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.

Department of Infectious Diseases Unit of Vector Borne Diseases Istituto Superiore di Sanità Viale Regina Elena 299 00161 Rome Italy

Department of Parasitology Faculty of Science Charles University Vinicna 7 12800 Prague Czech Republic

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Espinosa O.A., Serrano M.G., Camargo E.P., Teixeira M.M.G., Shaw J.J. An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology. 2016;145:430–442. doi: 10.1017/S0031182016002092. PubMed DOI

Ranque P. Ph.D. Thesis. Université d’Aix-Marseille II; Marseille, France: Apr 28, 1973. Étude morphologique et biologique de quelques Trypanosomidés récoltés au Sénégal. .

Saf’janova V.M. The Leishmanias; Protozoology, Academy of Sciences. Volume 7. USSR All Union Society of Protozoologists; Leningrad, Russia: 1982. The problem of taxonomy with Leishmania; pp. 95–101.

Killick-Kendrick R., Lainson R., Rioux J.A., Saf’janova V.M. The taxonomy of Leishmania-like parasites of reptiles. In: Rioux J.A., editor. Leishmania: Taxonomie et Phylogenèse. Applications Eco-epidéemiologiques (Colloque international du CNRS/INSERM, 1984), IMEE; Montpelier, France: 1986. pp. 143–148.

Akhoundi M., Kuhls K., Cannet A., Votypka J., Marty P., Delaunay P., Sereno D. A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl. Trop. Dis. 2016;10:e0004349. doi: 10.1371/journal.pntd.0004349. PubMed DOI PMC

Noyes H. Implications of a Neotropical origin of the genus Leishmania. Memórias do Instituto Oswaldo Cruz. 1998;93:657–662. doi: 10.1590/S0074-02761998000500017. PubMed DOI

Klatt S., Simpson L., Maslov D.A., Konthur Z. Leishmania tarentolae: Taxonomic classification and its application as a promising biotechnological expression host. PLoS Negl. Trop. Dis. 2019;13:e0007424. doi: 10.1371/journal.pntd.0007424. PubMed DOI PMC

Belova E.M. Reptiles and their importance in the epidemiology of leishmaniasis. Bull. World Health Organ. 1971;44:553–560. PubMed PMC

Wilson V.C.L.C., Southgate B.A. Lizard Leishmania. In: Lumsden W.H.R., Evans D.A., editors. Biology of the Kinetoplastida. Volume 2. Academic Press; London, UK: 1979. pp. 241–268.

Adler S. The behaviour of a lizard Leishmania in hamsters and baby mice. Rev. Do Inst. De Med. Trop. De Sao Paulo. 1962;4:61–64. PubMed

Breton M., Tremblay M.J., Ouellette M., Papadopoulou B. Live nonpathogenic parasitic vector as a candidate vaccine against visceral leishmaniasis. Infect. Immun. 2005;73:6372–6382. doi: 10.1128/IAI.73.10.6372-6382.2005. PubMed DOI PMC

Taylor V.M., Munoz D.L., Cedeno D.L., Velez I.D., Jones M.A., Robledo S.M. Leishmania tarentolae: Utility as an in vitro model for screening of antileishmanial agents. Exp. Parasitol. 2010;126:471–475. doi: 10.1016/j.exppara.2010.05.016. PubMed DOI

Novo S.P., Leles D., Bianucci R., Araujo A. Leishmania tarentolae molecular signatures in a 300 hundred-years-old human Brazilian mummy. Parasites Vectors. 2015;8:72. doi: 10.1186/s13071-015-0666-z. PubMed DOI PMC

Coughlan S., Mulhair P., Sanders M., Schonian G., Cotton J.A., Downing T. The genome of Leishmania adleri from a mammalian host highlights chromosome fission in Sauroleishmania. Sci. Rep. 2017;7:1–13. doi: 10.1038/srep43747. PubMed DOI PMC

Mendoza-Roldan J.A., Latrofa M.S., Iatta R., Manoj R.R.S., Panarese R., Annoscia G., Pombi M., Zatelli A., Beugnet F., Otranto D. Detection of Leishmania tarentolae in lizards, sand flies and dogs in southern Italy, where Leishmania infantum is endemic: Hindrances and opportunities. Parasites Vectors. 2021;14:461. doi: 10.1186/s13071-021-04973-2. PubMed DOI PMC

Pombi M., Giacomi A., Barlozzari G., Mendoza-Roldan J.A., Macrì G., Otranto D., Gabrielli S. Molecular detection of Leishmania (Sauroleishmania) tarentolae in human blood and Leishmania (Leishmania) infantum in Sergentomyia minuta: Unexpected host-parasite contacts. Med. Vet. Entomol. 2020;34:470–475. doi: 10.1111/mve.12464. PubMed DOI

Telford S.R. Hemoparasites of the Reptilia. Volume 1. CRC Press; Boca Raton, FL, USA: 2009. pp. 311–376. Color Atlas and Text.

