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

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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 (0.9-1.0x10 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.

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.

Electronic supplementary material

The online version of this article (doi:10.1186/s13071-015-1193-7) contains supplementary material, which is available to authorized users.

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Most cited references 83

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Acidocalcisomes.

Roberto Docampo, Silvia N J Moreno (2011)

Acidocalcisomes are acidic organelles containing calcium and a high concentration of phosphorus in the form of pyrophosphate (PP(i)) and polyphosphate (poly P). Organelles with these characteristics have been found from bacteria to human cells implying an early appearance and persistence over evolutionary time or their appearance by convergent evolution. Acidification of the organelles is driven by the presence of vacuolar proton pumps, one of which, the vacuolar proton pyrophosphatase, is absent in animals, where it is substituted by a vacuolar proton ATPase. A number of other pumps, antiporters, and channels have been described in acidocalcisomes of different species and are responsible for their internal content. Enzymes involved in the synthesis and degradation of PP(i) and poly P are present within the organelle. Acidocalcisomes function as storage sites for cations and phosphorus, and participate in PP(i) and poly P metabolism, calcium homeostasis, maintenance of intracellular pH, and osmoregulation. Experiments in which the acidocalcisome Ca(2+)-ATPase of different parasites were downregulated or eliminated, or acidocalcisome Ca(2+) was depleted revealed the importance of this store in Ca(2+) signaling needed for host invasion and virulence. Acidocalcisomes interact with other organelles in a number of organisms suggesting their association with the endosomal/lysosomal pathway, and are considered part of the lysosome-related group of organelles. 2011 Elsevier Ltd. All rights reserved.

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Evolutionary insights from bat trypanosomes: morphological, developmental and phylogenetic evidence of a new species, Trypanosoma (Schizotrypanum) erneyi sp. nov., in African bats closely related to Trypanosoma (Schizotrypanum) cruzi and allied species.

Luciana Lima, Flávia Maia da Silva, Luis Neves … (2012)

Parasites of the genus Trypanosoma are common in bats and those of the subgenus Schizotrypanum are restricted to bats throughout the world, with the exception of Trypanosoma (Schizotrypanum) cruzi that also infects other mammals and is restricted to the American Continent. We have characterized trypanosome isolates from Molossidae bats captured in Mozambique, Africa. Morphology and behaviour in culture, supported by phylogenetic inferences using SSU (small subunit) rRNA, gGAPDH (glycosomal glyceraldehyde 3-phosphate dehydrogenase) and Cyt b (cytochrome b) genes, allowed to classify the isolates as a new Schizotrypanum species named Trypanosoma (Schizotrypanum) erneyi sp. nov. This is the first report of a Schizotrypanum species from African bats cultured, characterized morphologically and biologically, and positioned in phylogenetic trees. The unprecedented finding of a new species of the subgenus Schizotrypanum from Africa that is closest related to the America-restricted Trypanosoma (Schizotrypanum) cruzi marinkellei and T. cruzi provides new insights into the origin and evolutionary history of T. cruzi and closely related bat trypanosomes. Altogether, data from our study support the hypothesis of an ancestor trypanosome parasite of bats evolving to infect other mammals, even humans, and adapted to transmission by triatomine bugs in the evolutionary history of T. cruzi in the New World. Copyright © 2012 Elsevier GmbH. All rights reserved.

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Is Open Access

Molecular Phylogeny and Biogeographic History of the Armored Neotropical Catfish Subfamilies Hypoptopomatinae, Neoplecostominae and Otothyrinae (Siluriformes: Loricariidae)

Fábio F Roxo, James Albert, Gabriel S. C. Silva … (2014)

The main objectives of this study are estimate a species-dense, time-calibrated molecular phylogeny of Hypoptopomatinae, Neoplecostominae, and Otothyrinae, which together comprise a group of armoured catfishes that is widely distributed across South America, to place the origin of major clades in time and space, and to demonstrate the role of river capture on patterns of diversification in these taxa. We used maximum likelihood and Bayesian methods to estimate a time-calibrated phylogeny of 115 loricariid species, using three mitochondrial and one nuclear genes to generate a matrix of 4,500 base pairs, and used parametric biogeographic analyses to estimate ancestral geographic ranges and to infer the effects of river capture events on the geographic distributions of these taxa. Our analysis recovered Hypoptopomatinae, Neoplecostominae, and Otothyrinae as monophyletic with strong statistical support, and Neoplecostominae as more closely related to Otothyrinae than to Hypoptopomatinae. Our time-calibrated phylogeny and ancestral-area estimations indicate an origin of Hypoptopomatinae, Neoplecostominae, and Otothyrinae during the Lower Eocene in the Atlantic Coastal Drainages, from which it is possible to infer several dispersal events to adjacent river basins during the Neogene. In conclusion we infer a strong influence of river capture in: (1) the accumulation of modern clade species-richness values; (2) the formation of the modern basin-wide species assemblages, and (3) the presence of many low-diversity, early-branching lineages restricted to the Atlantic Coastal Drainages. We further infer the importance of headwater stream capture and marine transgressions in shaping patterns in the distributions of Hypoptopomatinae, Neoplecostominae and Otothyrinae throughout South America.

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Author and article information

Contributors

Moara Lemos: moaralemos@gmail.com

Bruno R. Fermino: brunorf@usp.br

Cíntia Simas-Rodrigues: cintiasimasrodrigues@gmail.com

Luísa Hoffmann: luisa@biof.ufrj.br

Rosane Silva: silvaros@biof.ufrj.br

Erney P. Camargo: erney@usp.br

Marta M. G. Teixeira: mmgteix@icb.usp.br

Thaïs Souto-Padrón: 55 21 25626738 , souto.padron@micro.ufrj.br

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 6 November 2015

Publication date PMC-release: 6 November 2015

Publication date Collection: 2015

Volume: 8

Electronic Location Identifier: 573

Affiliations

[ ]Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro, Bloco I, sala 019. Av. Carlos Chagas Filho, 373, Ilha do Fundão, Rio de janeiro, 21941-902 Brazil

[ ]Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, Brazil

[ ]Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, São Paulo, Brazil

[ ]Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

[ ]Instituto Nacional para Pesquisa Translacional em Saúde e Ambiente na Região Amazônica, Conselho Nacional de Desenvolvimento Científico e Tecnológico/MCT, Rio de Janeiro, Brazil

[ ]Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Centro de Ciências da Saúde, bloco I, Rio de Janeiro, Brazil

Article

Publisher ID: 1193

DOI: 10.1186/s13071-015-1193-7

PMC ID: 4636803

PubMed ID: 26546294

SO-VID: 47e6009c-d0f7-4306-9435-f060f981b9b2

License:

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

Date received : 4 August 2015

Date accepted : 31 October 2015

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: trypanosoma,fish,catfish,leech,culture,phylogeny,taxonomy,morphology,ultrastructure,mixed infections

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: trypanosoma, fish, catfish, leech, culture, phylogeny, taxonomy, morphology, ultrastructure, mixed infections