Enhancing the Phytoremediation of Heavy Metals by Combining Hyperaccumulator and Heavy Metal-Resistant Plant Growth-Promoting Bacteria
Abstract
Heavy metals (HMs) have become a major environmental pollutant threatening ecosystems and human health. Although hyperaccumulators provide a viable alternative for the bioremediation of HMs, the potential of phytoremediation is often limited by the small biomass and slow growth rate of hyperaccumulators and HM toxicity to plants. Here, plant growth-promoting bacteria (PGPB)-assisted phytoremediation was used to enhance the phytoremediation of HM-contaminated soils. A PGPB with HM-tolerant (HMT-PGPB), Bacillus sp. PGP15 was isolated from the rhizosphere of a cadmium (Cd) hyperaccumulator, Solanum nigrum . Pot experiments demonstrated that inoculation with strain PGP15 could significantly increase the growth of S. nigrum . More importantly, strain PGP15 markedly improved Cd accumulation in S. nigrum while alleviating Cd-induced stress in S. nigrum . Specifically, PGP15 inoculation significantly decreased the contents of H 2 O 2 , MDA, and in S. nigrum , while the activities (per gram plant fresh weight) of SOD, APX, and CAT were significantly increased in the PGP15-inoculated plants compared with the control sample. These results suggested that the interactions between strain PGP15 and S. nigrum could overcome the limits of phytoremediation alone and highlighted the promising application potential of the PGPB-hyperaccumulator collaborative pattern in the bioremediation of HM-contaminated soils. Furthermore, the PGP15 genome was sequenced and compared with other strains to explore the mechanisms underlying plant growth promotion by HMT-PGPB. The results showed that core genes that define the fundamental metabolic capabilities of strain PGP15 might not be necessary for plant growth promotion. Meanwhile, PGP15-specific genes, including many transposable elements, played a crucial role in the adaptive evolution of HM resistance. Overall, our results improve the understanding of interactions between HMT-PGPB and plants and facilitate the application of HMT-PGPB in the phytoremediation of HM-contaminated soils.
- Authors:
- Publication Date:
- Sponsoring Org.:
- USDOE Office of Electricity (OE), Advanced Grid Research & Development. Power Systems Engineering Research
- OSTI Identifier:
- 1871067
- Grant/Contract Number:
- BE2021718; 2016YFD0800803
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Name: Frontiers in Plant Science Journal Volume: 13; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
Citation Formats
Zhang, Yong, Zhao, Shangjun, Liu, Sijia, Peng, Jing, Zhang, Hanchao, Zhao, Qiming, Zheng, Luqing, Chen, Yahua, Shen, Zhenguo, Xu, Xihui, and Chen, Chen. Enhancing the Phytoremediation of Heavy Metals by Combining Hyperaccumulator and Heavy Metal-Resistant Plant Growth-Promoting Bacteria. Switzerland: N. p., 2022.
Web. doi:10.3389/fpls.2022.912350.
Zhang, Yong, Zhao, Shangjun, Liu, Sijia, Peng, Jing, Zhang, Hanchao, Zhao, Qiming, Zheng, Luqing, Chen, Yahua, Shen, Zhenguo, Xu, Xihui, & Chen, Chen. Enhancing the Phytoremediation of Heavy Metals by Combining Hyperaccumulator and Heavy Metal-Resistant Plant Growth-Promoting Bacteria. Switzerland. https://doi.org/10.3389/fpls.2022.912350
Zhang, Yong, Zhao, Shangjun, Liu, Sijia, Peng, Jing, Zhang, Hanchao, Zhao, Qiming, Zheng, Luqing, Chen, Yahua, Shen, Zhenguo, Xu, Xihui, and Chen, Chen. Thu .
"Enhancing the Phytoremediation of Heavy Metals by Combining Hyperaccumulator and Heavy Metal-Resistant Plant Growth-Promoting Bacteria". Switzerland. https://doi.org/10.3389/fpls.2022.912350.