Maroli M., Gramiccia M., Gradoni L., Ready P.D., Smith D.F., Aquino C. Natural infections of phlebotomine sandflies with Trypanosomatidae in central and south Italy. Trans. R. Soc. Trop. Med. Hyg. 1988;82:227–228. doi: 10.1016/0035-9203(88)90421-X. PubMed DOI

Quate L.W. Phlebotomus sandflies of the Paloich area in the Sudan (Diptera, Psychodidae) J. Med Entomol. 1964;1:213–268. doi: 10.1093/jmedent/1.3.213. PubMed DOI

Mutinga M.J., Ngoka J.M. Suspected vectors of lizard leishmaniasis in Kenya and their possible role in partial immunization of the human populationl against Leishmania donovani in kala-azar endemic areas. Int. J. Trop. Insect Sci. 1981;1:207–210. doi: 10.1017/S1742758400000412. DOI

Adler S., Theodor O. Observations on Leishmania ceramodactyli n. sp. Trans. R. Soc. Trop. Med. Hyg. 1929;22:343–355. doi: 10.1016/S0035-9203(29)90025-0. DOI

Lainson R., Shaw J.J. Evolution, classification and geographical distribution. In: Peters W., Killick-Kendrick R., editors. The Leishmaniases in Biology and Medicine. Volume 1. Academic Press; Cambridge, MA, USA: 1987. pp. 1–120.

Adler S., Theodor O. Investigation on Mediterranean kala azar X—A note on Trypanosoma platydactyli and Leishmania tarentolae. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 1935;116:543–544. doi: 10.1098/rspb.1935.0008. DOI

Heisch R.B. On Leishmania adleri sp. nov. from lacertid lizards (Latastia sp.) in Kenya. Ann. Trop. Med. Parasitol. 1985;52:68–71. doi: 10.1080/00034983.1958.11685846. PubMed DOI

Killick-Kendrick R. Biology of Leishmania in phlebotomine sandflies. In: Lumsden W.H.R., Evans D.A., editors. Biology of the Kinetoplastida. Volume 2. Academic Press; London, UK: 1979. pp. 395–460.

Bates P.A. Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. Int. J. Parasitol. 2007;37:1097–1106. doi: 10.1016/j.ijpara.2007.04.003. PubMed DOI PMC

Wenyon C.M. Observations on the intestinal protozoa of three Egyptian lizards, with a note on a cell-invading fungus. Parasitology. 1921;12:350–365. doi: 10.1017/S0031182000014347. DOI

Wallbanks K.R., Maazoun R., Canning E.U., Rioux J.A. The identity of Leishmania tarentolae Wenyon 1921. Parasitology. 1985;90:67–78. doi: 10.1017/S0031182000049027. PubMed DOI

Pozio E., Gramiccia M., Gradoni L., Maroli M. Hémoflagellés de Tarentola mauritanica L., 1758 (Reptilia, Gekkonidae) In: Rioux J.A., editor. Leishmania. Taxonomie et phylogenèse. IMEEE; Montpellier, France: 1986. pp. 149–155.

Rioux J.A., Knoepfler L.P., Martini A., Callot J., Kremer M. Présence en France de Leishmania tarentolae Wenyon, 1921. Parasite du gecko Tarentola mauritanica (L. 1758) Ann. De Parasitol. Hum. Et Comparée. 1969;44:115–118. doi: 10.1051/parasite/1969441115. DOI

Pozio E., Gramiccia M., Gradoni L., Maroli M. Hemoflagellates in Cyrtodactylus kotschyi (Steindachner, 1870) (Reptilia, Gekkonidae) in Italy. Acta Trop. 1983;40:399–400. PubMed

Elwasila M. Leishmania tarentolae Wenyon, 1921 from the gecko Tarentola annularis in the Sudan. Parasitol. Res. 1988;74:591–592. doi: 10.1007/BF00531640. PubMed DOI

Bongiorno G., Di Muccio T., Gradoni L., Giacomi A., Pombi M., Gabrielli S., Gramiccia M. Natural infections of Sergentomyia minuta with kinetoplastid flagellates detected by gold standard methods in Rome province; Proceedings of the XXXI Congresso SoIPa & 2021 ESDA EVENT; Teramo, Italy. 16–19 June 2021; p. 230.

