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Plant-Feeding Phlebotomine Sand Flies, Vectors of Leishmaniasis, Prefer Cannabis Sativa

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Plant-Feeding Phlebotomine Sand Flies, Vectors of Leishmaniasis, Prefer Cannabis Sativa Plant-feeding phlebotomine sand flies, vectors of leishmaniasis, prefer Cannabis sativa Ibrahim Abbasia,1, Artur Trancoso Lopo de Queirozb,1, Oscar David Kirsteina, Abdelmajeed Nasereddinc, Ben Zion Horwitza, Asrat Hailud, Ikram Salahe, Tiago Feitosa Motab, Deborah Bittencourt Mothé Fragab, Patricia Sampaio Tavares Verasb, David Pochef, Richard Pochef, Aidyn Yeszhanovg, Cláudia Brodskynb, Zaria Torres-Pochef, and Alon Warburga,2 aDepartment of Microbiology and Molecular Genetics, Institute for Medical Research Israel-Canada, The Kuvin Centre for the Study of Infectious and Tropical Diseases, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, 91120, Israel; bInstituto Gonçalo Moniz-Fiocruz Bahia, 40296-710 Salvador, Bahia, Brazil; cGenomics Applications Laboratory, Core Research Facility, Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, 91120, Israel; dCollege of Health Sciences, School of Medicine, Addis Ababa University, Addis Ababa, Ethiopia; eMitrani Department of Desert Ecology, Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion 84990, Israel; fGenesis Laboratories, Inc., Wellington, CO 80549; and gM. Aikimbayev Kazakh Scientific Center of Quarantine and Zoonotic Diseases, A35P0K3 Almaty, Kazakhstan Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved September 25, 2018 (received for review June 17, 2018) Blood-sucking phlebotomine sand flies (Diptera: Psychodidae) trans- obligatory phloem-sucking insects concentrate scarce essential mit leishmaniasis as well as arboviral diseases and bartonellosis. amino acids from phloem by excreting the excess sugary solutions Sand fly females become infected with Leishmania parasites and in the form of honeydew (11). The specific types of sugars and transmit them while imbibing vertebrates’ blood, required as a source their relative concentrations in honeydew can be used to in- of protein for maturation of eggs. In addition, both females and males criminate honeydew consumers (7–9), while the plant sources of consume plant-derived sugar meals as a source of energy. Plant meals phloem-feeding insects can be identified by plant-specific PCR may comprise sugary solutions such as nectar or honeydew (secreted followed by DNA sequencing (12). The utility of PCR-based ap- by plant-sucking homopteran insects), as well as phloem sap that sand proaches for identifying plants consumed by phlebotomine sand flies obtain by piercing leaves and stems with their needle-like mouth- flies has been demonstrated in several studies (13, 14). Most of ECOLOGY parts. Hence, the structure of plant communities can influence the distribution and epidemiology of leishmaniasis. We designed a next- these studies employed the ribulose bisphosphate carboxylase generation sequencing (NGS)–based assay for determining the source large chain (rbcL) gene, which is an accepted marker for phylo- of sand fly plant meals, based upon the chloroplast DNA gene ribulose genetic and barcoding studies of plants (15). bisphosphate carboxylase large chain (rbcL). Here, we report on the State-of-the-art, next-generation sequencing (NGS) is much predilection of several sand fly species, vectors of leishmaniasis in more sensitive than Sanger DNA sequencing and can facilitate different parts of the world, for feeding on Cannabis sativa.Weinfer the acquisition of vast amounts of genomic data, from complex this preference based on the substantial percentage of sand flies that samples, in one reaction mixture (16–19). We developed an had fed on C. sativa plants despite the apparent “absence” of these NGS-based multidetection assay for wild-caught sand flies plants from most of the field sites. We discuss the conceivable impli- designed to identify Leishmania infections, blood and plant cations of the affinity of sand flies for C. sativa on their vectorial meals, as well as characterize their gut microbiome. Here, we capacity for Leishmania and the putative exploitation of their attrac- report on the plant feeding habits of several sand fly species, tion to C. sativa for the control of sand fly-borne diseases. Significance Cannabis sativa | leishmaniasis | next-generation sequencing | phlebotomine sand flies | plant feeding Sand fly females suck blood from vertebrate animals, including humans, and thereby transmit Leishmania parasites and arbo- hlebotomine sand flies (Diptera: Psychodidae) transmit viruses. In addition, both sand fly sexes consume plant-derived Pleishmaniasis, bartonellosis, and several arboviruses that infect sugar meals. Therefore, the structure of plant communities can humans (1, 2). The leishmaniases comprise a group