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The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes

BACKGROUND: Burkholderia species play an important ecological role related to xenobiosis, the promotion of plant growth, the biocontrol of agricultural diseases, and symbiotic and non-symbiotic biological nitrogen fixation. Here, we highlight our study as providing the first complete genome of a sym...

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Autores principales: Zuleta, Luiz Fernando Goda, Cunha, Claúdio de Oliveira, de Carvalho, Fabíola Marques, Ciapina, Luciane Prioli, Souza, Rangel Celso, Mercante, Fábio Martins, de Faria, Sergio Miana, Baldani, José Ivo, Straliotto, Rosangela, Hungria, Mariangela, de Vasconcelos, Ana Tereza Ribeiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4101177/
https://www.ncbi.nlm.nih.gov/pubmed/24972629
http://dx.doi.org/10.1186/1471-2164-15-535
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author Zuleta, Luiz Fernando Goda
Cunha, Claúdio de Oliveira
de Carvalho, Fabíola Marques
Ciapina, Luciane Prioli
Souza, Rangel Celso
Mercante, Fábio Martins
de Faria, Sergio Miana
Baldani, José Ivo
Straliotto, Rosangela
Hungria, Mariangela
de Vasconcelos, Ana Tereza Ribeiro
author_facet Zuleta, Luiz Fernando Goda
Cunha, Claúdio de Oliveira
de Carvalho, Fabíola Marques
Ciapina, Luciane Prioli
Souza, Rangel Celso
Mercante, Fábio Martins
de Faria, Sergio Miana
Baldani, José Ivo
Straliotto, Rosangela
Hungria, Mariangela
de Vasconcelos, Ana Tereza Ribeiro
author_sort Zuleta, Luiz Fernando Goda
collection PubMed
description BACKGROUND: Burkholderia species play an important ecological role related to xenobiosis, the promotion of plant growth, the biocontrol of agricultural diseases, and symbiotic and non-symbiotic biological nitrogen fixation. Here, we highlight our study as providing the first complete genome of a symbiotic strain of B. phenoliruptrix, BR3459a (=CLA1), which was originally isolated in Brazil from nodules of Mimosa flocculosa and is effective in fixing nitrogen in association with this leguminous species. RESULTS: Genomic comparisons with other pathogenic and non-pathogenic Burkholderia strains grouped B. phenoliruptrix BR3459a with plant-associated beneficial and environmental species, although it shares a high percentage of its gene repertoire with species of the B. cepacia complex (Bcc) and "pseudomallei" group. The genomic analyses showed that the bce genes involved in exopolysaccharide production are clustered together in the same genomic region, constituting part of the Group III cluster of non-pathogenic bacteria. Regarding environmental stresses, we highlight genes that might be relevant in responses to osmotic, heat, cold and general stresses. Furthermore, a number of particularly interesting genes involved in the machinery of the T1SS, T2SS, T3SS, T4ASS and T6SS secretion systems were identified. The xenobiotic properties of strain BR3459a were also investigated, and some enzymes involved in the degradation of styrene, nitrotoluene, dioxin, chlorocyclohexane, chlorobenzene and caprolactam were identified. The genomic analyses also revealed a large number of antibiotic-related genes, the most important of which were correlated with streptomycin and novobiocin. The symbiotic plasmid showed high sequence identity with the symbiotic plasmid of B. phymatum. Additionally, comparative analysis of 545 housekeeping genes among pathogenic and non-pathogenic Burkholderia species strongly supports the definition of a new genus for the second branch, which would include BR3459a. CONCLUSIONS: The analyses of B. phenoliruptrix BR3459a showed key property of fixing nitrogen that together with genes for high tolerance to environmental stresses might explain a successful strategy of symbiosis in the tropics. The strain also harbours interesting sets of genes with biotechnological potential. However, the resemblance of certain genes to those of pathogenic Burkholderia raise concerns about large-scale applications in agriculture or for bioremediation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-535) contains supplementary material, which is available to authorized users.