Di Muccio T., Scalone A., Bruno A., Marangi M., Grande R., Armignacco O., Gradoni L., Gramiccia M. Epidemiology of Imported Leishmaniasis in Italy: Implications for a European Endemic Country. PLoS ONE. 2015;10:e0129418. doi: 10.1371/journal.pone.0129418. PubMed DOI PMC

Diamond L.S., Herman C.M. Incidence of trypanosomes in the Canada goose as revealed by bone marrow culture. J. Parasitol. 1954;40:195–202. doi: 10.2307/3274299. DOI

Volf P., Volfova V. Establishment and maintenance of sand fly colonies. J. Vector Ecol. 2011;36:1–9. doi: 10.1111/j.1948-7134.2011.00106.x. PubMed DOI

Myskova J., Votypka J., Volf P. Leishmania in sand flies: Comparison of quantitative polymerase chain reaction with other techniques to determine the intensity of infection. J. Med. Entomol. 2008;45:133–138. doi: 10.1093/jmedent/45.1.133. PubMed DOI

Killick-Kendrick R. The life-cycle of Leishmania in the sandfly with special reference to the form infective to the vertebrate host. Ann. De Parasitol. Hum. Et Comparée. 1990;65:37–42. doi: 10.1051/parasite/1990651037. PubMed DOI

Sadlova J., Price H.P., Smith B.A., Votypka J., Volf P., Smith D.F. The stage-regulated HASPB and SHERP proteins are essential for differentiation of the protozoan parasite Leishmania major in its sand fly vector, Phlebotomus papatasi. Cell. Microbiol. 2010;12:1765–1779. doi: 10.1111/j.1462-5822.2010.01507.x. PubMed DOI PMC

Blum B., Bakalara N., Simpson L. A model for RNA editing in kinetoplastid mitochondria: RNA molecules transcribed from maxicircle DNA provide the edited information. Cell. 1990;60:189–198. doi: 10.1016/0092-8674(90)90735-W. PubMed DOI

Aphasizhev R., Aphasizheva I., Nelson R.E., Gao G., Simpson A.M., Kang X., Falick A.M., Sbicego S., Simpson L. Isolation of a U-insertion/deletion editing complex from Leishmania tarentolae mitochondria. EMBO J. 2003;22:913–924. doi: 10.1093/emboj/cdg083. PubMed DOI PMC

Aphasizhev R., Aphasizheva I. Mitochondrial RNA editing in trypanosomes: Small RNAs in control. Biochimie. 2013;100:125–131. doi: 10.1016/j.biochi.2014.01.003. PubMed DOI PMC

Abdossamadi Z., Taheri T., Seyed N., Montakhab-Yeganeh H., Zahedifard F., Taslimi Y., Habibzadeh S., Gholami E., Gharibzadeh A., Rafati S. Live Leishmania tarentolae secreting HNP1 as an immunotherapeutic tool against Leishmania infection in BALB/c mice. Immunotherapy. 2017;9:1089–1102. doi: 10.2217/imt-2017-0076. PubMed DOI

Montakhab-Yeganeh H., Abdossamadi Z., Zahedifard F., Taslimi Y., Badirzadeh A., Saljoughian N., Taheri T., Taghikhani M., Rafati S. Leishmania tarentolae expressing CXCL-10 as an efficient immunotherapy approach against Leishmania major-infected BALB/c mice. Parasite Imunol. 2017;39:e12461. doi: 10.1111/pim.12461. PubMed DOI

Pimenta P.F.P., Saraiva E.M., Rowton E., Modi G.B., Garraway L.A., Beverley S.M., Turco S.J., Sacks D.L. Evidence that the vectorial competence of phlebotomine sand flies for different species of Leishmania is controlled by structural polymorphisms in the surface lipophosphoglycan. Proc. Natl. Acad. Sci. USA. 1994;91:9155–9159. doi: 10.1073/pnas.91.19.9155. PubMed DOI PMC

Chajbullinova A., Votypka J., Sadlova J., Kvapilova K., Seblova V., Kreisinger J., Jirku M., Sanjoba C., Gantuya S., Matsumoto Y., et al. The development of Leishmania turanica in sand flies and competition with L. major. Parasites Vectors. 2012;5:219. doi: 10.1186/1756-3305-5-219. PubMed DOI PMC

Svobodova M., Sadlova J., Chang K.P., Volf P. Distribution and feeding preference of the sand flies Phlebotomus sergenti and P. papatasi in a cutaneous leishmaniasis focus in Sanliurfa, Turkey. Am. J. Trop. Med. Hyg. 2003;68:6–9. doi: 10.4269/ajtmh.2003.68.6. PubMed DOI

