Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation

Rhizoremediation is based on the ability of microorganisms to metabolize nutrients from plant root exudates and, thereby, to cometabolize or even mineralize toxic environmental contaminants. Novosphingobium sp. HR1a is a bacterial strain able to degrade a wide variety of polycyclic aromatic hydrocar...

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Autores: Molina Delgado, Lázaro, Udaondo, Zulema, Montero-Curiel, María, Wittich, Regina Michaela, García-Puente, Alicia, Segura, Ana
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2021
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/255147
Acceso en línea:http://hdl.handle.net/10261/255147
Access Level:acceso abierto
Palabra clave:Clover exudates
Phenomics
Metabolomics
Gene expression
Rhizoremediation
Polycyclic aromatic hydrocarbons (PAHs)
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
title Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
spellingShingle Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
Molina Delgado, Lázaro
Clover exudates
Phenomics
Metabolomics
Gene expression
Rhizoremediation
Polycyclic aromatic hydrocarbons (PAHs)
title_short Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
title_full Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
title_fullStr Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
title_full_unstemmed Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
title_sort Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediation
dc.creator.none.fl_str_mv Molina Delgado, Lázaro
Udaondo, Zulema
Montero-Curiel, María
Wittich, Regina Michaela
García-Puente, Alicia
Segura, Ana
author Molina Delgado, Lázaro
author_facet Molina Delgado, Lázaro
Udaondo, Zulema
Montero-Curiel, María
Wittich, Regina Michaela
García-Puente, Alicia
Segura, Ana
author_role author
author2 Udaondo, Zulema
Montero-Curiel, María
Wittich, Regina Michaela
García-Puente, Alicia
Segura, Ana
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv European Commission
Ministerio de Ciencia e Innovación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Clover exudates
Phenomics
Metabolomics
Gene expression
Rhizoremediation
Polycyclic aromatic hydrocarbons (PAHs)
topic Clover exudates
Phenomics
Metabolomics
Gene expression
Rhizoremediation
Polycyclic aromatic hydrocarbons (PAHs)
description Rhizoremediation is based on the ability of microorganisms to metabolize nutrients from plant root exudates and, thereby, to cometabolize or even mineralize toxic environmental contaminants. Novosphingobium sp. HR1a is a bacterial strain able to degrade a wide variety of polycyclic aromatic hydrocarbons (PAHs). Here, we have demonstrated that the number of CFU in microcosms vegetated with clover was almost 2 orders of magnitude higher than that in nonvegetated microcosms or microcosms vegetated with rye-grass or grass. Strain HR1a was able to eliminate 92% of the phenanthrene in the microcosms with clover after 9 days. We have studied the molecular basis of the interaction between strain HR1a and clover by phenomic, metabolomic, and transcriptomic analyses. By measuring the relative concentrations of several metabolites exudated by clover both in the presence and in the absence of the bacteria, we identified some compounds that were probably consumed in the rhizosphere; the transcriptomic analyses confirmed the expression of genes involved in the catabolism of these compounds. By using a transcriptional fusion of the green fluorescent protein (GFP) to the promoter of the gene encoding the dioxygenase involved in the degradation of PAHs, we have demonstrated that this gene is induced at higher levels in clover microcosms than in nonvegetated microcosms. Therefore, the positive interaction between clover and Novosphingobium sp. HR1a during rhizoremediation is a result of the bacterial utilization of different carbon and nitrogen sources released during seedling development and the capacity of clover exudates to induce the PAH degradation pathway. IMPORTANCE The success of an eco-friendly and cost-effective strategy for soil decontamination is conditioned by the understanding of the ecology of plant-microorganism interactions. Although many studies have been published about the bacterial metabolic capacities in the rhizosphere and about rhizoremediation of contaminants, there are fewer studies dealing with the integration of bacterial metabolic capacities in the rhizosphere during PAH bioremediation, and some aspects still remain controversial. Some authors have postulated that the presence of easily metabolizable carbon sources in root exudates might repress the expression of genes required for contaminant degradation, while others found that specific rhizosphere compounds can induce such genes. Novosphingobium sp. HR1a, which is our model organism, has two characteristics desirable in bacteria for use in remediation: its ubiquity and the capacity to degrade a wide variety of contaminants. We have demonstrated that this bacterium consumes several rhizospheric compounds without repression of the genes required for the mineralization of PAHs. In fact, some compounds even induced their expression.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/255147
url http://hdl.handle.net/10261/255147
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-85994-P
http://dx.doi.org/10.1128/mSphere.00412-21
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Clover root exudates favor novosphingobium sp. HR1a establishment in the rhizosphere and promote phenanthrene rhizoremediationMolina Delgado, LázaroUdaondo, ZulemaMontero-Curiel, MaríaWittich, Regina MichaelaGarcía-Puente, AliciaSegura, AnaClover exudatesPhenomicsMetabolomicsGene expressionRhizoremediationPolycyclic aromatic hydrocarbons (PAHs)Rhizoremediation is based on the ability of microorganisms to metabolize nutrients from plant root exudates and, thereby, to cometabolize or even mineralize toxic environmental contaminants. Novosphingobium sp. HR1a is a bacterial strain able to degrade a wide variety of polycyclic aromatic hydrocarbons (PAHs). Here, we have demonstrated that the number of CFU in microcosms vegetated with clover was almost 2 orders of magnitude higher than that in nonvegetated microcosms or microcosms vegetated with rye-grass or grass. Strain HR1a was able to eliminate 92% of the phenanthrene in the microcosms with clover after 9 days. We have studied the molecular basis of the interaction between strain HR1a and clover by phenomic, metabolomic, and transcriptomic analyses. By measuring the relative concentrations of several metabolites exudated by clover both in the presence and in the absence of the bacteria, we identified some compounds that were probably consumed in the rhizosphere; the transcriptomic analyses confirmed the expression of genes involved in the catabolism of these compounds. By using a transcriptional fusion of the green fluorescent protein (GFP) to the promoter of the gene encoding the dioxygenase involved in the degradation of PAHs, we have demonstrated that this gene is induced at higher levels in clover microcosms than in nonvegetated microcosms. Therefore, the positive interaction between clover and Novosphingobium sp. HR1a during rhizoremediation is a result of the bacterial utilization of different carbon and nitrogen sources released during seedling development and the capacity of clover exudates to induce the PAH degradation pathway. IMPORTANCE The success of an eco-friendly and cost-effective strategy for soil decontamination is conditioned by the understanding of the ecology of plant-microorganism interactions. Although many studies have been published about the bacterial metabolic capacities in the rhizosphere and about rhizoremediation of contaminants, there are fewer studies dealing with the integration of bacterial metabolic capacities in the rhizosphere during PAH bioremediation, and some aspects still remain controversial. Some authors have postulated that the presence of easily metabolizable carbon sources in root exudates might repress the expression of genes required for contaminant degradation, while others found that specific rhizosphere compounds can induce such genes. Novosphingobium sp. HR1a, which is our model organism, has two characteristics desirable in bacteria for use in remediation: its ubiquity and the capacity to degrade a wide variety of contaminants. We have demonstrated that this bacterium consumes several rhizospheric compounds without repression of the genes required for the mineralization of PAHs. In fact, some compounds even induced their expression.This work was supported by the European Regional Development Fund FEDER and a grant from the Spanish Ministry of Science and Innovation (grant number BIO2017-85994-P).American Society for MicrobiologyEuropean CommissionMinisterio de Ciencia e Innovación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2021202120212021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/255147reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BIO2017-85994-Phttp://dx.doi.org/10.1128/mSphere.00412-21Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2551472026-05-22T06:33:51Z
score 15,81155

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