Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family

Endosymbiont-bearing trypanosomatids have been considered excellent models for the study of cell evolution because the host protozoan co-evolves with an intracellular bacterium in a mutualistic relationship. Such protozoa inhabit a single invertebrate host during their entire life cycle and exhibit...

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Main Authors:	Motta, Maria Cristina Machado, Martins, Allan Cezar de Azevedo, de Souza, Silvana Sant’Anna, Catta-Preta, Carolina Moura Costa, Silva, Rosane, Klein, Cecilia Coimbra, de Almeida, Luiz Gonzaga Paula, de Lima Cunha, Oberdan, Ciapina, Luciane Prioli, Brocchi, Marcelo, Colabardini, Ana Cristina, de Araujo Lima, Bruna, Machado, Carlos Renato, de Almeida Soares, Célia Maria, Probst, Christian Macagnan, de Menezes, Claudia Beatriz Afonso, Thompson, Claudia Elizabeth, Bartholomeu, Daniella Castanheira, Gradia, Daniela Fiori, Pavoni, Daniela Parada, Grisard, Edmundo C., Fantinatti-Garboggini, Fabiana, Marchini, Fabricio Klerynton, Rodrigues-Luiz, Gabriela Flávia, Wagner, Glauber, Goldman, Gustavo Henrique, Fietto, Juliana Lopes Rangel, Elias, Maria Carolina, Goldman, Maria Helena S., Sagot, Marie-France, Pereira, Maristela, Stoco, Patrícia H., de Mendonça-Neto, Rondon Pessoa, Teixeira, Santuza Maria Ribeiro, Maciel, Talles Eduardo Ferreira, de Oliveira Mendes, Tiago Antônio, Ürményi, Turán P., de Souza, Wanderley, Schenkman, Sergio, de Vasconcelos, Ana Tereza Ribeiro
Format:	Online
Language:	English
Published:	Public Library of Science 2013
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3616161/