@article{osti_1871067,
title = {Enhancing the Phytoremediation of Heavy Metals by Combining Hyperaccumulator and Heavy Metal-Resistant Plant Growth-Promoting Bacteria},
author = {Zhang, Yong and Zhao, Shangjun and Liu, Sijia and Peng, Jing and Zhang, Hanchao and Zhao, Qiming and Zheng, Luqing and Chen, Yahua and Shen, Zhenguo and Xu, Xihui and Chen, Chen},
abstractNote = {Heavy metals (HMs) have become a major environmental pollutant threatening ecosystems and human health. Although hyperaccumulators provide a viable alternative for the bioremediation of HMs, the potential of phytoremediation is often limited by the small biomass and slow growth rate of hyperaccumulators and HM toxicity to plants. Here, plant growth-promoting bacteria (PGPB)-assisted phytoremediation was used to enhance the phytoremediation of HM-contaminated soils. A PGPB with HM-tolerant (HMT-PGPB), Bacillus sp. PGP15 was isolated from the rhizosphere of a cadmium (Cd) hyperaccumulator, Solanum nigrum . Pot experiments demonstrated that inoculation with strain PGP15 could significantly increase the growth of S. nigrum . More importantly, strain PGP15 markedly improved Cd accumulation in S. nigrum while alleviating Cd-induced stress in S. nigrum . Specifically, PGP15 inoculation significantly decreased the contents of H 2 O 2 , MDA, and O 2 · − in S. nigrum , while the activities (per gram plant fresh weight) of SOD, APX, and CAT were significantly increased in the PGP15-inoculated plants compared with the control sample. These results suggested that the interactions between strain PGP15 and S. nigrum could overcome the limits of phytoremediation alone and highlighted the promising application potential of the PGPB-hyperaccumulator collaborative pattern in the bioremediation of HM-contaminated soils. Furthermore, the PGP15 genome was sequenced and compared with other strains to explore the mechanisms underlying plant growth promotion by HMT-PGPB. The results showed that core genes that define the fundamental metabolic capabilities of strain PGP15 might not be necessary for plant growth promotion. Meanwhile, PGP15-specific genes, including many transposable elements, played a crucial role in the adaptive evolution of HM resistance. Overall, our results improve the understanding of interactions between HMT-PGPB and plants and facilitate the application of HMT-PGPB in the phytoremediation of HM-contaminated soils.},
doi = {10.3389/fpls.2022.912350},
journal = {Frontiers in Plant Science},
number = ,
volume = 13,
place = {Switzerland},
year = {Thu Jun 02 00:00:00 EDT 2022},
month = {Thu Jun 02 00:00:00 EDT 2022}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.3389/fpls.2022.912350
https://doi.org/10.3389/fpls.2022.912350
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Characterization of Cu(II) and Cd(II) resistance mechanisms in Sphingobium sp. PHE-SPH and Ochrobactrum sp. PHE-OCH and their potential application in the bioremediation of heavy metal-phenanthrene co-contaminated sites
journal, December 2015
- Chen, Chen; Lei, Wenrui; Lu, Min
- Environmental Science and Pollution Research, Vol. 23, Issue 7
Nanopore sequencing and assembly of a human genome with ultra-long reads
journal, January 2018
- Jain, Miten; Koren, Sergey; Miga, Karen H.
- Nature Biotechnology, Vol. 36, Issue 4
Metal(loid)-Contaminated Soils as a Source of Culturable Heterotrophic Aerobic Bacteria for Remediation Applications
journal, April 2017
- Pires, Carlos; Franco, Albina R.; Pereira, Sofia I. A.
- Geomicrobiology Journal, Vol. 34, Issue 9
Beyond horizontal gene transfer: the role of plasmids in bacterial evolution
journal, January 2021
- Rodríguez-Beltrán, Jerónimo; DelaFuente, Javier; León-Sampedro, Ricardo
- Nature Reviews Microbiology, Vol. 19, Issue 6
Proven and potential involvement of vitamins in interactions of plants with plant growth-promoting bacteria—an overview
journal, January 2014
- Palacios, Oskar A.; Bashan, Yoav; de-Bashan, Luz E.
- Biology and Fertility of Soils, Vol. 50, Issue 3
Versatile and open software for comparing large genomes
journal, January 2004
- Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
- Genome Biology, Vol. 5, Issue 2, R12
Inoculating Helianthus annuus (sunflower) grown in zinc and cadmium contaminated soils with plant growth promoting bacteria – Effects on phytoremediation strategies
journal, June 2013
- Marques, Ana P. G. C.; Moreira, Helena; Franco, Albina R.
- Chemosphere, Vol. 92, Issue 1
Exogenous foliar application of fulvic acid alleviate cadmium toxicity in lettuce (Lactuca sativa L.)
journal, January 2019
- Wang, Yanmei; Yang, Ruixi; Zheng, Jiaying
- Ecotoxicology and Environmental Safety, Vol. 167
Long-term effect of epigenetic modification in plant–microbe interactions: modification of DNA methylation induced by plant growth-promoting bacteria mediates promotion process
journal, February 2022
- Chen, Chen; Wang, Miao; Zhu, Jingzhi
- Microbiome, Vol. 10, Issue 1
Adverse Health Effects of Chronic Exposure to Low-Level Cadmium in Foodstuffs and Cigarette Smoke
journal, July 2004
- Satarug, Soisungwan; Moore, Michael R.
