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Field and experimental evidence of a new caiman trypanosome species closely phylogenetically related to fish trypanosomes and transmitted by leeches.

ABSTRACT: Trypanosoma terena and Trypanosoma ralphi are known species of the South American crocodilians Caiman crocodilus, Caiman yacare and Melanosuchus niger and are phylogenetically related to the tsetse-transmitted Trypanosoma grayi of the African Crocodylus niloticus. These trypanosomes form the Crocodilian clade of the terrestrial clade of the genus Trypanosoma. A PCR-survey for trypanosomes in caiman blood samples and in leeches taken from caimans revealed unknown trypanosome diversity and frequent mixed infections. Phylogenies based on SSU (small subunit) of rRNA and gGAPDH (glycosomal Glyceraldehyde Phosphate Dehydrogenase) gene sequences revealed a new trypanosome species clustering with T. terena and T. ralphi in the crocodilian clade and an additional new species nesting in the distant Aquatic clade of trypanosomes, which is herein named Trypanosoma clandestinus n. sp. This new species was found in Caiman yacare, Caiman crocodilus and M. niger from the Pantanal and Amazonian biomes in Brazil. Large numbers of dividing epimastigotes and unique thin and long trypomastigotes were found in the guts of leeches (Haementeria sp.) removed from the mouths of caimans. The trypanosomes recovered from the leeches had sequences identical to those of T. clandestinus of caiman blood samples. Experimental infestation of young caimans (Caiman yacare) with infected leeches resulted in long-lasting T. clandestinus infections that permitted us to delineate its life cycle. In contrast to T. terena, T. ralphi and T. grayi, which are detectable by hemoculturing, microscopy and standard PCR of caiman blood, T. clandestinus passes undetected by these methods due to very low parasitemia and could be detected solely by the more sensitive nested PCR method. T. clandestinus n. sp. is the first crocodilian trypanosome known to be transmitted by leeches and positioned in the aquatic clade closest to fish trypanosomes. Our data show that caimans can host trypanosomes of the aquatic or terrestrial clade, sometimes simultaneously.

SUBMITTER: Fermino BR

PROVIDER: S-EPMC4683569 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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Field and experimental evidence of a new caiman trypanosome species closely phylogenetically related to fish trypanosomes and transmitted by leeches.

Fermino Bruno R BR Paiva Fernando F Soares Priscilla P Tavares Luiz Eduardo R LE Viola Laerte B LB Ferreira Robson C RC Botero-Arias Robinson R de-Paula Cátia D CD Campaner Marta M Takata Carmen S A CS Teixeira Marta M G MM Camargo Erney P EP

International journal for parasitology. Parasites and wildlife 20151021 3

Trypanosoma terena and Trypanosoma ralphi are known species of the South American crocodilians Caiman crocodilus, Caiman yacare and Melanosuchus niger and are phylogenetically related to the tsetse-transmitted Trypanosoma grayi of the African Crocodylus niloticus. These trypanosomes form the Crocodilian clade of the terrestrial clade of the genus Trypanosoma. A PCR-survey for trypanosomes in caiman blood samples and in leeches taken from caimans revealed unknown trypanosome diversity and frequen ...[more]

PMID: 26767165

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Project description:Several Trypanosoma species transmitted by leeches infect marine and freshwater fish worldwide. To date, all South American fish trypanosome species identified have been based on unreliable morphological parameters. We recently isolated and cultured trypanosomes from the Brazilian armoured catfishes Hypostomus luetkeni and H. affinis. Here, we report the first phylogenetic analyses of South American (Brazilian) trypanosomes isolated from fish, and from leeches removed from these fish. We also analysed morphologically and morphometrically the different forms of fish, leech and cultured trypanosomes.V7V8 SSU rRNA and gGAPDH sequences were used for phylogenetic analysis of Brazilian fish and leech trypanosomes. Trypanosomes from cultures, fish blood and leech samples were also characterized morphologically and morphometrically by light and electron microscopy.In blood smears from fish high trypanosome prevalence (90-100 %) and parasitemia (0.9-1.0x10(2)) were observed. Phylogenetic relationships using SSU rRNA and gGAPDH showed that, despite relevant sequence divergence, all Brazilian fish (and derived cultures) and leech trypanosomes clustered together into a single clade. The Brazilian clade clustered with European, North American and African fish trypanosomes. Based on sequence analysis, we uncovered a new species of Brazilian fish trypanosome, Trypanosoma abeli n. sp. Trypanosoma abeli cultures contained pleomorphic epimastigotes, small trypomastigotes and rare sphaeromastigotes. Ultrastructural features of T. abeli included a cytostome-cytopharynx complex in epi- and trypomastigotes, a compact rod-like kinetoplast, lysosome-related organelles (LROs) and multivesicular bodies. Trypanosomes found in fish blood smears and leech samples were highly pleomorphic, in agreement with sequence data suggesting that catfishes and leeches often have mixed trypanosome infections.Trypanosoma abeli n. sp. is the first trypanosome from South American fishes isolated in culture, positioned in phylogenetic trees and characterized at the ultrastructural level. Trypanosoma abeli n. sp. is highly prevalent in H. luetkeni and H. affinis armoured catfish from the Atlantic Forest biome, and in other catfish species from the Amazon and the Pantanal. Sequencing data suggested that Brazilian catfish often have mixed trypanosome infections, highlighting the importance of molecular characterization to identify trypanosome species in fishes and leeches.

Project description:Purpose: The aim was, in the frame of an anti-vector strategy, to use such genes to control Human and/or animal trypanosomiasis. The present objective was to verify whether field tsetse fly gene expression was modified in response to natural infection with trypanosomes as it was when insectary-raised flies were experimentally infected. Method: mRNA from 10 samples of Glossina palpalis (5 non-infected and 5 infected by Trypanosoma congolense s.l.) were sequenced on a high-output flow cell (400M clusters) using the NextSeq® 500/550 High Output v2 150 cycles kit (Illumina), in paired-end 75/75nt mode. The sequenced reads that passed quality filter were mapped onto the genome with the local alignment algorithm subread-align (Liao et al., 2013). Differential analysis was done with the SARTools R package (Varet et al., 2016), which runs separately DESeq2 (Love et al., 2014) and egdeR (Robinson et al., 2010). We identified orthologs between Glossina and Drosophila based on the identification of bidirectional best hits (BBH) using blastp (Altschul et al., 1997), and then made functional enrichment and pathway mapping of these DEGs. Results: Using the RNA-seq approach, differentially expressed genes (DEGs) have been identified in infected versus non-infected tsetse flies, including down-regulated genes and up-regulated genes. Some of the genes, whether down- or up-regulated, were very highly differentially expressed. Down-regulated genes were mainly involved in transcription/translation processes, while up-regulated encoded genes governing amino acid and nucleotide biosynthesis pathways. The data on the molecular cross-talk between the host and the parasite (and the fly microbiome that is always present) recorded when using an experimental biological model have its counterpart in field flies which in turn validates the use of experimental host/parasite couples. Conclusion: This study is the first evaluation of transcriptomic mechanisms related to infection in field tsetse flies. This opens up prospects for vector-based control strategies, and more precisely the blocking of transmission.

Dataset Information

Field and experimental evidence of a new caiman trypanosome species closely phylogenetically related to fish trypanosomes and transmitted by leeches.

Publications

Field and experimental evidence of a new caiman trypanosome species closely phylogenetically related to fish trypanosomes and transmitted by leeches.

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