of diseases with influence the transmission dynamics of sand fly-borne diseases. diverse clinical manifestations afflicting millions of humans, typically Our findings demonstrate that, in proportion to their abun- in impoverished regions of the world (3). Only female sand flies feed dance, Cannabis sativa plants were consumed by sand flies on blood, which is required for the maturation of their eggs (1). much more frequently than expected (i.e., C. sativa is probably Consequently, sand fly females contract Leishmania (Kinetoplastida: highly attractive to sand flies). We discuss the conceivable in- Trypanosomatidae) infections when they ingest infected blood and fluence of C. sativa on the transmission of Leishmania and its transmit the parasites during subsequent blood meals. potential utility for sand fly control. In addition to the females consuming blood, both male and female sand flies regularly ingest plant-derived sugar meals as a Author contributions: O.D.K. and A.W. designed research; I.A., O.D.K., A.N., B.Z.H., A.H., source of energy. Because of the dependence of sand flies on plant I.S., T.F.M., D.B.M.F., D.P., R.P., A.Y., C.B., Z.T.-P., and A.W. performed research; P.S.T.V. meals, the structure of plant communities can affect the spatial contributed new reagents/analytic tools; I.A., A.T.L.d.Q., and A.N. analyzed data; and I.A., and temporal distribution of sand fly populations (4). Moreover, A.T.L.d.Q., and A.W. wrote the paper. certain plants upon which sand flies feed can shorten their life or The authors declare no conflict of interest. reduce their capacity for transmitting leishmaniasis (5, 6). This article is a PNAS Direct Submission. Sand fly plant meals may comprise nectar, honeydew, and/or Published under the PNAS license. phloem sap. While nectar and honeydew are readily accessible Data deposition: The sequences reported in this paper have been deposited in the Gen- on the surface of plants, in flowers, and in extrafloral nectaries, Bank database (accession nos. MH733441–MH733473). to reach the phloem, sand flies pierce leaves and stems with their 1I.A. and A.T.L.d.Q. contributed equally to this work. needle-like mouthparts (7–10). 2To whom correspondence should be addressed. Email: [email protected]. Although phloem sap is highly nutritious and generally lacks This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. toxicity, only a restricted range of homopteran insects (Hemiptera: 1073/pnas.1810435115/-/DCSupplemental. Sternorrhyncha) feed exclusively on phloem sap. Some of these www.pnas.org/cgi/doi/10.1073/pnas.1810435115 PNAS Latest Articles | 1of6 Downloaded by guest on October 2, 2021 Tubas, Palestinian authority Kfar Adumim, Judean Desert, Bura, Kazakhstan Phlebotomus sergenti - Phlebotomus sergenti - Phlebotomus mongolensis - Leishmania tropica - Leishmania tropica - Leishmania major - CutaneousCutaneous LeLeishmaniasisishmaniasasis CutaneousCutaneous LeishmaniasisLeishmaniasa is CutaneousCutaneous LeLeishmaniasisishmaniassis Kazakhstan Asia Israel/Palestinian Authority Africa Ethiopia Brazil Camaçari, Bahia, Brazil, Sde Eliyahu, Israel Sheraro,Sh Tigray,Ti EthiopiaEthi i Lutzomyia longipalpis - Phlebotomus papatasi - Phlebotomus orientalis - Leishmania infantum - Leishmania major - Cutaneous Leishmania donovani - Visceral Leishmaniasis Leishmaniasis Visceral Leishmaniasis Fig. 1. Compound scheme comprising a map showing the countries where sand flies were sampled and representative photographs of the sampling sites. The endemic sand fly and Leishmania species, as well as the diseases they cause, are also indicated. The leaf icon denotes the presence of C. sativa DNA in plant-fed sand flies. important vectors of leishmaniasis in different parts of the from 804 sand flies, achieved rbcL amplification in 65 of them, world (Fig. 1). and sequenced the rbcL amplicons from 36 (Table 1 and SI Ap- pendix,Fig.S1). The derived rbcL sequences implicated mostly Results and Discussion common plants such as sesame (Sesamum indicum), the salient crop Initially, we performed laboratory experiments to ascertain that cultivated in that region, as well as various wild tree species from the plant DNA would be detectable in plant-fed sand flies. We per- family Fabaceae. In addition, among the plant-fed sand flies, we formed PCR using primers for rbcL on insectary-reared sand flies were surprised to find four that had consumed Cannabis sativa, that had access (24 h) to freshly cut branches and leaves. Of the which was never observed at the study site (SI Appendix,TableS1). eight flies offered Pistacia lentiscus, 50% (2) of the males and 75% Following these preliminary studies, we developed and began (3) of the females were positive for rbcL compared with 100% using an NGS-based multidetection assay on wild-caught sand flies. (four males and four females)
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