Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization

Despite the availability of data on the functional and phylogenetic diversity of plant-associated microbiota, the molecular mechanisms governing the successful establishment of plant bacterial communities remain mostly elusive. To investigate bacterial traits associated with successful colonization...

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Main Authors: Rafael Soares Correa de Souza, Jaderson Silveira Leite Armanhi, Natália de Brito Damasceno, Juan Imperial, Paulo Arruda
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01779/full
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author Rafael Soares Correa de Souza
Rafael Soares Correa de Souza
Rafael Soares Correa de Souza
Jaderson Silveira Leite Armanhi
Jaderson Silveira Leite Armanhi
Jaderson Silveira Leite Armanhi
Natália de Brito Damasceno
Natália de Brito Damasceno
Natália de Brito Damasceno
Juan Imperial
Juan Imperial
Paulo Arruda
Paulo Arruda
Paulo Arruda
author_facet Rafael Soares Correa de Souza
Rafael Soares Correa de Souza
Rafael Soares Correa de Souza
Jaderson Silveira Leite Armanhi
Jaderson Silveira Leite Armanhi
Jaderson Silveira Leite Armanhi
Natália de Brito Damasceno
Natália de Brito Damasceno
Natália de Brito Damasceno
Juan Imperial
Juan Imperial
Paulo Arruda
Paulo Arruda
Paulo Arruda
author_sort Rafael Soares Correa de Souza
collection DOAJ
description Despite the availability of data on the functional and phylogenetic diversity of plant-associated microbiota, the molecular mechanisms governing the successful establishment of plant bacterial communities remain mostly elusive. To investigate bacterial traits associated with successful colonization of plants, we sequenced the genome of 26 bacteria of a synthetic microbial community (SynCom), 12 of which displayed robust and 14 displayed non-robust colonization lifestyles when inoculated in maize plants. We examined the colonization profile of individual bacteria in inoculated plants and inspected their genomes for traits correlated to the colonization lifestyle. Comparative genomic analysis between robust and non-robust bacteria revealed that commonly investigated plant growth-promoting features such as auxin production, nitrogen (N) fixation, phosphate acquisition, and ACC deaminase are not deterministic for robust colonization. Functions related to carbon (C) and N acquisition, including transporters of carbohydrates and amino acids, and kinases involved in signaling mechanisms associated with C and N uptake, were enriched in robust colonizers. While enrichment of carbohydrate transporters was linked to a wide range of metabolites, amino acid transporters were primarily related to the uptake of branched-chain amino acids. Our findings identify diversification of nutrient uptake phenotypes in bacteria as determinants for successful bacterial colonization of plants.
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spelling doaj.art-0e33731df37448ca863c49160c973ca22022-12-22T01:29:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-08-011010.3389/fmicb.2019.01779436354Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant ColonizationRafael Soares Correa de Souza0Rafael Soares Correa de Souza1Rafael Soares Correa de Souza2Jaderson Silveira Leite Armanhi3Jaderson Silveira Leite Armanhi4Jaderson Silveira Leite Armanhi5Natália de Brito Damasceno6Natália de Brito Damasceno7Natália de Brito Damasceno8Juan Imperial9Juan Imperial10Paulo Arruda11Paulo Arruda12Paulo Arruda13Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas, Campinas, BrazilDepartamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, BrazilGenomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas, Campinas, BrazilCentro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas, Campinas, BrazilDepartamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, BrazilGenomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas, Campinas, BrazilCentro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas, Campinas, BrazilDepartamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, BrazilGenomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas, Campinas, BrazilCentro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Campus Montegancedo UPM, Madrid, SpainInstituto de Ciencias Agrarias, Consejo Superior de Investigaciones Científicas, Madrid, SpainCentro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas, Campinas, BrazilDepartamento de Genética e Evolução, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, BrazilGenomics for Climate Change Research Center (GCCRC), Universidade Estadual de Campinas, Campinas, BrazilDespite the availability of data on the functional and phylogenetic diversity of plant-associated microbiota, the molecular mechanisms governing the successful establishment of plant bacterial communities remain mostly elusive. To investigate bacterial traits associated with successful colonization of plants, we sequenced the genome of 26 bacteria of a synthetic microbial community (SynCom), 12 of which displayed robust and 14 displayed non-robust colonization lifestyles when inoculated in maize plants. We examined the colonization profile of individual bacteria in inoculated plants and inspected their genomes for traits correlated to the colonization lifestyle. Comparative genomic analysis between robust and non-robust bacteria revealed that commonly investigated plant growth-promoting features such as auxin production, nitrogen (N) fixation, phosphate acquisition, and ACC deaminase are not deterministic for robust colonization. Functions related to carbon (C) and N acquisition, including transporters of carbohydrates and amino acids, and kinases involved in signaling mechanisms associated with C and N uptake, were enriched in robust colonizers. While enrichment of carbohydrate transporters was linked to a wide range of metabolites, amino acid transporters were primarily related to the uptake of branched-chain amino acids. Our findings identify diversification of nutrient uptake phenotypes in bacteria as determinants for successful bacterial colonization of plants.https://www.frontiersin.org/article/10.3389/fmicb.2019.01779/fullsynthetic microbial community (SynCom)plant microbiomebacterial genomeplant–microbe associationplant-beneficial bacteria
spellingShingle Rafael Soares Correa de Souza
Rafael Soares Correa de Souza
Rafael Soares Correa de Souza
Jaderson Silveira Leite Armanhi
Jaderson Silveira Leite Armanhi
Jaderson Silveira Leite Armanhi
Natália de Brito Damasceno
Natália de Brito Damasceno
Natália de Brito Damasceno
Juan Imperial
Juan Imperial
Paulo Arruda
Paulo Arruda
Paulo Arruda
Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization
Frontiers in Microbiology
synthetic microbial community (SynCom)
plant microbiome
bacterial genome
plant–microbe association
plant-beneficial bacteria
title Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization
title_full Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization
title_fullStr Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization
title_full_unstemmed Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization
title_short Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization
title_sort genome sequences of a plant beneficial synthetic bacterial community reveal genetic features for successful plant colonization
topic synthetic microbial community (SynCom)
plant microbiome
bacterial genome
plant–microbe association
plant-beneficial bacteria
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01779/full
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