- Environmental Health Perspectives, Vol. 112, Issue 10
Genome-Wide Patterns of Adaptation to Temperate Environments Associated with Transposable Elements in Drosophila
journal, April 2010
- González, Josefa; Karasov, Talia L.; Messer, Philipp W.
- PLoS Genetics, Vol. 6, Issue 4
Long-term stabilization of Cd in agricultural soil using mercapto-functionalized nano-silica (MPTS/nano-silica): A three-year field study
journal, July 2020
- Wang, Yangyang; Liu, Yidan; Zhan, Wenhao
- Ecotoxicology and Environmental Safety, Vol. 197
Review of remediation technologies for sediments contaminated by heavy metals
journal, March 2018
- Peng, Weihua; Li, Xiaomin; Xiao, Shengtao
- Journal of Soils and Sediments, Vol. 18, Issue 4
Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects
journal, September 2005
- Compant, S.; Duffy, B.; Nowak, J.
- Applied and Environmental Microbiology, Vol. 71, Issue 9
Horizontal Gene Exchange in Environmental Microbiota
journal, January 2011
- Aminov, Rustam I.
- Frontiers in Microbiology, Vol. 2
Promotion of growth and phytoextraction of cadmium and lead in Solanum nigrum L. mediated by plant-growth-promoting rhizobacteria
journal, December 2020
- He, Xiaoman; Xu, Mingjing; Wei, Qingpeng
- Ecotoxicology and Environmental Safety, Vol. 205
Application of soil amendments to contaminated soils for heavy metal immobilization and improved soil quality—a critical review
journal, February 2018
- Lwin, Chaw Su; Seo, Byoung-Hwan; Kim, Hyun-Uk
- Soil Science and Plant Nutrition, Vol. 64, Issue 2
The impact of transposable elements in adaptive evolution
journal, August 2018
- Schrader, Lukas; Schmitz, Jürgen
- Molecular Ecology, Vol. 28, Issue 6
Rapid determination of free proline for water-stress studies
journal, August 1973
- Bates, L. S.; Waldren, R. P.; Teare, I. D.
- Plant and Soil, Vol. 39, Issue 1
Effects of cadmium and arsenic on growth and metal accumulation of Cd-hyperaccumulator Solanum nigrum L.
journal, March 2008
- Sun, Yuebing; Zhou, Qixing; Diao, Chunyan
- Bioresource Technology, Vol. 99, Issue 5
The important contribution of transposable elements to phenotypic variation and evolution
journal, February 2022
- Catlin, Nathan S.; Josephs, Emily B.
- Current Opinion in Plant Biology, Vol. 65
Mechanisms of, and Barriers to, Horizontal Gene Transfer between Bacteria
journal, September 2005
- Thomas, Christopher M.; Nielsen, Kaare M.
- Nature Reviews Microbiology, Vol. 3, Issue 9
Non-Renal Effects and the Risk Assessment of Environmental Cadmium Exposure
journal, May 2014
- Åkesson, Agneta; Barregard, Lars; Bergdahl, Ingvar A.
- Environmental Health Perspectives, Vol. 122, Issue 5
Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.)
journal, February 2005
- Belimov, A. A.; Hontzeas, N.; Safronova, V. I.
- Soil Biology and Biochemistry, Vol. 37, Issue 2
The impact of transposable elements in environmental adaptation
journal, January 2013
- Casacuberta, Elena; González, Josefa
- Molecular Ecology, Vol. 22, Issue 6
Heavy metals in food crops, soil, and water in the Lihe River Watershed of the Taihu Region and their potential health risks when ingested
journal, February 2018
- Chen, Lian; Zhou, Shenglu; Shi, Yaxing
- Science of The Total Environment, Vol. 615
Influence of root exudates on the extracellular proteome of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42
journal, January 2015
- Kierul, Kinga; Voigt, Birgit; Albrecht, Dirk
- Microbiology, Vol. 161, Issue 1
Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads
journal, June 2017
- Wick, Ryan R.; Judd, Louise M.; Gorrie, Claire L.
- PLOS Computational Biology, Vol. 13, Issue 6
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents
journal, October 1983
- Lichtenthaler, Hartmut K.; Wellburn, Alan R.
- Biochemical Society Transactions, Vol. 11, Issue 5
A simple method for the preparation of horseradish peroxidase
journal, June 1954
- Kenten, R. H.; Mann, P. J. G.
