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Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds

INTRODUCTION: Bradyrhizobium diazoefficiens, a symbiotic nitrogen fixer for soybean, forms nodules after developing a symbiotic association with the root. For this association, bacteria need to move toward and attach to the root. These steps are mediated by the surface and phenotypic cell properties...

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Autores principales: Sandhu, Armaan Kaur, Brown, McKenzie Rae, Subramanian, Senthil, Brözel, Volker S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10233038/
https://www.ncbi.nlm.nih.gov/pubmed/37275139
http://dx.doi.org/10.3389/fmicb.2023.1190396
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author Sandhu, Armaan Kaur
Brown, McKenzie Rae
Subramanian, Senthil
Brözel, Volker S.
author_facet Sandhu, Armaan Kaur
Brown, McKenzie Rae
Subramanian, Senthil
Brözel, Volker S.
author_sort Sandhu, Armaan Kaur
collection PubMed
description INTRODUCTION: Bradyrhizobium diazoefficiens, a symbiotic nitrogen fixer for soybean, forms nodules after developing a symbiotic association with the root. For this association, bacteria need to move toward and attach to the root. These steps are mediated by the surface and phenotypic cell properties of bacteria and secreted root exudate compounds. Immense work has been carried out on nodule formation and nitrogen fixation, but little is known about the phenotype of these microorganisms under the influence of different root exudate chemical compounds (RECCs) or how this phenotype impacts the root attachment ability. METHODS: To address this knowledge gap, we studied the impact of 12 different RECCs, one commonly used carbon source, and soil-extracted solubilized organic matter (SESOM) on attachment and attachment-related properties of B. diazoefficiens USDA110. We measured motility-related properties (swimming, swarming, chemotaxis, and flagellar expression), attachment-related properties (surface hydrophobicity, biofilm formation, and attachment to cellulose and soybean roots), and surface polysaccharide properties (colony morphology, exopolysaccharide quantification, lectin binding profile, and lipopolysaccharide profiling). RESULTS AND DISCUSSION: We found that USDA 110 displays a high degree of surface phenotypic plasticity when grown on the various individual RECCs. Some of the RECCs played specific roles in modulating the motility and root attachment processes. Serine increased cell surface hydrophobicity and root and cellulose attachment, with no EPS formed. Gluconate and lactate increased EPS production and biofilm formation, while decreasing hydrophobicity and root attachment, and raffinose and gentisate promoted motility and chemotaxis. The results also indicated that the biofilm formation trait on hydrophilic surfaces (polystyrene) cannot be related to the attachment ability of Bradyrhizobium to the soybean root. Among the tested phenotypic properties, bacterial cell surface hydrophobicity was the one with a significant impact on root attachment ability. We conclude that USDA 110 displays surface plasticity properties and attachment phenotype determined by individual RECCs from the soybean. Conclusions made based on its behavior in standard carbon sources, such as arabinose or mannitol, do not hold for its behavior in soil.
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spelling pubmed-102330382023-06-02 Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds Sandhu, Armaan Kaur Brown, McKenzie Rae Subramanian, Senthil Brözel, Volker S. Front Microbiol Microbiology INTRODUCTION: Bradyrhizobium diazoefficiens, a symbiotic nitrogen fixer for soybean, forms nodules after developing a symbiotic association with the root. For this association, bacteria need to move toward and attach to the root. These steps are mediated by the surface and phenotypic cell properties of bacteria and secreted root exudate compounds. Immense work has been carried out on nodule formation and nitrogen fixation, but little is known about the phenotype of these microorganisms under the influence of different root exudate chemical compounds (RECCs) or how this phenotype impacts the root attachment ability. METHODS: To address this knowledge gap, we studied the impact of 12 different RECCs, one commonly used carbon source, and soil-extracted solubilized organic matter (SESOM) on attachment and attachment-related properties of B. diazoefficiens USDA110. We measured motility-related properties (swimming, swarming, chemotaxis, and flagellar expression), attachment-related properties (surface hydrophobicity, biofilm formation, and attachment to cellulose and soybean roots), and surface polysaccharide properties (colony morphology, exopolysaccharide quantification, lectin binding profile, and lipopolysaccharide profiling). RESULTS AND DISCUSSION: We found that USDA 110 displays a high degree of surface phenotypic plasticity when grown on the various individual RECCs. Some of the RECCs played specific roles in modulating the motility and root attachment processes. Serine increased cell surface hydrophobicity and root and cellulose attachment, with no EPS formed. Gluconate and lactate increased EPS production and biofilm formation, while decreasing hydrophobicity and root attachment, and raffinose and gentisate promoted motility and chemotaxis. The results also indicated that the biofilm formation trait on hydrophilic surfaces (polystyrene) cannot be related to the attachment ability of Bradyrhizobium to the soybean root. Among the tested phenotypic properties, bacterial cell surface hydrophobicity was the one with a significant impact on root attachment ability. We conclude that USDA 110 displays surface plasticity properties and attachment phenotype determined by individual RECCs from the soybean. Conclusions made based on its behavior in standard carbon sources, such as arabinose or mannitol, do not hold for its behavior in soil. Frontiers Media S.A. 2023-05-18 /pmc/articles/PMC10233038/ /pubmed/37275139 http://dx.doi.org/10.3389/fmicb.2023.1190396 Text en Copyright © 2023 Sandhu, Brown, Subramanian and Brözel. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Sandhu, Armaan Kaur
Brown, McKenzie Rae
Subramanian, Senthil
Brözel, Volker S.
Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds
title Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds
title_full Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds
title_fullStr Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds
title_full_unstemmed Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds
title_short Bradyrhizobium diazoefficiens USDA 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds
title_sort bradyrhizobium diazoefficiens usda 110 displays plasticity in the attachment phenotype when grown in different soybean root exudate compounds
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10233038/
https://www.ncbi.nlm.nih.gov/pubmed/37275139
http://dx.doi.org/10.3389/fmicb.2023.1190396
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