Development of Various Leishmania (Sauroleishmania) tarentolae Strains in Three Phlebotomus Species

Abstract

Leishmania (Sauroleishmania) tarentolae is transmitted by reptile-biting sand flies of the genus Sergentomyia, but the role of Phlebotomus sand flies in circulation of this parasite is unknown. Here, we compared the development of L. (S.) tarentolae strains in three Phlebotomus species: P. papatasi, P. sergenti, and P. perniciosus. Laboratory-bred sand flies were membrane-fed on blood with parasite suspension and dissected on days 1 and 7 post blood meal. Parasites were measured on Giemsa-stained gut smears and five morphological forms were distinguished. In all parasite-vector combinations, promastigotes were found in Malpighian tubules, often in high numbers, which suggests that this tissue is a typical location for L. (S.) tarentolae development in sand flies. All three studied strains colonized the hindgut, but also migrated anteriorly to both parts of the midgut and colonized the stomodeal valve. Significant differences were demonstrated between sand fly species: highest infection rates, high parasite loads, and the most frequent anterior migration with colonization of the stomodeal valve were found in P. perniciosus, while all these parameters were lowest in P. sergenti. In conclusion, the peripylarian type of development was demonstrated for three L. (S.) tarentolae strains in three Phlebotomus sand flies. We suggest paying more attention to Phlebotomus species, particularly P. perniciosus and P. papatasi, as potential secondary vectors of Sauroleishmania.

Experimental infections of sand flies and geckos with Leishmania (Sauroleishmania) adleri and Leishmania (S.) hoogstraali

“…Although it is generally accepted that Sauroleishmania parasites are transmitted by reptile-biting sand flies of the genus Sergentomyia , the role of other sand flies in Sauroleishmania transmission should be reconsidered. The susceptibility of Phlebotomus species to Sauroleishmania infections has been experimentally demonstrated by several authors [ 13 , 14 ] and now confirmed in the present study. Some Phlebotomus species were reported to feed on reptiles [ 4 , 13 , 27 ], and recent molecular detection of Leishmania ( Sauroleishmania ) tarentolae in Phlebotomus spp.…”

“…Morphological stages of the parasites were determined as described previously for members of the subgenus Sauroleishmania [ 14 ]: (i) long nectomonad promastigotes (body length ≥ 14 μm); (ii) short nectomonad promastigotes (body length < 14 μm and flagella length < 2-fold the body length); (iii) metacyclic-like promastigotes (body length < 14 μm and flagella length ≥ 2-fold body length); (iv) amastigote-like forms; and (v) haptomonad promastigotes. Differences in number of metacyclic-like stages were tested by the Chi-square ( χ 2 ) tests using SPSS software version 27 (SPSS IBM Corp.).…”

“…Sand flies of the genus Sergentomyia , which feed preferentially on cold-blooded animals, are generally accepted as the vectors of Sauroleishmania [ 12 ]. However, it has been reported that some Sauroleishmania species can cause late-stage infections in Phlebotomus sand flies; consequently, their possible involvement in Sauroleishmania transmission should also be considered [ 13 , 14 ].…”

“…In the sand fly intestinal tract, the parasites initially multiply as promastigotes within the blood meal surrounded by a peritrophic matrix. Once the peritrophic matrix is broken, promastigotes migrate into various parts of the sand fly gut [ 14 , 15 ] and, according to the description of Lainson and Shaw [ 16 ], undergo either hypopylarian, peripylarian or suprapylarian types of development. Hypopylarian development is confined to the hindgut (pylorus and rectum) and is considered typical of Leishmania ( Sauroleishmania [ S .])…”

Porcisia transmission by prediuresis of sand flies

“…In the dixenous Leishmania genus, three types of development have been recognized: suprapylarian development, typical of the subgenus Leishmania , is restricted to the mesenteron; peripylarian development, known in the subgenus Viannia and some Sauroleishmania species, also involves multiplication in the hindgut prior to the anterior migration and colonization of the stomodeal valve; and finally, hypopylarian development in other Sauroleishmania species is restricted to the hind gut ( Lainson and Shaw, 1987 ). Occurrence of low numbers of Leishmania promastigotes in MT, reported in natural or experimental infections, has been interpreted as a consequence of peristaltic backwash from the midgut ( Lainson and Shaw, 1968 ) and invasion of MT by Leishmania has been more frequently observed in unnatural vector- parasite pairs or atypical experimental conditions like maltose or fructose diet and reduced temperature ( Rangel et al., 1985 ; Walters et al., 1987 ; Anez et al., 1989 ; Nieves and Pimenta, 2000 ; Ticha et al., 2021 ). In the dixenous genus Endotrypanum , which is closely relative to Porcisia , development in MT has been observed more frequently than in Leishmania , but in variable proportion in different sand fly species and in a lower percentage of females compared with midgut infections ( Shaw, 1981 ; Franco et al., 1997 ).…”