Palit A., Bhattacharya S.K., Kundu S.N. Host preference of Phlebotomus argentipes and Phlebotomus papatasi in different biotopes of West Bengal, India. Int. J. Environ. Health Res. 2005;15:449–454. doi: 10.1080/09603120500392525. PubMed DOI

McMillan B. Leishmaniasis in the Sudan Republic. 22. Leishmania hoogstraali sp. n. in the gecko. J. Parasitol. 1965;51:336–339. doi: 10.2307/3275947. PubMed DOI

Kamhawi S., Modi G.B., Pimenta P.F.P., Rowton E., Sacks D.L. The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology. 2000;121:25–33. doi: 10.1017/S0031182099006125. PubMed DOI

Maroli M., Jalouk L., Al Ahmed M., Bianchi R., Bongiorno G., Khoury C., Gradoni L. Aspects of the bionomics of Phlebotomus sergenti sandflies from an endemic area of anthroponotic cutaneous leishmaniasis in Aleppo Governorate, Syria. Med. Vet. Entomol. 2009;23:148–154. doi: 10.1111/j.1365-2915.2009.00808.x. PubMed DOI

Maroli M., Gramiccia M., Gradoni L., Troiani M., Ascione R. Natural infection of Phlebotomus perniciosus with MON 72 zymodeme of Leishmania infantum in the Campania region of Italy. Acta Trop. 1994;57:333–335. doi: 10.1016/0001-706X(94)90079-5. PubMed DOI

Volf P., Myskova J. Sand flies and Leishmania: Specific versus permissive vectors. Trends Parasitol. 2007;23:91–92. doi: 10.1016/j.pt.2006.12.010. PubMed DOI PMC

Bongiorno G., Habluetzel A., Khoury C., Maroli M. Host preferences of phlebotomine sand flies at a hypoendemic focus of canine leishmaniasis in central Italy. Acta Trop. 2003;88:109–116. doi: 10.1016/S0001-706X(03)00190-6. PubMed DOI

Rossi E., Bongiorno G., Ciolli E., Di Muccio T., Scalone A., Gramiccia M., Gradoni L., Maroli M. Seasonal phenology, host-blood feeding preferences and natural Leishmania infection of Phlebotomus perniciosus (Diptera, Psychodidae) in a high-endemic focus of canine leishmaniasis in Rome province, Italy. Acta Trop. 2008;105:158–165. doi: 10.1016/j.actatropica.2007.10.005. PubMed DOI

Remadi L., Chargui N., Jimenez M., Molina R., Haouas N., González E., Chaabane-Banaouas R., Salah E.B., Haddaji M., Chaabouni Y., et al. Molecular detection and identification of Leishmania DNA and blood meal analysis in Phlebotomus (Larroussius) species. PLoS Negl. Trop. Dis. 2020;14:e0008077. doi: 10.1371/journal.pntd.0008077. PubMed DOI PMC

Bettini S., Gramiccia M., Gradoni L., Atzeni M.C. Leishmaniasis in Sardinia: II. Natural infection of Phlebotomus perniciosus Newstead 1911, by Leishmania infantum Nicolle 1908, in the province of Cagliari. Trans. R. Soc. Trop. Med. Hyg. 1986;80:458–459. doi: 10.1016/0035-9203(86)90344-5. PubMed DOI

Bongiorno G., Lisi O., Severini F., Vaccalluzzo V., Khoury C., Di Muccio T., Gradoni L., Maroli M., D’Urso V., Gramiccia M. Investigations on sand fly bionomics and Leishmania natural infections in Eastern Sicily, Italy, with particular reference to Phlebotomus sergenti; Proceedings of the VIII International Symposium on Phlebotomine Sandflies; Puerto Iguazu, Argentina. 22–25 September 2014; id 45-O.

Latrofa M.S., Mendoza-Roldan J.A., Manoj R., Dantas-Torres F., Otranto D. A duplex real-time PCR assay for the detection and differentiation of Leishmania infantum and Leishmania tarentolae in vectors and potential reservoir hosts. Entomol. Gen. 2021 doi: 10.1127/entomologia/2021/1178. DOI

Franco A.M.R., Tesh R.B., Guzman H., Deane M.P., Grimaldi G., Jr. Development of Endotrypanum (Kinetoplastida: Trypanosomatidae) in experimentally infected phlebotomine sand flies (Diptera: Psychodidae) J. Med Entomol. 1997;34:189–192. doi: 10.1093/jmedent/34.2.189. PubMed DOI

McConville M.J., Turco S.J., Ferguson M.A., Sacks D.L. Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J. 1992;11:3593–3600. doi: 10.1002/j.1460-2075.1992.tb05443.x. PubMed DOI PMC

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