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Use of Endophytic and Rhizosphere Bacteria to Improve Use of Endophytic and Rhizosphere Bacteria To Improve Phytoremediation of Arsenic-Contaminated Industrial Soils by Autochthonous Betula celtiberica Victoria Mesa, Alejandro Navazas, Ricardo González, Aida González, Nele Weyens, Béatrice Lauga, Jose Luis R. Gallego, Jesús Sánchez, Ana Isabel Peláez To cite this version: Victoria Mesa, Alejandro Navazas, Ricardo González, Aida González, Nele Weyens, et al.. Use of Endophytic and Rhizosphere Bacteria To Improve Phytoremediation of Arsenic-Contaminated Indus- trial Soils by Autochthonous Betula celtiberica. Applied and Environmental Microbiology, American Society for Microbiology, 2017, 83 (8), 10.1128/AEM.03411-16. hal-01644095 HAL Id: hal-01644095 https://hal.archives-ouvertes.fr/hal-01644095 Submitted on 11 Jan 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. ENVIRONMENTAL MICROBIOLOGY crossm Use of Endophytic and Rhizosphere Bacteria To Improve Phytoremediation of Arsenic-Contaminated Industrial Soils Downloaded from by Autochthonous Betula celtiberica Victoria Mesa,a Alejandro Navazas,b,c Ricardo González-Gil,b Aida González,b Nele Weyens,c Béatrice Lauga,d Jose Luis R. Gallego,e Jesús Sánchez,a Ana Isabel Peláeza a Departamento de Biología Funcional–IUBA, Universidad de Oviedo, Oviedo, Spain ; Departamento de Biología http://aem.asm.org/ de Organismos y Sistemas–IUBA, Universidad de Oviedo, Oviedo, Spainb; Centre for Environmental Sciences (CMK), Hasselt University, Hasselt, Belgiumc; Equipe Environnement et Microbiologie (EEM), CNRS/Univ. Pau et des Pays Adour, Institut des sciences analytiques et de physico-chimie pour l'environnement et les matériaux- IPREM, UMR5254, Pau, Franced; Departamento de Explotación y Prospección Minera–IUBA, Universidad de Oviedo, Mieres, Spaine ABSTRACT The aim of this study was to investigate the potential of indigenous arsenic-tolerant bacteria to enhance arsenic phytoremediation by the autochthonous Received 16 December 2016 Accepted 6 February 2017 on April 6, 2017 by UNIVERSIDAD DE OVIEDO pseudometallophyte Betula celtiberica. The first goal was to perform an initial analy- Accepted manuscript posted online 10 sis of the entire rhizosphere and endophytic bacterial communities of the above- February 2017 named accumulator plant, including the cultivable bacterial species. B. celtiberica’s Citation Mesa V, Navazas A, González-Gil R, microbiome was dominated by taxa related to Flavobacteriales, Burkholderiales, and González A, Weyens N, Lauga B, Gallego JLR, Sánchez J, Peláez AI. 2017. Use of endophytic Pseudomonadales, especially the Pseudomonas and Flavobacterium genera. A total of and rhizosphere bacteria to improve 54 cultivable rhizobacteria and 41 root endophytes, mainly affiliated with the phyla phytoremediation of arsenic-contaminated Proteobacteria, Bacteroidetes, Firmicutes, and Actinobacteria, were isolated and charac- industrial soils by autochthonous Betula celtiberica. Appl Environ Microbiol 83:e03411- terized with respect to several potentially useful features for metal plant accumula- 16. https://doi.org/10.1128/AEM.03411-16. tion, such as the ability to promote plant growth, metal chelation, and/or mitigation Editor Harold L. Drake, University of Bayreuth of heavy-metal stress. Seven bacterial isolates were further selected and tested for in Copyright © 2017 American Society for vitro accumulation of arsenic in plants; four of them were finally assayed in field- Microbiology. All Rights Reserved. Address correspondence to Victoria Mesa, scale bioaugmentation experiments. The exposure to arsenic in vitro caused an increase [email protected]. in the total nonprotein thiol compound content in roots, suggesting a detoxifica- tion mechanism through phytochelatin complexation. In the contaminated field, the siderophore and indole-3-acetic acid producers of the endophytic bacterial consortium enhanced arsenic accumulation in the leaves and roots of Betula celti- berica, whereas the rhizosphere isolate Ensifer adhaerens strain 91R mainly promoted plant growth. Field experimentation showed that additional factors, such as soil ar- senic content and pH, influenced arsenic uptake in the plant, attesting to the rele- vance of field conditions in the success of phytoextraction strategies. IMPORTANCE Microorganisms and plants have developed several ways of dealing with arsenic, allowing them to resist and metabolize this metalloid. These properties form the basis of phytoremediation treatments and the understanding that the in- teractions of plants with