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spelling pubmed-41011772014-07-18 The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes Zuleta, Luiz Fernando Goda Cunha, Claúdio de Oliveira de Carvalho, Fabíola Marques Ciapina, Luciane Prioli Souza, Rangel Celso Mercante, Fábio Martins de Faria, Sergio Miana Baldani, José Ivo Straliotto, Rosangela Hungria, Mariangela de Vasconcelos, Ana Tereza Ribeiro BMC Genomics Research Article BACKGROUND: Burkholderia species play an important ecological role related to xenobiosis, the promotion of plant growth, the biocontrol of agricultural diseases, and symbiotic and non-symbiotic biological nitrogen fixation. Here, we highlight our study as providing the first complete genome of a symbiotic strain of B. phenoliruptrix, BR3459a (=CLA1), which was originally isolated in Brazil from nodules of Mimosa flocculosa and is effective in fixing nitrogen in association with this leguminous species. RESULTS: Genomic comparisons with other pathogenic and non-pathogenic Burkholderia strains grouped B. phenoliruptrix BR3459a with plant-associated beneficial and environmental species, although it shares a high percentage of its gene repertoire with species of the B. cepacia complex (Bcc) and "pseudomallei" group. The genomic analyses showed that the bce genes involved in exopolysaccharide production are clustered together in the same genomic region, constituting part of the Group III cluster of non-pathogenic bacteria. Regarding environmental stresses, we highlight genes that might be relevant in responses to osmotic, heat, cold and general stresses. Furthermore, a number of particularly interesting genes involved in the machinery of the T1SS, T2SS, T3SS, T4ASS and T6SS secretion systems were identified. The xenobiotic properties of strain BR3459a were also investigated, and some enzymes involved in the degradation of styrene, nitrotoluene, dioxin, chlorocyclohexane, chlorobenzene and caprolactam were identified. The genomic analyses also revealed a large number of antibiotic-related genes, the most important of which were correlated with streptomycin and novobiocin. The symbiotic plasmid showed high sequence identity with the symbiotic plasmid of B. phymatum. Additionally, comparative analysis of 545 housekeeping genes among pathogenic and non-pathogenic Burkholderia species strongly supports the definition of a new genus for the second branch, which would include BR3459a. CONCLUSIONS: The analyses of B. phenoliruptrix BR3459a showed key property of fixing nitrogen that together with genes for high tolerance to environmental stresses might explain a successful strategy of symbiosis in the tropics. The strain also harbours interesting sets of genes with biotechnological potential. However, the resemblance of certain genes to those of pathogenic Burkholderia raise concerns about large-scale applications in agriculture or for bioremediation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-535) contains supplementary material, which is available to authorized users. BioMed Central 2014-06-28 /pmc/articles/PMC4101177/ /pubmed/24972629 http://dx.doi.org/10.1186/1471-2164-15-535 Text en © Zuleta et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.
spellingShingle Research Article
Zuleta, Luiz Fernando Goda
Cunha, Claúdio de Oliveira
de Carvalho, Fabíola Marques
Ciapina, Luciane Prioli
Souza, Rangel Celso
Mercante, Fábio Martins
de Faria, Sergio Miana
Baldani, José Ivo
Straliotto, Rosangela
Hungria, Mariangela
de Vasconcelos, Ana Tereza Ribeiro
The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes
title The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes
title_full The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes
title_fullStr The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes
title_full_unstemmed The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes
title_short The complete genome of Burkholderia phenoliruptrix strain BR3459a, a symbiont of Mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes
title_sort complete genome of burkholderia phenoliruptrix strain br3459a, a symbiont of mimosa flocculosa: highlighting the coexistence of symbiotic and pathogenic genes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4101177/
https://www.ncbi.nlm.nih.gov/pubmed/24972629
http://dx.doi.org/10.1186/1471-2164-15-535
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