Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil Biorestoration

ABSTRACT The environmental deterioration produced by heavy metals derived from anthropogenic activities has gradually increased. The worldwide dissemination of toxic metals in crop soils represents a threat for sustainability and biosafety in agriculture and requires strategies for the recovery of m...

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Main Authors: Jesús Guzmán-Moreno, Luis Fernando García-Ortega, Lilia Torres-Saucedo, Paulina Rivas-Noriega, Rosa María Ramírez-Santoyo, Lenin Sánchez-Calderón, Iliana Noemi Quiroz-Serrano, Luz Elena Vidales-Rodríguez
Format: Article
Language:English
Published: American Society for Microbiology 2022-10-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.00656-22
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author Jesús Guzmán-Moreno
Luis Fernando García-Ortega
Lilia Torres-Saucedo
Paulina Rivas-Noriega
Rosa María Ramírez-Santoyo
Lenin Sánchez-Calderón
Iliana Noemi Quiroz-Serrano
Luz Elena Vidales-Rodríguez
author_facet Jesús Guzmán-Moreno
Luis Fernando García-Ortega
Lilia Torres-Saucedo
Paulina Rivas-Noriega
Rosa María Ramírez-Santoyo
Lenin Sánchez-Calderón
Iliana Noemi Quiroz-Serrano
Luz Elena Vidales-Rodríguez
author_sort Jesús Guzmán-Moreno
collection DOAJ
description ABSTRACT The environmental deterioration produced by heavy metals derived from anthropogenic activities has gradually increased. The worldwide dissemination of toxic metals in crop soils represents a threat for sustainability and biosafety in agriculture and requires strategies for the recovery of metal-polluted crop soils. The biorestoration of metal-polluted soils using technologies that combine plants and microorganisms has gained attention in recent decades due to the beneficial and synergistic effects produced by its biotic interactions. In this context, native and heavy metal-resistant plant growth-promoting bacteria (PGPB) play a crucial role in the development of strategies for sustainable biorestoration of metal-contaminated soils. In this study, we present a genomic analysis and characterization of the rhizospheric bacterium Bacillus megaterium HgT21 isolated from metal-polluted soil from Zacatecas, Mexico. The results reveal that this autochthonous bacterium contains an important set of genes related to a variety of operons associated with mercury, arsenic, copper, cobalt, cadmium, zinc and aluminum resistance. Additionally, halotolerance-, beta-lactam resistance-, phosphate solubilization-, and plant growth-promotion-related genes were identified. The analysis of resistance to metal ions revealed resistance to mercury (HgII+), arsenate [AsO4]³–, cobalt (Co2+), zinc (Zn2+), and copper (Cu2+). Moreover, the ability of the HgT21 strain to produce indole acetic acid (a phytohormone) and promote the growth of Arabidopsis thaliana seedlings in vitro was also demonstrated. The genotype and phenotype of Bacillus megaterium HgT21 reveal its potential to be used as a model of both plant growth-promoting and metal multiresistant bacteria. IMPORTANCE Metal-polluted environments are natural sources of a wide variety of PGPB adapted to cope with toxic metal concentrations. In this work, the bacterial strain Bacillus megaterium HgT21 was isolated from metal-contaminated soil and is proposed as a model for the study of metal multiresistance in spore-forming Gram-positive bacteria due to the presence of a variety of metal resistance-associated genes similar to those encountered in the metal multiresistant Gram-negative Cupriavidus metallidurans CH34. The ability of B. megaterium HgT21 to promote the growth of plants also makes it suitable for the study of plant-bacteria interactions in metal-polluted environments, which is key for the development of techniques for the biorestoration of metal-contaminated soils used for agriculture.
