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      Genetic tools discriminate strains of Leishmania infantum isolated from  humans and dogs in Sicily, Italy

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          Abstract

          Background

          Leishmaniasis is one of the most important vector-borne diseases and it represents a serious world health problem affecting millions of people. High levels of Leishmania infections, affecting both humans and animals, are recognized among Italian regions. Among these, Sicily has one of the highest prevalence of Leishmania infection.

          Methodology/Principal Findings

          Seventy-eight Leishmania strains isolated from human and animal samples across Sicily, were analyzed for the polymorphic k26-gene and genotypes were assigned according to the size of the PCR products. A multilocus microsatellite typing (MLMT) approach based on the analysis of 11 independent loci was used to investigate populations structure and genetic diversity of the isolated strains. Six L. infantum reference strains were included in the analysis for comparison. Bayesian clustering analysis of microsatellite data showed that all the isolated strains clustered in two genetically distinct populations, corresponding to human and canine isolates respectively. A further subdivision was observed between the two main groups, giving a good correlation between human strains and their geographic origin, conversely canine population showed a great genetic variability diffused in the territory.

          Conclusions/Significance

          Among the 78 Leishmania isolates, K26 analysis detected 71 samples (91%) as MON-1 zymodeme, confirming it as the predominant strain in Mediterranean area and 7 human samples (9%) as non-MON-1. MLMT gives important insights into the epidemiology of leishmaniases and allows characterization of different strains to a higher resolution than possible with zymodeme typing. Two main populations presented a strong correlation respect to the different hosts, exhibiting a co-circulation of two distinct populations of L. infantum. The population found in infected humans exhibited a correlation with geographic origin. These clusters could represent a geographically restricted population of strains with the same or related genotypes. This study can contribute to an understanding of Leishmania epidemiology, including the spread of reservoirs and sand fly vectors in the different foci of infection, characterizing parasites within the different hosts.

          Author summary

          High levels of Leishmania spp. infections affecting both humans and animals are recognized among Italian regions; in particular, Sicily is an endemic area for Leishmania infantum. In this study 78 Sicilian L. infantum strains isolated from humans and dogs were assessed to investigate their biodiversity by genetic tools. Results were compared with 6 L. infantum reference strains included in the analysis. The evaluation of K26 genetic markers identified 91% of samples as belonging to the MON-1 zymodeme, confirming it as the predominant strain in the Mediterranean area and 9% of the samples–all isolated from humans–as non-MON-1. Multilocus microsatellite typing has proven to be a powerful tool to discriminate strains showing all the isolated strains clustered in two genetically distinct populations, corresponding to human and canine isolates, respectively. A further subdivision was observed between the two main groups, giving in the human population a correlation between microsatellite profile and geographical origin. Our results demonstrate that genetic tools are able to discriminate Leishmania strains and to give useful insights into the epidemiology of leishmaniasis, raising questions on the role of dogs as main reservoirs for human leishmaniasis in the Sicily region.

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          Most cited references33

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          Microsatellite mutations in the germline: implications for evolutionary inference.

          Microsatellite DNA sequences mutate at rates several orders of magnitude higher than that of the bulk of DNA. Such high rates mean that spontaneous mutations that form new-length variants can realistically be seen in pedigree analysis. Data on observed mutation events from various organisms are now accumulating, allowing inferences on DNA sequence evolution to be made through an unusually direct approach. Here I discuss and integrate microsatellite mutation data in an evolutionary context. A striking feature of the mutation process is that it seems highly heterogeneous, with distinct differences between species, repeat types, loci and alleles. Age and sex also affect the mutation rate. Within genomes at equilibrium, the microsatellite-length distribution is a delicate balance between biased mutation processes and point mutations acting towards the decay of repetitive DNA. Indeed, simple repeats do not evolve simply.
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            Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector.

