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Genomic analysis of two phlebotomine sand fly vectors of Leishmania from the New and Old World.

ABSTRACT: Phlebotomine sand flies are of global significance as important vectors of human disease, transmitting bacterial, viral, and protozoan pathogens, including the kinetoplastid parasites of the genus Leishmania, the causative agents of devastating diseases collectively termed leishmaniasis. More than 40 pathogenic Leishmania species are transmitted to humans by approximately 35 sand fly species in 98 countries with hundreds of millions of people at risk around the world. No approved efficacious vaccine exists for leishmaniasis and available therapeutic drugs are either toxic and/or expensive, or the parasites are becoming resistant to the more recently developed drugs. Therefore, sand fly and/or reservoir control are currently the most effective strategies to break transmission. To better understand the biology of sand flies, including the mechanisms involved in their vectorial capacity, insecticide resistance, and population structures we sequenced the genomes of two geographically widespread and important sand fly vector species: Phlebotomus papatasi, a vector of Leishmania parasites that cause cutaneous leishmaniasis, (distributed in Europe, the Middle East and North Africa) and Lutzomyia longipalpis, a vector of Leishmania parasites that cause visceral leishmaniasis (distributed across Central and South America). We categorized and curated genes involved in processes important to their roles as disease vectors, including chemosensation, blood feeding, circadian rhythm, immunity, and detoxification, as well as mobile genetic elements. We also defined gene orthology and observed micro-synteny among the genomes. Finally, we present the genetic diversity and population structure of these species in their respective geographical areas. These genomes will be a foundation on which to base future efforts to prevent vector-borne transmission of Leishmania parasites.

SUBMITTER: Labbe F

PROVIDER: S-EPMC10138862 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Genomic analysis of two phlebotomine sand fly vectors of Leishmania from the New and Old World.

Labbé Frédéric F Abdeladhim Maha M Abrudan Jenica J Araki Alejandra Saori AS Araujo Ricardo N RN Arensburger Peter P Benoit Joshua B JB Brazil Reginaldo Pecanha RP Bruno Rafaela V RV Bueno da Silva Rivas Gustavo G Carvalho de Abreu Vinicius V Charamis Jason J Coutinho-Abreu Iliano V IV da Costa-Latgé Samara G SG Darby Alistair A Dillon Viv M VM Emrich Scott J SJ Fernandez-Medina Daniela D Figueiredo Gontijo Nelder N Flanley Catherine M CM Gatherer Derek D Genta Fernando A FA Gesing Sandra S Giraldo-Calderón Gloria I GI Gomes Bruno B Aguiar Eric Roberto Guimaraes Rocha ERGR Hamilton James G C JGC Hamarsheh Omar O Hawksworth Mallory M Hendershot Jacob M JM Hickner Paul V PV Imler Jean-Luc JL Ioannidis Panagiotis P Jennings Emily C EC Kamhawi Shaden S Karageorgiou Charikleia C Kennedy Ryan C RC Krueger Andreas A Latorre-Estivalis José M JM Ligoxygakis Petros P Meireles-Filho Antonio Carlos A ACA Minx Patrick P Miranda Jose Carlos JC Montague Michael J MJ Nowling Ronald J RJ Oliveira Fabiano F Ortigão-Farias João J Pavan Marcio G MG Horacio Pereira Marcos M Nobrega Pitaluga Andre A Proveti Olmo Roenick R Ramalho-Ortigao Marcelo M Ribeiro José M C JMC Rosendale Andrew J AJ Sant'Anna Mauricio R V MRV Scherer Steven E SE Secundino Nágila F C NFC Shoue Douglas A DA da Silva Moraes Caroline C Gesto João Silveira Moledo JSM Souza Nataly Araujo NA Syed Zainulabueddin Z Tadros Samuel S Teles-de-Freitas Rayane R Telleria Erich L EL Tomlinson Chad C Traub-Csekö Yara M YM Marques João Trindade JT Tu Zhijian Z Unger Maria F MF Valenzuela Jesus J Ferreira Flávia V FV de Oliveira Karla P V KPV Vigoder Felipe M FM Vontas John J Wang Lihui L Weedall Gareth D GD Zhioua Elyes E Richards Stephen S Warren Wesley C WC Waterhouse Robert M RM Dillon Rod J RJ McDowell Mary Ann MA

PLoS neglected tropical diseases 20230412 4

Phlebotomine sand flies are of global significance as important vectors of human disease, transmitting bacterial, viral, and protozoan pathogens, including the kinetoplastid parasites of the genus Leishmania, the causative agents of devastating diseases collectively termed leishmaniasis. More than 40 pathogenic Leishmania species are transmitted to humans by approximately 35 sand fly species in 98 countries with hundreds of millions of people at risk around the world. No approved efficacious vac ...[more]

