Cargando…

Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses

Some non-pathogenic trypanosomatids maintain a mutualistic relationship with a betaproteobacterium of the Alcaligenaceae family. Intensive nutritional exchanges have been reported between the two partners, indicating that these protozoa are excellent biological models to study metabolic co-evolution...

Descripción completa

Detalles Bibliográficos
Autores principales: Klein, Cecilia C., Alves, João M. P., Serrano, Myrna G., Buck, Gregory A., Vasconcelos, Ana Tereza R., Sagot, Marie-France, Teixeira, Marta M. G., Camargo, Erney P., Motta, Maria Cristina M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3833962/
https://www.ncbi.nlm.nih.gov/pubmed/24260300
http://dx.doi.org/10.1371/journal.pone.0079786
_version_ 1782291920596238336
author Klein, Cecilia C.
Alves, João M. P.
Serrano, Myrna G.
Buck, Gregory A.
Vasconcelos, Ana Tereza R.
Sagot, Marie-France
Teixeira, Marta M. G.
Camargo, Erney P.
Motta, Maria Cristina M.
author_facet Klein, Cecilia C.
Alves, João M. P.
Serrano, Myrna G.
Buck, Gregory A.
Vasconcelos, Ana Tereza R.
Sagot, Marie-France
Teixeira, Marta M. G.
Camargo, Erney P.
Motta, Maria Cristina M.
author_sort Klein, Cecilia C.
collection PubMed
description Some non-pathogenic trypanosomatids maintain a mutualistic relationship with a betaproteobacterium of the Alcaligenaceae family. Intensive nutritional exchanges have been reported between the two partners, indicating that these protozoa are excellent biological models to study metabolic co-evolution. We previously sequenced and herein investigate the entire genomes of five trypanosomatids which harbor a symbiotic bacterium (SHTs for Symbiont-Haboring Trypanosomatids) and the respective bacteria (TPEs for Trypanosomatid Proteobacterial Endosymbiont), as well as two trypanosomatids without symbionts (RTs for Regular Trypanosomatids), for the presence of genes of the classical pathways for vitamin biosynthesis. Our data show that genes for the biosynthetic pathways of thiamine, biotin, and nicotinic acid are absent from all trypanosomatid genomes. This is in agreement with the absolute growth requirement for these vitamins in all protozoa of the family. Also absent from the genomes of RTs are the genes for the synthesis of pantothenic acid, folic acid, riboflavin, and vitamin B(6.) This is also in agreement with the available data showing that RTs are auxotrophic for these essential vitamins. On the other hand, SHTs are autotrophic for such vitamins. Indeed, all the genes of the corresponding biosynthetic pathways were identified, most of them in the symbiont genomes, while a few genes, mostly of eukaryotic origin, were found in the host genomes. The only exceptions to the latter are: the gene coding for the enzyme ketopantoate reductase (EC:1.1.1.169) which is related instead to the Firmicutes bacteria; and two other genes, one involved in the salvage pathway of pantothenic acid and the other in the synthesis of ubiquinone, that are related to Gammaproteobacteria. Their presence in trypanosomatids may result from lateral gene transfer. Taken together, our results reinforce the idea that the low nutritional requirement of SHTs is associated with the presence of the symbiotic bacterium, which contains most genes for vitamin production.
format Online
Article
Text
id pubmed-3833962
institution National Center for Biotechnology Information
language English
publishDate 2013
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-38339622013-11-20 Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses Klein, Cecilia C. Alves, João M. P. Serrano, Myrna G. Buck, Gregory A. Vasconcelos, Ana Tereza R. Sagot, Marie-France Teixeira, Marta M. G. Camargo, Erney P. Motta, Maria Cristina M. PLoS One Research Article Some non-pathogenic trypanosomatids maintain a mutualistic relationship with a betaproteobacterium of the Alcaligenaceae family. Intensive nutritional exchanges have been reported between the two partners, indicating that these protozoa are excellent biological models to study metabolic co-evolution. We previously sequenced and herein investigate the entire genomes of five trypanosomatids which harbor a symbiotic bacterium (SHTs for Symbiont-Haboring Trypanosomatids) and the respective bacteria (TPEs for Trypanosomatid Proteobacterial Endosymbiont), as well as two trypanosomatids without symbionts (RTs for Regular Trypanosomatids), for the presence of genes of the classical pathways for vitamin biosynthesis. Our data show that genes for the biosynthetic pathways of thiamine, biotin, and nicotinic acid are absent from all trypanosomatid genomes. This is in agreement with the absolute growth requirement for these vitamins in all protozoa of the family. Also absent from the genomes of RTs are the genes for the synthesis of pantothenic acid, folic acid, riboflavin, and vitamin B(6.) This is also in agreement with the available data showing that RTs are auxotrophic for these essential vitamins. On the other hand, SHTs are autotrophic for such vitamins. Indeed, all the genes of the corresponding biosynthetic pathways were identified, most of them in the symbiont genomes, while a few genes, mostly of eukaryotic origin, were found in the host genomes. The only exceptions to the latter are: the gene coding for the enzyme ketopantoate reductase (EC:1.1.1.169) which is related instead to the Firmicutes bacteria; and two other genes, one involved in the salvage pathway of pantothenic acid and the other in the synthesis of ubiquinone, that are related to Gammaproteobacteria. Their presence in trypanosomatids may result from lateral gene transfer. Taken together, our results reinforce the idea that the low nutritional requirement of SHTs is associated with the presence of the symbiotic bacterium, which contains most genes for vitamin production. Public Library of Science 2013-11-19 /pmc/articles/PMC3833962/ /pubmed/24260300 http://dx.doi.org/10.1371/journal.pone.0079786 Text en © 2013 Klein 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.
spellingShingle Research Article
Klein, Cecilia C.
Alves, João M. P.
Serrano, Myrna G.
Buck, Gregory A.
Vasconcelos, Ana Tereza R.
Sagot, Marie-France
Teixeira, Marta M. G.
Camargo, Erney P.
Motta, Maria Cristina M.
Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses
title Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses
title_full Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses
title_fullStr Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses
title_full_unstemmed Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses
title_short Biosynthesis of Vitamins and Cofactors in Bacterium-Harbouring Trypanosomatids Depends on the Symbiotic Association as Revealed by Genomic Analyses
title_sort biosynthesis of vitamins and cofactors in bacterium-harbouring trypanosomatids depends on the symbiotic association as revealed by genomic analyses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3833962/
https://www.ncbi.nlm.nih.gov/pubmed/24260300
http://dx.doi.org/10.1371/journal.pone.0079786
work_keys_str_mv AT kleinceciliac biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT alvesjoaomp biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT serranomyrnag biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT buckgregorya biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT vasconcelosanaterezar biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT sagotmariefrance biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT teixeiramartamg biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT camargoerneyp biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses
AT mottamariacristinam biosynthesisofvitaminsandcofactorsinbacteriumharbouringtrypanosomatidsdependsonthesymbioticassociationasrevealedbygenomicanalyses