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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oai:doaj.org-article:04361a4f8ada4266a6fe83785071c88c2021-11-18T07:50:51ZPredicting the proteins of Angomonas deanei, Strigomonas culicis and their respective endosymbionts reveals new aspects of the trypanosomatidae family.1932-620310.1371/journal.pone.0060209https://doaj.org/article/04361a4f8ada4266a6fe83785071c88c2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23560078/?tool=EBIhttps://doaj.org/toc/1932-6203Endosymbiont-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.Maria Cristina Machado MottaAllan Cezar de Azevedo MartinsSilvana Sant'Anna de SouzaCarolina Moura Costa Catta-PretaRosane SilvaCecilia Coimbra KleinLuiz Gonzaga Paula de AlmeidaOberdan de Lima CunhaLuciane Prioli CiapinaMarcelo BrocchiAna Cristina ColabardiniBruna de Araujo LimaCarlos Renato MachadoCélia Maria de Almeida SoaresChristian Macagnan ProbstClaudia Beatriz Afonso de MenezesClaudia Elizabeth ThompsonDaniella Castanheira BartholomeuDaniela Fiori GradiaDaniela Parada PavoniEdmundo C GrisardFabiana Fantinatti-GarbogginiFabricio Klerynton MarchiniGabriela Flávia Rodrigues-LuizGlauber WagnerGustavo Henrique GoldmanJuliana Lopes Rangel FiettoMaria Carolina EliasMaria Helena S GoldmanMarie-France SagotMaristela PereiraPatrícia H StocoRondon Pessoa de Mendonça-NetoSantuza Maria Ribeiro TeixeiraTalles Eduardo Ferreira MacielTiago Antônio de Oliveira MendesTurán P ÜrményiWanderley de SouzaSergio SchenkmanAna Tereza Ribeiro de VasconcelosPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 4, p e60209 (2013) |
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Medicine R Science Q |
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Medicine R Science Q Maria Cristina Machado Motta Allan Cezar de Azevedo Martins Silvana Sant'Anna de Souza Carolina Moura Costa Catta-Preta Rosane Silva Cecilia Coimbra Klein Luiz Gonzaga Paula de Almeida Oberdan de Lima Cunha Luciane Prioli Ciapina Marcelo Brocchi Ana Cristina Colabardini Bruna de Araujo Lima Carlos Renato Machado Célia Maria de Almeida Soares Christian Macagnan Probst Claudia Beatriz Afonso de Menezes Claudia Elizabeth Thompson Daniella Castanheira Bartholomeu Daniela Fiori Gradia Daniela Parada Pavoni Edmundo C Grisard Fabiana Fantinatti-Garboggini Fabricio Klerynton Marchini Gabriela Flávia Rodrigues-Luiz Glauber Wagner Gustavo Henrique Goldman Juliana Lopes Rangel Fietto Maria Carolina Elias Maria Helena S Goldman Marie-France Sagot Maristela Pereira Patrícia H Stoco Rondon Pessoa de Mendonça-Neto Santuza Maria Ribeiro Teixeira Talles Eduardo Ferreira Maciel Tiago Antônio de Oliveira Mendes Turán P Ürményi Wanderley de Souza Sergio Schenkman Ana Tereza Ribeiro de Vasconcelos 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. |
format |
article |
author |
Maria Cristina Machado Motta Allan Cezar de Azevedo Martins Silvana Sant'Anna de Souza Carolina Moura Costa Catta-Preta Rosane Silva Cecilia Coimbra Klein Luiz Gonzaga Paula de Almeida Oberdan de Lima Cunha Luciane Prioli Ciapina Marcelo Brocchi Ana Cristina Colabardini Bruna de Araujo Lima Carlos Renato Machado Célia Maria de Almeida Soares Christian Macagnan Probst Claudia Beatriz Afonso de Menezes Claudia Elizabeth Thompson Daniella Castanheira Bartholomeu Daniela Fiori Gradia Daniela Parada Pavoni Edmundo C Grisard Fabiana Fantinatti-Garboggini Fabricio Klerynton Marchini Gabriela Flávia Rodrigues-Luiz Glauber Wagner Gustavo Henrique Goldman Juliana Lopes Rangel Fietto Maria Carolina Elias Maria Helena S Goldman Marie-France Sagot Maristela Pereira Patrícia H Stoco Rondon Pessoa de Mendonça-Neto Santuza Maria Ribeiro Teixeira Talles Eduardo Ferreira Maciel Tiago Antônio de Oliveira Mendes Turán P Ürményi Wanderley de Souza Sergio Schenkman Ana Tereza Ribeiro de Vasconcelos |
author_facet |
Maria Cristina Machado Motta Allan Cezar de Azevedo Martins Silvana Sant'Anna de Souza Carolina Moura Costa Catta-Preta Rosane Silva Cecilia Coimbra Klein Luiz Gonzaga Paula de Almeida Oberdan de Lima Cunha Luciane Prioli Ciapina Marcelo Brocchi Ana Cristina Colabardini Bruna de Araujo Lima Carlos Renato Machado Célia Maria de Almeida Soares Christian Macagnan Probst Claudia Beatriz Afonso de Menezes Claudia Elizabeth Thompson Daniella Castanheira Bartholomeu Daniela Fiori Gradia Daniela Parada Pavoni Edmundo C Grisard Fabiana Fantinatti-Garboggini Fabricio Klerynton Marchini Gabriela Flávia Rodrigues-Luiz Glauber Wagner Gustavo Henrique Goldman Juliana Lopes Rangel Fietto Maria Carolina Elias Maria Helena S Goldman Marie-France Sagot Maristela Pereira Patrícia H Stoco Rondon Pessoa de Mendonça-Neto Santuza Maria Ribeiro Teixeira Talles Eduardo Ferreira Maciel Tiago Antônio de Oliveira Mendes Turán P Ürményi Wanderley de Souza Sergio Schenkman Ana Tereza Ribeiro de Vasconcelos |
author_sort |
Maria Cristina Machado Motta |
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. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2013 |
url |
https://doaj.org/article/04361a4f8ada4266a6fe83785071c88c |
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