PMID: 37043542

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Project description:BackgroundThe recent geographical expansion of phlebotomine vectors of Leishmania infantum in the Mediterranean subregion has been attributed to ongoing climate changes. At these latitudes, the activity of sand flies is typically seasonal; because seasonal phenomena are also sensitive to general variations in climate, current phenological data sets can provide a baseline for continuing investigations on sand fly population dynamics that may impact on future scenarios of leishmaniasis transmission. With this aim, in 2011-2013 a consortium of partners from eight Mediterranean countries carried out entomological investigations in sites where L. infantum transmission was recently reported.Methods/principal findingsA common protocol for sand fly collection included monthly captures by CDC light traps, complemented by sticky traps in most of the sites. Collections were replicated for more than one season in order to reduce the effects of local weather events. In each site, the trapping effort was left unchanged throughout the survey to legitimate inter-seasonal comparisons. Data from 99,000 collected specimens were analyzed, resulting in the description of seasonal dynamics of 56,000 sand flies belonging to L. infantum vector species throughout a wide geographical area, namely P. perniciosus (Portugal, Spain and Italy), P. ariasi (France), P. neglectus (Greece), P. tobbi (Cyprus and Turkey), P. balcanicus and P. kandelakii (Georgia). Time of sand fly appearance/disappearance in collections differed between sites, and seasonal densities showed variations in each site. Significant correlations were found between latitude/mean annual temperature of sites and i) the first month of sand fly appearance, that ranged from early April to the first half of June; ii) the type of density trend, varying from a single peak in July/August to multiple peaks increasing in magnitude from May through September. A 3-modal trend, recorded for P. tobbi in Cyprus, represents a novel finding for a L. infantum vector. Adults ended the activity starting from mid September through November, without significant correlation with latitude/mean annual temperature of sites. The period of potential exposure to L.infantum in the Mediterranean subregion, as inferred by adult densities calculated from 3 years, 37 sites and 6 competent vector species, was associated to a regular bell-shaped density curve having a wide peak center encompassing the July-September period, and falling between early May to late October for more than 99% of values. Apparently no risk for leishmaniasis transmission took place from December through March in the years considered. We found a common pattern of nocturnal females activity, whose density peaked between 11 pm and 2 am.ConclusionsDespite annual variations, multiple collections performed over consecutive years provided homogeneous patterns of the potential behavior of leishmaniasis vectors in selected sites, which we propose may represent sentinel areas for future monitoring. In the investigated years, higher potential risk for L. infantum transmission in the Mediterranean was identified in the June-October period (97% relative vector density), however such risk was not equally distributed throughout the region, since density waves of adults occurred earlier and were more frequent in southern territories.

Project description:BackgroundPhlebotomine sand flies are known to transmit Leishmania parasites, bacteria and viruses that affect humans and animals in many countries worldwide. Precise sand fly identification is essential to prevent phlebotomine-borne diseases. Over the past two decades, progress in matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) has emerged as an accurate tool for arthropod identification. The objective of the present study was to investigate the usefulness of MALDI-TOF MS as a tool for identifying field-caught phlebotomine.Methodology/principal findingsSand flies were captured in four sites in north Algeria. A subset was morphologically and genetically identified. Six species were found in these areas and a total of 28 stored frozen specimens were used for the creation of the reference spectrum database. The relevance of this original method for sand fly identification was validated by two successive blind tests including the morphological identification of 80 new specimens which were stored at -80°C, and 292 unknown specimens, including engorged specimens, which were preserved under different conditions. Intra-species reproducibility and inter-species specificity of the protein profiles were obtained, allowing us to distinguish specimens at the gender level. Querying of the sand fly database using the MS spectra from the blind test groups revealed concordant results between morphological and MALDI-TOF MS identification. However, MS identification results were less efficient for specimens which were engorged or stored in alcohol. Identification of 362 phlebotomine sand flies, captured at four Algerian sites, by MALDI-TOF MS, revealed that the subgenus Larroussius was predominant at all the study sites, except for in M'sila where P. (Phlebotomus) papatasi was the only sand fly species detected.ConclusionThe present study highlights the application of MALDI-TOF MS for monitoring sand fly fauna captured in the field. The low cost, reliability and rapidity of MALDI-TOF MS analyses opens up new ways in the management of phlebotomine sand fly-borne diseases.

Project description:BackgroundPhlebotomine sand flies are blood-feeding insects of great medical and veterinary significance acting as vectors of Leishmania parasites. Studying the blood-feeding pattern of these insects may help in the understanding of their interactions with potential reservoir hosts of Leishmania parasites. In this study, we developed real time PCR assays for the identification of sand fly blood meal.MethodsSix pairs of primers were designed based on cytochrome b gene sequences available in GenBank of the following potential hosts: dog, cat, horse, chicken, black rat, and human. Firstly, SYBR Green-based real time PCR assays were conducted using a standard curve with eight different concentrations (i.e., 10 ng, 1 ng, 100 pg, 10 pg, 1 pg, 100 fg, 10 fg and 1 fg per 2 μl) of DNA samples extracted from EDTA blood samples from each target animal. Then, DNA samples extracted from field-collected engorged female sand flies belonging to three species (i.e., Lutzomyia longipalpis, L. migonei and L. lenti) were tested by the protocols standardized herein. Additionally, female sand flies were experimentally fed on a black rat (Rattus rattus) and used for evaluating the time course of the detection of the protocol targeting this species.ResultsThe protocols performed well with detection limits of 10 pg to 100 fg. Field-collected female sand flies were fed on blood from humans (73%), chickens (23%), dogs (22%), horses (15%), black rats (11%) and cats (2%). Interestingly, 76.1% of the L. longipalpis females were positive for human blood. In total, 48% of the tested females were fed on single sources, 31% on two and 12% on three. The analysis of the time course showed that the real time PCR protocol targeting the black rat DNA was able to detect small amounts of the host DNA up to 5 days after the blood meal.ConclusionsThe real time PCR assays standardized herein successfully detected small amounts of host DNA in female sand flies fed on different vertebrate species and, specifically for the black rats, up to 5 days after the blood meal. These assays represent promising tools for the identification of blood meal in field-collected female sand flies.

Dataset Information

Genomic analysis of two phlebotomine sand fly vectors of Leishmania from the New and Old World.

Publications

Genomic analysis of two phlebotomine sand fly vectors of Leishmania from the New and Old World.

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