id	pubmed-3616161
recordtype	oai_dc
spelling	pubmed-36161612013-04-04 Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family Motta, Maria Cristina Machado Martins, Allan Cezar de Azevedo de Souza, Silvana Sant’Anna Catta-Preta, Carolina Moura Costa Silva, Rosane Klein, Cecilia Coimbra de Almeida, Luiz Gonzaga Paula de Lima Cunha, Oberdan Ciapina, Luciane Prioli Brocchi, Marcelo Colabardini, Ana Cristina de Araujo Lima, Bruna Machado, Carlos Renato de Almeida Soares, Célia Maria Probst, Christian Macagnan de Menezes, Claudia Beatriz Afonso Thompson, Claudia Elizabeth Bartholomeu, Daniella Castanheira Gradia, Daniela Fiori Pavoni, Daniela Parada Grisard, Edmundo C. Fantinatti-Garboggini, Fabiana Marchini, Fabricio Klerynton Rodrigues-Luiz, Gabriela Flávia Wagner, Glauber Goldman, Gustavo Henrique Fietto, Juliana Lopes Rangel Elias, Maria Carolina Goldman, Maria Helena S. Sagot, Marie-France Pereira, Maristela Stoco, Patrícia H. de Mendonça-Neto, Rondon Pessoa Teixeira, Santuza Maria Ribeiro Maciel, Talles Eduardo Ferreira de Oliveira Mendes, Tiago Antônio Ürményi, Turán P. de Souza, Wanderley Schenkman, Sergio de Vasconcelos, Ana Tereza Ribeiro Research Article Endosymbiont-bearing trypanosomatids have been considered excellent models for the study of cell evolution because the host protozoan co-evolves with an intracellular bacterium in a mutualistic relationship. Such protozoa inhabit a single invertebrate host during their entire life cycle and exhibit special characteristics that group them in a particular phylogenetic cluster of the Trypanosomatidae family, thus classified as monoxenics. In an effort to better understand such symbiotic association, we used DNA pyrosequencing and a reference-guided assembly to generate reads that predicted 16,960 and 12,162 open reading frames (ORFs) in two symbiont-bearing trypanosomatids, Angomonas deanei (previously named as Crithidia deanei) and Strigomonas culicis (first known as Blastocrithidia culicis), respectively. Identification of each ORF was based primarily on TriTrypDB using tblastn, and each ORF was confirmed by employing getorf from EMBOSS and Newbler 2.6 when necessary. The monoxenic organisms revealed conserved housekeeping functions when compared to other trypanosomatids, especially compared with Leishmania major. However, major differences were found in ORFs corresponding to the cytoskeleton, the kinetoplast, and the paraflagellar structure. The monoxenic organisms also contain a large number of genes for cytosolic calpain-like and surface gp63 metalloproteases and a reduced number of compartmentalized cysteine proteases in comparison to other TriTryp organisms, reflecting adaptations to the presence of the symbiont. The assembled bacterial endosymbiont sequences exhibit a high A+T content with a total of 787 and 769 ORFs for the Angomonas deanei and Strigomonas culicis endosymbionts, respectively, and indicate that these organisms hold a common ancestor related to the Alcaligenaceae family. Importantly, both symbionts contain enzymes that complement essential host cell biosynthetic pathways, such as those for amino acid, lipid and purine/pyrimidine metabolism. These findings increase our understanding of the intricate symbiotic relationship between the bacterium and the trypanosomatid host and provide clues to better understand eukaryotic cell evolution. Public Library of Science 2013-04-03 /pmc/articles/PMC3616161/ /pubmed/23560078 http://dx.doi.org/10.1371/journal.pone.0060209 Text en © 2013 Motta et al http://creativecommons.org/licenses/by/4.0/ 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 properly credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Motta, Maria Cristina Machado Martins, Allan Cezar de Azevedo de Souza, Silvana Sant’Anna Catta-Preta, Carolina Moura Costa Silva, Rosane Klein, Cecilia Coimbra de Almeida, Luiz Gonzaga Paula de Lima Cunha, Oberdan Ciapina, Luciane Prioli Brocchi, Marcelo Colabardini, Ana Cristina de Araujo Lima, Bruna Machado, Carlos Renato de Almeida Soares, Célia Maria Probst, Christian Macagnan de Menezes, Claudia Beatriz Afonso Thompson, Claudia Elizabeth Bartholomeu, Daniella Castanheira Gradia, Daniela Fiori Pavoni, Daniela Parada Grisard, Edmundo C. Fantinatti-Garboggini, Fabiana Marchini, Fabricio Klerynton Rodrigues-Luiz, Gabriela Flávia Wagner, Glauber Goldman, Gustavo Henrique Fietto, Juliana Lopes Rangel Elias, Maria Carolina Goldman, Maria Helena S. Sagot, Marie-France Pereira, Maristela Stoco, Patrícia H. de Mendonça-Neto, Rondon Pessoa Teixeira, Santuza Maria Ribeiro Maciel, Talles Eduardo Ferreira de Oliveira Mendes, Tiago Antônio Ürményi, Turán P. de Souza, Wanderley Schenkman, Sergio de Vasconcelos, Ana Tereza Ribeiro