            Genetic exchange has not been shown to be a mechanism underlying the extensive diversity of Leishmania parasites. We report here evidence that the invertebrate stages of Leishmania are capable of having a sexual cycle consistent with a meiotic process like that described for African trypanosomes. Hybrid progeny were generated that bore full genomic complements from both parents, but kinetoplast DNA maxicircles from one parent. Mating occurred only in the sand fly vector, and hybrids were transmitted to the mammalian host by sand fly bite. Genetic exchange likely contributes to phenotypic diversity in natural populations, and analysis of hybrid progeny will be useful for positional cloning of the genes controlling traits such as virulence, tissue tropism, and drug resistance.
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              Taxonomy of Leishmania. Use of isoenzymes. Suggestions for a new classification.

              The authors propose a new classification for the genus Leishmania Ross, 1903 based both on the use of intrinsic and extrinsic characters and on Linnean and Adansonian methods. The type of vertebrate host makes it possible to recognize the genus group: Leishmania designates Kinetoplastida parasites of mammals. Neighbouring forms which parasite reptiles are now grouped in the genus Sauroleishmania Ranque, 1973. Characteristics of the intravectorial cycle (supra- and peri-pyloric) are used to define the subgenus group (Leishmania, Viannia Lainson and Shaw, 1987). The classification uses biochemical, particularly enzymatic, characters. Elementary taxonomic units are made up of all the strains having the same isoenzyme profile, i.e. the zymodeme. The grouping of the zymodemes is usually performed through automatic techniques which lead to bush-like trees (dendrograms) showing either simple affinities between units (phenograms) or their phyletic relationships (cladograms). The branches recognized as being stable are individualized as "zymodeme complexes". They bear the name of either the previously defined species taxa or that of a specially created one. Two examples of taxonomic constructions, phenetic and cladistic, are presented. Finally, a general classification of the genus is proposed.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: Validation
                Role: Data curationRole: MethodologyRole: SupervisionRole: Visualization
                Role: InvestigationRole: SoftwareRole: ValidationRole: Writing – original draft
                Role: InvestigationRole: Methodology
                Role: ValidationRole: Visualization
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: SoftwareRole: SupervisionRole: Writing – original draft
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                24 July 2020
                July 2020
                : 14
                : 7
                : e0008465
                Affiliations
                [1 ] National Reference Center for Leishmaniasis (C.Re.Na.L.), Istituto Zooprofilattico Sperimentale della Sicilia, Palermo, Italy
                [2 ] Section of Dermatology, Department of Health Promotion, Maternal-Infant, Internal Medicine and Specialization of Excellence “G. D’Alessandro” (PROMISE) University of Palermo, Palermo, Italy.
                [3 ] Tecnologie Diagnostiche Innovative, Istituto Zooprofilattico Sperimentale della Sicilia, Palermo, Italy
                University of Iowa, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-0464-4474
                http://orcid.org/0000-0001-6181-6984
                http://orcid.org/0000-0002-5527-1890
                Article
                PNTD-D-20-00313
                10.1371/journal.pntd.0008465
                7406075
                32706789
                f42ed48f-dced-422f-b778-f08ce7e27a9e
                © 2020 Castelli et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 26 February 2020
                : 9 June 2020
                Page count
                Figures: 5, Tables: 4, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003196, Ministero della Salute;
                Award ID: RC IZS SI 02/18.
                Award Recipient :
                This work is supported by grants from ‘Istituto Zooprofilattico Sperimentale della Sicilia”, Palermo, Italy code number: RC IZS SI 02/18. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Leishmania
                Leishmania Infantum
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Leishmania
                Medicine and Health Sciences
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Leishmaniasis
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Protozoan Infections
                Leishmaniasis
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Zoonoses
                Leishmaniasis
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Biology and Life Sciences
                Genetics
                Population Genetics
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Earth Sciences
                Geography
                Biology and Life Sciences
                Genetics
                Human Genetics
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-08-05
                All relevant data are within the paper and its Supporting Information files. All DNA sequences obtained in the study are available from the GenBank at NCBI (AN: KM677134.1).

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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