Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species

Abstract Background 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 Brazilia...

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Main Authors: Moara Lemos, Bruno R. Fermino, Cíntia Simas-Rodrigues, Luísa Hoffmann, Rosane Silva, Erney P. Camargo, Marta M. G. Teixeira, Thaïs Souto-Padrón
Format: Article
Language:English
Published: BMC 2015-11-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-015-1193-7
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author Moara Lemos
Bruno R. Fermino
Cíntia Simas-Rodrigues
Luísa Hoffmann
Rosane Silva
Erney P. Camargo
Marta M. G. Teixeira
Thaïs Souto-Padrón
author_facet Moara Lemos
Bruno R. Fermino
Cíntia Simas-Rodrigues
Luísa Hoffmann
Rosane Silva
Erney P. Camargo
Marta M. G. Teixeira
Thaïs Souto-Padrón
author_sort Moara Lemos
collection DOAJ
description Abstract Background 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. Methods 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. Results In blood smears from fish high trypanosome prevalence (90–100 %) and parasitemia (0.9-1.0x102) 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. Conclusions 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.
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spelling doaj.art-64609c13130b45c8bd27de45e7f7614e2023-06-04T11:09:31ZengBMCParasites & Vectors1756-33052015-11-018111710.1186/s13071-015-1193-7Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome speciesMoara Lemos0Bruno R. Fermino1Cíntia Simas-Rodrigues2Luísa Hoffmann3Rosane Silva4Erney P. Camargo5Marta M. G. Teixeira6Thaïs Souto-Padrón7Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Centro de Ciências da Saúde, Universidade Federal do Rio de JaneiroDepartamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São PauloDepartamento de Bioquímica, Instituto de Química, Universidade de São PauloInstituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de JaneiroInstituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de JaneiroDepartamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São PauloDepartamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São PauloDepartamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Centro de Ciências da Saúde, Universidade Federal do Rio de JaneiroAbstract Background 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. Methods 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. Results In blood smears from fish high trypanosome prevalence (90–100 %) and parasitemia (0.9-1.0x102) 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. Conclusions 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.https://doi.org/10.1186/s13071-015-1193-7TrypanosomaFishCatfishLeechCulturePhylogeny
spellingShingle Moara Lemos
Bruno R. Fermino
Cíntia Simas-Rodrigues
Luísa Hoffmann
Rosane Silva
Erney P. Camargo
Marta M. G. Teixeira
Thaïs Souto-Padrón
Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species
Parasites & Vectors
Trypanosoma
Fish
Catfish
Leech
Culture
Phylogeny
title Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species
title_full Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species
title_fullStr Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species
title_full_unstemmed Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species
title_short Phylogenetic and morphological characterization of trypanosomes from Brazilian armoured catfishes and leeches reveal high species diversity, mixed infections and a new fish trypanosome species
title_sort phylogenetic and morphological characterization of trypanosomes from brazilian armoured catfishes and leeches reveal high species diversity mixed infections and a new fish trypanosome species
topic Trypanosoma
Fish
Catfish
Leech
Culture
Phylogeny
url https://doi.org/10.1186/s13071-015-1193-7
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