Refractoriness of Sergentomyia schwetzi to Leishmania spp. is mediated by the peritrophic matrix

Abstract

BackgroundThe peritrophic matrix (PM) is an acellular chitin-containing envelope which in most blood sucking insects encloses the ingested blood meal and protects the midgut epithelium. Type I PM present in sand flies and other blood sucking batch feeders is secreted around the meal by the entire midgut in response to feeding. Here we tested the hypothesis that in Sergentomyia schwetzi the PM creates a physical barrier that prevents escape of Leishmania parasites from the endoperitrophic space.Methodology/Principal findingsMorphology and ultrastructure of the PM as well the production of endogenous chitinase in S. schwetzi were compared with three sand fly species, which are natural vectors of Leishmania. Long persistence of the PM in S. schwetzi was not accompanied by different morphology or decreased production of chitinase. To confirm the role of the PM in refractoriness of S. schwetzi to Leishmania parasites, culture supernatant from the fungus Beauveria bassiana containing chitinase was added to the infective bloodmeal to disintegrate the PM artificially. In females treated with B. bassiana culture supernatants the PM was weakened and permeable, lacking multilayered inner structure; Leishmania colonized the midgut and the stomodeal valve and produced metacyclic forms. In control females Leishmania infections were lost during defecation.Conclusions/SignificancePersistence of the PM till defecation of the bloodmeal represents an important factor responsible for refractoriness of S. schwetzi to Leishmania development. Leishmania major as well as L. donovani promastigotes survived defecation and developed late-stage infections only in females with PM disintegrated artificially by B. bassiana culture supernatants containing exogenous chitinase.

Association of Phlebotomus guggisbergi with Leishmania major and Leishmania tropica in a complex transmission setting for cutaneous leishmaniasis in Gilgil, Nakuru county, Kenya

“…Although we identified rock hyrax bloodmeal in one uninfected Sergentomyia spp., sandflies of this genus are known to be refractory to Leishmania parasites that are pathogenic to humans [59]. However, because they can feed on humans, it is important to control their biting nuisance.…”

Interactions between host biogenic amines and sand fly salivary yellow-related proteins

“…The degradation of serotonin is connected with oxidative stress [34], similarly to heme detoxification [35]. The midgut epithelium of blood-sucking insects is protected from these toxins by the peritrophic matrix (PM) [35], which differs between S. schwetzi and P. argentipes in morphology and duration: in S. schwetzi the PM is thicker and has a prolonged persistence [36], and thus could block the unfavourable effects of serotonin on oviposition.…”

Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae)

“…Generally, transmission of Mundinia by sand flies must be still considered as various sand fly species present in endemic localities cannot be included into the laboratory study being never colonized, particularly South American and South Asian members of the genus Sergentomyia. The only species of the genus Sergentomyia where vector competence has been directly tested by experimental infections, S. schwetzi, was demonstrated to be refractory to Leishmania parasites [53][54]. However, the vector competence of other species of this large genus of sand flies may differ (reviewed by [55]).…”