Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With Plants

Beneficial 1-aminocyclopropane-1-carboxylate (ACC) deaminase-producing bacteria promote plant growth and stress resistance, constituting a sustainable alternative to the excessive use of chemicals in agriculture. In this work, the increased plant growth promotion activity of the ACC deaminase-produc...

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Main Authors: Francisco X. Nascimento, Paola Urón, Bernard R. Glick, Admir Giachini, Márcio J. Rossi
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.752288/full
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author Francisco X. Nascimento
Francisco X. Nascimento
Paola Urón
Bernard R. Glick
Admir Giachini
Márcio J. Rossi
author_facet Francisco X. Nascimento
Francisco X. Nascimento
Paola Urón
Bernard R. Glick
Admir Giachini
Márcio J. Rossi
author_sort Francisco X. Nascimento
collection DOAJ
description Beneficial 1-aminocyclopropane-1-carboxylate (ACC) deaminase-producing bacteria promote plant growth and stress resistance, constituting a sustainable alternative to the excessive use of chemicals in agriculture. In this work, the increased plant growth promotion activity of the ACC deaminase-producing Pseudomonas thivervalensis SC5, its ability to limit the growth of phytopathogens, and the genomics behind these important properties are described in detail. P. thivervalensis SC5 displayed several active plant growth promotion traits and significantly increased cucumber plant growth and resistance against salt stress (100mmol/L NaCl) under greenhouse conditions. Strain SC5 also limited the in vitro growth of the pathogens Botrytis cinerea and Pseudomonas syringae DC3000 indicating active biological control activities. Comprehensive analysis revealed that P. thivervalensis SC5 genome is rich in genetic elements involved in nutrient acquisition (N, P, S, and Fe); osmotic stress tolerance (e.g., glycine-betaine, trehalose, and ectoine biosynthesis); motility, chemotaxis and attachment to plant tissues; root exudate metabolism including the modulation of plant phenolics (e.g., hydroxycinnamic acids), lignin, and flavonoids (e.g., quercetin); resistance against plant defenses (e.g., reactive oxygens species-ROS); plant hormone modulation (e.g., ethylene, auxins, cytokinins, and salicylic acid), and bacterial and fungal phytopathogen antagonistic traits (e.g., 2,4-diacetylphloroglucinol, HCN, a fragin-like non ribosomal peptide, bacteriocins, a lantipeptide, and quorum-quenching activities), bringing detailed insights into the action of this versatile plant-growth-promoting bacterium. Ultimately, the combination of both increased plant growth promotion/protection and biological control abilities makes P. thivervalensis SC5 a prime candidate for its development as a biofertilizer/biostimulant/biocontrol product. The genomic analysis of this bacterium brings new insights into the functioning of Pseudomonas and their role in beneficial plant-microbe interactions.
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spelling doaj.art-013191c6d9a8412f81f6f4692dc2465c2022-12-21T21:30:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.752288752288Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With PlantsFrancisco X. Nascimento0Francisco X. Nascimento1Paola Urón2Bernard R. Glick3Admir Giachini4Márcio J. Rossi5iBET, Instituto de Biologia Experimental e Tecnológica, Oeiras, PortugalLaboratório de Microbiologia e Bioprocessos, Departamento de Microbiologia, Universidade Federal de Santa Catarina, Florianópolis, BrazilLaboratório de Microbiologia e Bioprocessos, Departamento de Microbiologia, Universidade Federal de Santa Catarina, Florianópolis, BrazilDepartment of Biology, University of Waterloo, Waterloo, ON, CanadaLaboratório de Microbiologia e Bioprocessos, Departamento de Microbiologia, Universidade Federal de Santa Catarina, Florianópolis, BrazilLaboratório de Microbiologia e Bioprocessos, Departamento de Microbiologia, Universidade Federal de Santa Catarina, Florianópolis, BrazilBeneficial 1-aminocyclopropane-1-carboxylate (ACC) deaminase-producing bacteria promote plant growth and stress resistance, constituting a sustainable alternative to the excessive use of chemicals in agriculture. In this work, the increased plant growth promotion activity of the ACC deaminase-producing Pseudomonas thivervalensis SC5, its ability to limit the growth of phytopathogens, and the genomics behind these important properties are described in detail. P. thivervalensis SC5 displayed several active plant growth promotion traits and significantly increased cucumber plant growth and resistance against salt stress (100mmol/L NaCl) under greenhouse conditions. Strain SC5 also limited the in vitro growth of the pathogens Botrytis cinerea and Pseudomonas syringae DC3000 indicating active biological control activities. Comprehensive analysis revealed that P. thivervalensis SC5 genome is rich in genetic elements involved in nutrient acquisition (N, P, S, and Fe); osmotic stress tolerance (e.g., glycine-betaine, trehalose, and ectoine biosynthesis); motility, chemotaxis and attachment to plant tissues; root exudate metabolism including the modulation of plant phenolics (e.g., hydroxycinnamic acids), lignin, and flavonoids (e.g., quercetin); resistance against plant defenses (e.g., reactive oxygens species-ROS); plant hormone modulation (e.g., ethylene, auxins, cytokinins, and salicylic acid), and bacterial and fungal phytopathogen antagonistic traits (e.g., 2,4-diacetylphloroglucinol, HCN, a fragin-like non ribosomal peptide, bacteriocins, a lantipeptide, and quorum-quenching activities), bringing detailed insights into the action of this versatile plant-growth-promoting bacterium. Ultimately, the combination of both increased plant growth promotion/protection and biological control abilities makes P. thivervalensis SC5 a prime candidate for its development as a biofertilizer/biostimulant/biocontrol product. The genomic analysis of this bacterium brings new insights into the functioning of Pseudomonas and their role in beneficial plant-microbe interactions.https://www.frontiersin.org/articles/10.3389/fmicb.2021.752288/fullPseudomonasplant-growth-promoting bacteria1-aminocyclopropane-1-carboxylate deaminasegenomicsplant-microbe interaction
spellingShingle Francisco X. Nascimento
Francisco X. Nascimento
Paola Urón
Bernard R. Glick
Admir Giachini
Márcio J. Rossi
Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With Plants
Frontiers in Microbiology
Pseudomonas
plant-growth-promoting bacteria
1-aminocyclopropane-1-carboxylate deaminase
genomics
plant-microbe interaction
title Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With Plants
title_full Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With Plants
title_fullStr Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With Plants
title_full_unstemmed Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With Plants
title_short Genomic Analysis of the 1-Aminocyclopropane-1-Carboxylate Deaminase-Producing Pseudomonas thivervalensis SC5 Reveals Its Multifaceted Roles in Soil and in Beneficial Interactions With Plants
title_sort genomic analysis of the 1 aminocyclopropane 1 carboxylate deaminase producing pseudomonas thivervalensis sc5 reveals its multifaceted roles in soil and in beneficial interactions with plants
topic Pseudomonas
plant-growth-promoting bacteria
1-aminocyclopropane-1-carboxylate deaminase
genomics
plant-microbe interaction
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.752288/full
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