spellingShingle	Motta, Maria Cristina Machado Martins, Allan Cezar de Azevedo de Souza, Silvana Sant’Anna Catta-Preta, Carolina Moura Costa Silva, Rosane Klein, Cecilia Coimbra de Almeida, Luiz Gonzaga Paula de Lima Cunha, Oberdan Ciapina, Luciane Prioli Brocchi, Marcelo Colabardini, Ana Cristina de Araujo Lima, Bruna Machado, Carlos Renato de Almeida Soares, Célia Maria Probst, Christian Macagnan de Menezes, Claudia Beatriz Afonso Thompson, Claudia Elizabeth Bartholomeu, Daniella Castanheira Gradia, Daniela Fiori Pavoni, Daniela Parada Grisard, Edmundo C. Fantinatti-Garboggini, Fabiana Marchini, Fabricio Klerynton Rodrigues-Luiz, Gabriela Flávia Wagner, Glauber Goldman, Gustavo Henrique Fietto, Juliana Lopes Rangel Elias, Maria Carolina Goldman, Maria Helena S. Sagot, Marie-France Pereira, Maristela Stoco, Patrícia H. de Mendonça-Neto, Rondon Pessoa Teixeira, Santuza Maria Ribeiro Maciel, Talles Eduardo Ferreira de Oliveira Mendes, Tiago Antônio Ürményi, Turán P. de Souza, Wanderley Schenkman, Sergio de Vasconcelos, Ana Tereza Ribeiro Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family
author_facet	Motta, Maria Cristina Machado Martins, Allan Cezar de Azevedo de Souza, Silvana Sant’Anna Catta-Preta, Carolina Moura Costa Silva, Rosane Klein, Cecilia Coimbra de Almeida, Luiz Gonzaga Paula de Lima Cunha, Oberdan Ciapina, Luciane Prioli Brocchi, Marcelo Colabardini, Ana Cristina de Araujo Lima, Bruna Machado, Carlos Renato de Almeida Soares, Célia Maria Probst, Christian Macagnan de Menezes, Claudia Beatriz Afonso Thompson, Claudia Elizabeth Bartholomeu, Daniella Castanheira Gradia, Daniela Fiori Pavoni, Daniela Parada Grisard, Edmundo C. Fantinatti-Garboggini, Fabiana Marchini, Fabricio Klerynton Rodrigues-Luiz, Gabriela Flávia Wagner, Glauber Goldman, Gustavo Henrique Fietto, Juliana Lopes Rangel Elias, Maria Carolina Goldman, Maria Helena S. Sagot, Marie-France Pereira, Maristela Stoco, Patrícia H. de Mendonça-Neto, Rondon Pessoa Teixeira, Santuza Maria Ribeiro Maciel, Talles Eduardo Ferreira de Oliveira Mendes, Tiago Antônio Ürményi, Turán P. de Souza, Wanderley Schenkman, Sergio de Vasconcelos, Ana Tereza Ribeiro
author_sort	Motta, Maria Cristina Machado
title	Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family
title_short	Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family
title_full	Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family
title_fullStr	Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family
title_full_unstemmed	Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family
title_sort	predicting the proteins of angomonas deanei, strigomonas culicis and their respective endosymbionts reveals new aspects of the trypanosomatidae family
description	Endosymbiont-bearing trypanosomatids have been considered excellent models for the study of cell evolution because the host protozoan co-evolves with an intracellular bacterium in a mutualistic relationship. Such protozoa inhabit a single invertebrate host during their entire life cycle and exhibit special characteristics that group them in a particular phylogenetic cluster of the Trypanosomatidae family, thus classified as monoxenics. In an effort to better understand such symbiotic association, we used DNA pyrosequencing and a reference-guided assembly to generate reads that predicted 16,960 and 12,162 open reading frames (ORFs) in two symbiont-bearing trypanosomatids, Angomonas deanei (previously named as Crithidia deanei) and Strigomonas culicis (first known as Blastocrithidia culicis), respectively. Identification of each ORF was based primarily on TriTrypDB using tblastn, and each ORF was confirmed by employing getorf from EMBOSS and Newbler 2.6 when necessary. The monoxenic organisms revealed conserved housekeeping functions when compared to other trypanosomatids, especially compared with Leishmania major. However, major differences were found in ORFs corresponding to the cytoskeleton, the kinetoplast, and the paraflagellar structure. The monoxenic organisms also contain a large number of genes for cytosolic calpain-like and surface gp63 metalloproteases and a reduced number of compartmentalized cysteine proteases in comparison to other TriTryp organisms, reflecting adaptations to the presence of the symbiont. The assembled bacterial endosymbiont sequences exhibit a high A+T content with a total of 787 and 769 ORFs for the Angomonas deanei and Strigomonas culicis endosymbionts, respectively, and indicate that these organisms hold a common ancestor related to the Alcaligenaceae family. Importantly, both symbionts contain enzymes that complement essential host cell biosynthetic pathways, such as those for amino acid, lipid and purine/pyrimidine metabolism. These findings increase our understanding of the intricate symbiotic relationship between the bacterium and the trypanosomatid host and provide clues to better understand eukaryotic cell evolution.
publisher	Public Library of Science
publishDate	2013
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3616161/
_version_	1611967521024376832

Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family

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