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      Complexity and multi-factoriality of Trypanosoma cruzi sylvatic cycle in coatis, Nasua nasua (Procyonidae), and triatomine bugs in the Brazilian Pantanal

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          Abstract

          Background

          Trypanosoma cruzi is dispersed in nature through many transmission mechanisms among a high diversity of vectors and mammalian species, representing particular behaviors and habitats. Thus, each locality has a unique set of conditions underlying the maintenance of this parasite in the wild. The aim of the present study was to evaluate the life-cycle of T. cruzi in free-ranging coatis from the central region of the Brazilian Pantanal using a multi-factorial approach.

          Methods

          Three methodological blocks were used in the present study: (i) We evaluated T. cruzi infection using serological (ELISA) and parasitological (hemoculture) tests in free-ranging coatis captured from October 2010 to March 2012. In addition, we characterized T. cruzi isolates as DTUs (Discrete Typing Units); (ii) We evaluated Trypanosoma infection in species of Triatoma and Rhodnius inhabiting coati arboreal nests from May to September 2012 using parasitological and molecular assays; and (iii) We analyzed a set of longitudinal data (from 2005 to 2012) concerning the effects of T. cruzi infection on this coati population. Herein, we investigated whether seasonality, host sex, and host age influence T. cruzi prevalence and patterns of infection.

          Results

          The 2010–2012 period presented high seroprevalence on coatis (72.0 % ELISA) and a high percentage of individuals with infectivity competence (20.5 % positive hemoculture). All isolates presented TcI band patterns, occurring in single ( n = 3) and mixed infections (1 TcI/ T. rangeli; 4 with undefined characterization). Both male and female individuals presented the same transmission potential, expressed as positive hemoculture, which was only detected in the summer. However, overall, the data (2005–2012) highlighted the importance of females for T. cruzi maintenance in the winter. Moreover, twenty-three (67.6 %) bugs from five coati nests (71.4 %) were infected with flagellated forms. Seventeen samples were characterized as T. cruzi (TcI and TcIII genotypes).

          Conclusion

          In the Pantanal region, T. cruzi is transmitted in a complex, multifactorial, dynamic and non-linear transmission web. The coati nests might be inserted in this web, acting as important transmission foci at the arboreal stratum to different mammal species with arboreal or scansorial behavior.

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          Most cited references44

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          Molecular Cloning : A Laboratory Manual

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            Mechanism of genetic exchange in American trypanosomes.

            The kinetoplastid Protozoa are responsible for devastating diseases. In the Americas, Trypanosoma cruzi is the agent of Chagas' disease--a widespread disease transmissible from animals to humans (zoonosis)--which is transmitted by exposure to infected faeces of blood-sucking triatomine bugs. The presence of genetic exchange in T. cruzi and in Leishmania is much debated. Here, by producing hybrid clones, we show that T. cruzi has an extant capacity for genetic exchange. The mechanism is unusual and distinct from that proposed for the African trypanosome, Trypanosoma brucei. Two biological clones of T. cruzi were transfected to carry different drug-resistance markers, and were passaged together through the entire life cycle. Six double-drug-resistant progeny clones, recovered from the mammalian stage of the life cycle, show fusion of parental genotypes, loss of alleles, homologous recombination, and uniparental inheritance of kinetoplast maxicircle DNA. There are strong genetic parallels between these experimental hybrids and the genotypes among natural isolates of T. cruzi. In this instance, aneuploidy through nuclear hybridization results in recombination across far greater genetic distances than mendelian genetic exchange. This mechanism also parallels genome duplication.
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              Two hybridization events define the population structure of Trypanosoma cruzi.

              Genetic variation in Trypanosoma cruzi is likely a key determinant in transmission and pathogenesis of Chagas disease. We have examined nine loci as markers for the extant T. cruzi strains. Four distinct alleles were found for each locus, corresponding to the sequence classes present in the homozygous discrete typing units (DTUs) I, IIa, IIb, and IIc. The alleles in DTUs IIa and IIc showed a spectrum of polymorphism ranging from DTU I-like to DTU IIb-like, in addition to DTU-specific sequence variation. DTUs IId and IIe were indistinguishable, showing DTU homozygosity at one locus and heterozygosity with DTU IIb and IIc allelic sequences at eight loci. Recombination between the DTU IIb and IIc alleles is evidenced from mosaic polymorphisms. These data imply that two discrete hybridization events resulted in the formation of the current DTUs. We propose a model in which a fusion between ancestral DTU I and IIb strains gave rise to a heterozygous hybrid that homogenized its genome to become the homozygous progenitor of DTUs IIa and IIc. The second hybridization between DTU IIb and IIc strains that generated DTUs IId and IIe resulted in extensive heterozygosity with subsequent recombination of parental genotypes.
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                Author and article information

                Contributors
                fernanda.alves@fiocruz.br
                juliane.bioma@gmail.com
                fabiana.rocha@triade.org.br
                herrera@ucdb.br
                guilherme.mourao@embrapa.br
                jansen@ioc.fiocruz.br
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                1 July 2016
                1 July 2016
                2016
                : 9
                : 378
                Affiliations
                [ ]Laboratório de Biologia de Tripanossomatídeos, Fundação Oswaldo Cruz, Rio de Janeiro, Rio de Janeiro, Brasil
                [ ]Laboratório de Vida Selvagem, Empresa Brasileira de Pesquisa Agropecuária (Embrapa)/Pantanal, Corumbá, Mato Grosso do Sul Brasil
                [ ]Programa de Pós-Graduação em Ecologia e Monitoramento Ambiental, Universidade Federal da Paraíba–Campus Litoral, Rio Tinto, Brasil
                [ ]Laboratório de Parasitologia Animal, Universidade Católica Dom Bosco, Campo Grande, Mato Grosso do Sul Brasil
                Article
                1649
                10.1186/s13071-016-1649-4
                4930594
                27370106
                fe913d59-4b5c-4578-a26b-392e0fe1380f
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 11 February 2016
                : 16 June 2016
                Funding
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100006507, Fundação Oswaldo Cruz;
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100004586, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro;
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100003046, Empresa Brasileira de Pesquisa Agropecuária;
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Funded by: Chagas EpiNet
                Award ID: EU 223034
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Parasitology
                trypanosoma cruzi,nasua nasua,rhodnius,triatoma,pantanal,sylvatic cycle
                Parasitology
                trypanosoma cruzi, nasua nasua, rhodnius, triatoma, pantanal, sylvatic cycle

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