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spelling doaj.art-d5de714dd0894595af8c08889b4df2282022-12-22T04:34:37ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.00656-22Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil BiorestorationJesús Guzmán-Moreno0Luis Fernando García-Ortega1Lilia Torres-Saucedo2Paulina Rivas-Noriega3Rosa María Ramírez-Santoyo4Lenin Sánchez-Calderón5Iliana Noemi Quiroz-Serrano6Luz Elena Vidales-Rodríguez7Laboratorio de Biología de Bacterias y Hongos Filamentosos, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas, Zacatecas, Zacatecas, MexicoDepartamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV), Irapuato, Guanajuato, MexicoLaboratorio de Biología de Bacterias y Hongos Filamentosos, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas, Zacatecas, Zacatecas, MexicoLaboratorio de Biología de Bacterias y Hongos Filamentosos, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas, Zacatecas, Zacatecas, MexicoLaboratorio de Biología de Bacterias y Hongos Filamentosos, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas, Zacatecas, Zacatecas, MexicoLaboratorio de Genómica Evolutiva, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas, Zacatecas, Zacatecas, MexicoLaboratorio de Biología de Bacterias y Hongos Filamentosos, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas, Zacatecas, Zacatecas, MexicoLaboratorio de Biología de Bacterias y Hongos Filamentosos, Unidad Académica de Ciencias Biológicas, Universidad Autónoma de Zacatecas, Zacatecas, Zacatecas, MexicoABSTRACT The environmental deterioration produced by heavy metals derived from anthropogenic activities has gradually increased. The worldwide dissemination of toxic metals in crop soils represents a threat for sustainability and biosafety in agriculture and requires strategies for the recovery of metal-polluted crop soils. The biorestoration of metal-polluted soils using technologies that combine plants and microorganisms has gained attention in recent decades due to the beneficial and synergistic effects produced by its biotic interactions. In this context, native and heavy metal-resistant plant growth-promoting bacteria (PGPB) play a crucial role in the development of strategies for sustainable biorestoration of metal-contaminated soils. In this study, we present a genomic analysis and characterization of the rhizospheric bacterium Bacillus megaterium HgT21 isolated from metal-polluted soil from Zacatecas, Mexico. The results reveal that this autochthonous bacterium contains an important set of genes related to a variety of operons associated with mercury, arsenic, copper, cobalt, cadmium, zinc and aluminum resistance. Additionally, halotolerance-, beta-lactam resistance-, phosphate solubilization-, and plant growth-promotion-related genes were identified. The analysis of resistance to metal ions revealed resistance to mercury (HgII+), arsenate [AsO4]³–, cobalt (Co2+), zinc (Zn2+), and copper (Cu2+). Moreover, the ability of the HgT21 strain to produce indole acetic acid (a phytohormone) and promote the growth of Arabidopsis thaliana seedlings in vitro was also demonstrated. The genotype and phenotype of Bacillus megaterium HgT21 reveal its potential to be used as a model of both plant growth-promoting and metal multiresistant bacteria. IMPORTANCE Metal-polluted environments are natural sources of a wide variety of PGPB adapted to cope with toxic metal concentrations. In this work, the bacterial strain Bacillus megaterium HgT21 was isolated from metal-contaminated soil and is proposed as a model for the study of metal multiresistance in spore-forming Gram-positive bacteria due to the presence of a variety of metal resistance-associated genes similar to those encountered in the metal multiresistant Gram-negative Cupriavidus metallidurans CH34. The ability of B. megaterium HgT21 to promote the growth of plants also makes it suitable for the study of plant-bacteria interactions in metal-polluted environments, which is key for the development of techniques for the biorestoration of metal-contaminated soils used for agriculture.https://journals.asm.org/doi/10.1128/spectrum.00656-22Bacillus megateriummetal resistanceplant growth-promoting bacteriametal contamination
spellingShingle Jesús Guzmán-Moreno
Luis Fernando García-Ortega
Lilia Torres-Saucedo
Paulina Rivas-Noriega
Rosa María Ramírez-Santoyo
Lenin Sánchez-Calderón
Iliana Noemi Quiroz-Serrano
Luz Elena Vidales-Rodríguez
Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil Biorestoration
Microbiology Spectrum
Bacillus megaterium
metal resistance
plant growth-promoting bacteria
metal contamination
title Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil Biorestoration
title_full Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil Biorestoration
title_fullStr Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil Biorestoration
title_full_unstemmed Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil Biorestoration
title_short Bacillus megaterium HgT21: a Promising Metal Multiresistant Plant Growth-Promoting Bacteria for Soil Biorestoration
title_sort bacillus megaterium hgt21 a promising metal multiresistant plant growth promoting bacteria for soil biorestoration
topic Bacillus megaterium
metal resistance
plant growth-promoting bacteria
metal contamination
url https://journals.asm.org/doi/10.1128/spectrum.00656-22
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