expression of immune-related genes in G. p. gambiensis challenged with T. b. gambiense. The aim was to characterize transcriptomic events occurring in the tsetse gut during the parasite establishment step, which is the crucial first step in the parasite development cycle within its vector. The selected genes were chosen from those previously shown to be highly expressed in G. m. morsitans, to allow further comparison of gene expression in both Glossina species. Using quantitative PCR, genes were amplified from the dissected midguts of trypanosome-stimulated, infected, non-infected, and self-cleared flies at three sampling timepoints (3, 10, and 20 days) after a bloodmeal. At the 3-day sampling point, transferrin transcripts were significantly up-regulated in trypanosome-challenged flies versus flies fed on non-infected mice. In self-cleared flies, serpin-2 and thioredoxin peroxidase-3 transcripts were significantly up-regulated 10 days after trypanosome challenge, whereas nitric oxide synthase and chitin-binding protein transcripts were up-regulated after 20 days. Although the expression levels of the other genes were highly variable, the expression of immune-related genes in G. p. gambiensis appears to be a time-dependent process. The possible biological significance of these findings is discussed, and the results are compared with previous reports for G. m. morsitans.

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“…The different steps are described in the corresponding report (Hamidou Soumana et al, 2015), as well as pro parte in reports related to the differential expression of S. glossinidius and W. glossinidia genes (Hamidou Soumana et al, 2014a,b). Sample processing is summarized in Figure 1.…”

Section: Methodsmentioning

confidence: 99%

“…Using a microarray approach, we recently investigated the effect of trypanosome ingestion by G. palpalis gambiensis (Gpg) flies on the transcriptome signatures of Sodalis glossinidius (Farikou et al, 2010; Hamidou Soumana et al, 2014a) and Wigglesworthia glossinidia (Hamidou Soumana et al, 2014b), two symbionts of tsetse flies (Aksoy et al, 2014). The aim of this previous work was to identify the genes that are differentially expressed in trypanosome infected vs. non-infected or self-cured (refractory) flies and that, consequently, can be suspected to positively or negatively control fly infection.…”

Section: Introductionmentioning

confidence: 99%

Comparative Genomics of Glossina palpalis gambiensis and G. morsitans morsitans to Reveal Gene Orthologs Involved in Infection by Trypanosoma brucei gambiense

et al. 2017

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Blood-feeding Glossina palpalis gambiense (Gpg) fly transmits the single-celled eukaryotic parasite Trypanosoma brucei gambiense (Tbg), the second Glossina fly African trypanosome pair being Glossina morsitans/T.brucei rhodesiense. Whatever the T. brucei subspecies, whereas the onset of their developmental program in the zoo-anthropophilic blood feeding flies does unfold in the fly midgut, its completion is taking place in the fly salivary gland where does emerge a low size metacyclic trypomastigote population displaying features that account for its establishment in mammals-human individuals included. Considering that the two Glossina—T. brucei pairs introduced above share similarity with respect to the developmental program of this African parasite, we were curious to map on the Glossina morsitans morsitans (Gmm), the Differentially Expressed Genes (DEGs) we listed in a previous study. Briefly, using the gut samples collected at days 3, 10, and 20 from Gpg that were fed or not at day 0 on Tbg—hosting mice, these DGE lists were obtained from RNA seq—based approaches. Here, post the mapping on the quality controlled DEGs on the Gmm genome, the identified ortholog genes were further annotated, the resulting datasets being compared. Around 50% of the Gpg DEGs were shown to have orthologs in the Gmm genome. Under one of the three Glossina midgut sampling conditions, the number of DEGs was even higher when mapping on the Gmm genome than initially recorded. Many Gmm genes annotated as “Hypothetical” were mapped and annotated on many distinct databases allowing some of them to be properly identified. We identify Glossina fly candidate genes encoding (a) a broad panel of proteases as well as (b) chitin—binding proteins, (c) antimicrobial peptide production—Pro3 protein, transferrin, mucin, atttacin, cecropin, etc—to further select in functional studies, the objectives being to probe and validated fly genome manipulation that prevents the onset of the developmental program of one or the other T. brucei spp. stumpy form sampled by one of the other bloodfeeding Glossina subspecies.

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Cited by 25 publications

References 63 publications

Identification of overexpressed genes in Sodalis glossinidius inhabiting trypanosome-infected self-cured tsetse flies

Identification of overexpressed genes in Sodalis glossinidius inhabiting trypanosome-infected self-cured tsetse flies

Midgut expression of immune-related genes in Glossina palpalis gambiensis challenged with Trypanosoma brucei gambiense

Comparative Genomics of Glossina palpalis gambiensis and G. morsitans morsitans to Reveal Gene Orthologs Involved in Infection by Trypanosoma brucei gambiense

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