soil bacteria are crucial for the optimization of arsenic up- take. To address this in our work, we initially performed a microbiome analysis of the autochthonous Betula celtiberica plants growing in arsenic-contaminated soils, in- cluding endosphere and rhizosphere bacterial communities. We then proceeded to isolate and characterize the cultivable bacteria that were potentially better suited to enhance phytoextraction efficiency. Eventually, we went to the field application stage. Our results corroborated the idea that recovery of pseudometallophyte- associated bacteria adapted to a large historically contaminated site and their use in April 2017 Volume 83 Issue 8 e03411-16 Applied and Environmental Microbiology aem.asm.org 1 Mesa et al. Applied and Environmental Microbiology bioaugmentation technologies are affordable experimental approaches and poten- tially very useful for implementing effective phytoremediation strategies with plants and their indigenous bacteria. KEYWORDS contaminated soil, arsenic, root endophytes, rhizobacteria, Betula, field- scale study, phytoextraction, bioaugmentation rsenic (As) is a natural component of the earth’s crust and is widely distributed Athroughout the environment (air, water, and land). Other sources of environmental arsenic are anthropogenic, e.g., insecticides, mining, industrial processes, coal combus- Downloaded from tion, timber preservatives, etc. (1). High concentrations of As lead to environmental damage and health problems (2, 3). Arsenic exists in four oxidation states, predomi- nantly arsenate [As(V)] and arsenite [As(III)] and to a lesser extent arsenic [As(0)] and arsine As(ϪIII) (4, 5). As(V) is a phosphate analogue and interferes with essential cellular processes, such as oxidative phosphorylation and ATP synthesis, whereas the toxicity of As(III) is due to its tendency to bind to sulfhydryl groups, affecting general protein functioning (6). http://aem.asm.org/ A sustainable technology for cleaning As-contaminated soils is phytoremediation, which is defined as the use of plants to remove or reduce toxic concentrations of hazardous substances in the environment (7). As part of As detoxification, plants produce metabolites, like nonprotein thiols (NPTs), cysteine, glutathione (GSH), or phytochelatins (PCs) synthe- sized from GSH, which are involved in the defense pathways of plants against As-induced oxidative stress (8). PCs have been identified in plants and some microorganisms (9). Phytoremediation of As-, Cd-, and Pb-contaminated soils is more cost-effective, more efficient, and less time-consuming than most other remediation technologies (10). on April 6, 2017 by UNIVERSIDAD DE OVIEDO Phytoremediation can reduce the available concentrations of inorganic compounds through different processes, such as phytoextraction, rhizofiltration, phytostabilization, or phytovolatilization (11, 12). Phytoextraction seeks to remove inorganic contami- nants, especially heavy metals, metalloids, and radionuclides, from contaminated soils through uptake by plants and accumulation in harvestable plant biomass (13). Microbial processes play a major role in As cycling in the plant-soil-microbe system, and effective phytoremediation of contaminated soils involves interactions with plant- associated microbes (14). Some bacterial mechanisms that enhance phytoremediation consist of plant growth by bacterial metabolites, such as indole-3-acetic acid (IAA), metal chelation by siderophores, and organic acid production, soil acidification, solu- bilization of metal phosphates, methylation, and moderation of heavy-metal stress by bacterial 1-amino-cyclopropane-1-carboxylic acid deaminase (ACCD) (15, 16). Rhizobac- teria that colonize the vicinity of roots accelerate metal mobility and plant availability by various processes, including redox transformations and the release of protons and organic acids, whereas endophytic bacteria colonize the internal tissues of plants and promote plant growth through mechanisms such as phosphate solubilization, IAA and sid- erophore production, and/or supplying essential vitamins to plants (17, 18). In addition to their tolerance for heavy-metal stress, plant-associated bacteria can act as biocontrol agents against certain pathogenic organisms and ensure nitrogen fixation and the production of growth regulators (19). In Asturias (northeastern Spain), several areas are contaminated with arsenic as a result of recent industrial (chemical, metallurgical, and siderurgical) dismantling. A representative example of a large-scale contaminated site
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