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Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales

BACKGROUND: The Rhizobiales (Proteobacteria) order is an abundant and diverse group of microorganisms, being extensively studied for its lifestyle based on the association with plants, animals, and humans. New studies have demonstrated that the last common ancestor (LCA) of Rhizobiales had a free-li...

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Autores principales: Lemos, Leandro Nascimento, de Carvalho, Fabíola Marques, Gerber, Alexandra, Guimarães, Ana Paula C., Jonck, Celio Roberto, Ciapina, Luciane Prioli, de Vasconcelos, Ana Tereza Ribeiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8555084/
https://www.ncbi.nlm.nih.gov/pubmed/34711170
http://dx.doi.org/10.1186/s12866-021-02354-4
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author Lemos, Leandro Nascimento
de Carvalho, Fabíola Marques
Gerber, Alexandra
Guimarães, Ana Paula C.
Jonck, Celio Roberto
Ciapina, Luciane Prioli
de Vasconcelos, Ana Tereza Ribeiro
author_facet Lemos, Leandro Nascimento
de Carvalho, Fabíola Marques
Gerber, Alexandra
Guimarães, Ana Paula C.
Jonck, Celio Roberto
Ciapina, Luciane Prioli
de Vasconcelos, Ana Tereza Ribeiro
author_sort Lemos, Leandro Nascimento
collection PubMed
description BACKGROUND: The Rhizobiales (Proteobacteria) order is an abundant and diverse group of microorganisms, being extensively studied for its lifestyle based on the association with plants, animals, and humans. New studies have demonstrated that the last common ancestor (LCA) of Rhizobiales had a free-living lifestyle, but the phylogenetic and metabolism characterization of basal lineages remains unclear. Here, we used a high-resolution phylogenomic approach to test the monophyly of the Aestuariivirgaceae family, a new taxonomic group of Rhizobiales. Furthermore, a deep metabolic investigation provided an overview of the main functional traits that can be associated with its lifestyle. We hypothesized that the presence of pathways (e.g., Glycolysis/Gluconeogenesis) and the absence of pathogenic genes would be associated with a free-living lifestyle in Aestuariivirgaceae. RESULTS: Using high-resolution phylogenomics approaches, our results revealed a clear separation of Aestuariivirgaceae into a distinct clade of other Rhizobiales family, suggesting a basal split early group and corroborate the monophyly of this group. A deep functional annotation indicated a metabolic versatility, which includes putative genes related to sugar degradation and aerobic respiration. Furthermore, many of these traits could reflect a basal metabolism and adaptations of Rhizobiales, as such the presence of Glycolysis/Gluconeogenesis pathway and the absence of pathogenicity genes, suggesting a free-living lifestyle in the Aestuariivirgaceae members. CONCLUSIONS: Aestuariivirgaceae (Rhizobiales) family is a monophyletic taxon of the Rhizobiales with a free-living lifestyle and a versatile metabolism that allows these microorganisms to survive in the most diverse microbiomes, demonstrating their adaptability to living in systems with different conditions, such as extremely cold environments to tropical rivers. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02354-4.
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spelling pubmed-85550842021-10-29 Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales Lemos, Leandro Nascimento de Carvalho, Fabíola Marques Gerber, Alexandra Guimarães, Ana Paula C. Jonck, Celio Roberto Ciapina, Luciane Prioli de Vasconcelos, Ana Tereza Ribeiro BMC Microbiol Research BACKGROUND: The Rhizobiales (Proteobacteria) order is an abundant and diverse group of microorganisms, being extensively studied for its lifestyle based on the association with plants, animals, and humans. New studies have demonstrated that the last common ancestor (LCA) of Rhizobiales had a free-living lifestyle, but the phylogenetic and metabolism characterization of basal lineages remains unclear. Here, we used a high-resolution phylogenomic approach to test the monophyly of the Aestuariivirgaceae family, a new taxonomic group of Rhizobiales. Furthermore, a deep metabolic investigation provided an overview of the main functional traits that can be associated with its lifestyle. We hypothesized that the presence of pathways (e.g., Glycolysis/Gluconeogenesis) and the absence of pathogenic genes would be associated with a free-living lifestyle in Aestuariivirgaceae. RESULTS: Using high-resolution phylogenomics approaches, our results revealed a clear separation of Aestuariivirgaceae into a distinct clade of other Rhizobiales family, suggesting a basal split early group and corroborate the monophyly of this group. A deep functional annotation indicated a metabolic versatility, which includes putative genes related to sugar degradation and aerobic respiration. Furthermore, many of these traits could reflect a basal metabolism and adaptations of Rhizobiales, as such the presence of Glycolysis/Gluconeogenesis pathway and the absence of pathogenicity genes, suggesting a free-living lifestyle in the Aestuariivirgaceae members. CONCLUSIONS: Aestuariivirgaceae (Rhizobiales) family is a monophyletic taxon of the Rhizobiales with a free-living lifestyle and a versatile metabolism that allows these microorganisms to survive in the most diverse microbiomes, demonstrating their adaptability to living in systems with different conditions, such as extremely cold environments to tropical rivers. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02354-4. BioMed Central 2021-10-28 /pmc/articles/PMC8555084/ /pubmed/34711170 http://dx.doi.org/10.1186/s12866-021-02354-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Lemos, Leandro Nascimento
de Carvalho, Fabíola Marques
Gerber, Alexandra
Guimarães, Ana Paula C.
Jonck, Celio Roberto
Ciapina, Luciane Prioli
de Vasconcelos, Ana Tereza Ribeiro
Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales
title Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales
title_full Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales
title_fullStr Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales
title_full_unstemmed Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales
title_short Genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in Rhizobiales
title_sort genome-centric metagenomics reveals insights into the evolution and metabolism of a new free-living group in rhizobiales
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8555084/
https://www.ncbi.nlm.nih.gov/pubmed/34711170
http://dx.doi.org/10.1186/s12866-021-02354-4
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