- Biochemical Journal, Vol. 57, Issue 2
Hydrogen-rich water pretreatment alters photosynthetic gas exchange, chlorophyll fluorescence, and antioxidant activities in heat-stressed cucumber leaves
journal, June 2017
- Chen, Qiuhong; Zhao, Xueqiang; Lei, Dekun
- Plant Growth Regulation, Vol. 83, Issue 1
Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization
journal, May 2010
- Compant, Stéphane; Clément, Christophe; Sessitsch, Angela
- Soil Biology and Biochemistry, Vol. 42, Issue 5
Superoxide Dismutases: I. Occurrence in Higher Plants
journal, February 1977
- Giannopolitis, Constantine N.; Ries, Stanley K.
- Plant Physiology, Vol. 59, Issue 2
Universal chemical assay for the detection and determination of siderophores
journal, January 1987
- Schwyn, Bernhard; Neilands, J. B.
- Analytical Biochemistry, Vol. 160, Issue 1, p. 47-56
A large transposable element mediates metal resistance in the fungus Paecilomyces variotii
journal, March 2022
- Urquhart, Andrew S.; Chong, Nicholas F.; Yang, Yongqing
- Current Biology, Vol. 32, Issue 5
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003
- Li, L.
- Genome Research, Vol. 13, Issue 9
Phytoremediation of heavy metals by Alternanthera bettzickiana: Growth and physiological response
journal, April 2016
- Tauqeer, Hafiz Muhammad; Ali, Shafaqat; Rizwan, Muhammad
- Ecotoxicology and Environmental Safety, Vol. 126
From the Lab to the Farm: An Industrial Perspective of Plant Beneficial Microorganisms
journal, August 2016
- Parnell, J. Jacob; Berka, Randy; Young, Hugh A.
- Frontiers in Plant Science, Vol. 7
Exploring plant‐microbe interactions of the rhizobacteria Bacillus subtilis and Bacillus mycoides by use of the CRISPR‐Cas9 system
journal, August 2018
- Yi, Yanglei; Li, Zhibo; Song, Chunxu
- Environmental Microbiology, Vol. 20, Issue 12
Editorial: Horizontal Gene Transfer Mediated Bacterial Antibiotic Resistance
journal, August 2019
- Sun, Dongchang; Jeannot, Katy; Xiao, Yonghong
- Frontiers in Microbiology, Vol. 10
Soil contamination by heavy metals: Measurements from a closed unlined landfill
journal, December 2008
- Kasassi, A.; Rakimbei, P.; Karagiannidis, A.
- Bioresource Technology, Vol. 99, Issue 18
EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences
journal, October 2007
- Kim, Byung Kwon; Lim, Young-Woon; Kim, Myungjin
- International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 10
JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison
journal, November 2015
- Richter, Michael; Rosselló-Móra, Ramon; Oliver Glöckner, Frank
- Bioinformatics, Vol. 32, Issue 6
Prokka: rapid prokaryotic genome annotation
journal, March 2014
- Seemann, T.
- Bioinformatics, Vol. 30, Issue 14
Multiple Sequence Alignment Using ClustalW and ClustalX
journal, August 2002
- Thompson, Julie D.; Gibson, Toby. J.; Higgins, Des G.
- Current Protocols in Bioinformatics, Vol. 00, Issue 1
Oxidative stress and some antioxidant systems in acid rain-treated bean plants
journal, February 2000
- Velikova, V.; Yordanov, I.; Edreva, A.
- Plant Science, Vol. 151, Issue 1
Interaction of Cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake
journal, January 2014
- Chen, Liang; Luo, Shenglian; Li, Xiaojie
- Soil Biology and Biochemistry, Vol. 68
MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity
journal, January 2012
- Wang, Y.; Tang, H.; DeBarry, J. D.
- Nucleic Acids Research, Vol. 40, Issue 7
Colorimetric Estimation of Indoleacetic acid
journal, January 1951
- Gordon, Solon A.; Weber, Robert P.
- Plant Physiology, Vol. 26, Issue 1
Comparative genomics and physiological investigation supported safety, cold adaptation, efficient hydrolytic and plant growth-promoting potential of psychrotrophic Glutamicibacter arilaitensis LJH19, isolated from night-soil compost
journal, April 2021
- Borker, Shruti Sinai; Thakur, Aman; Kumar, Sanjeet
- BMC Genomics, Vol. 22, Issue 1
Current status of cadmium as an environmental health problem
journal, August 2009
- Järup, Lars; Åkesson, Agneta
- Toxicology and Applied Pharmacology, Vol. 238, Issue 3
SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data
journal, December 2017
- Chen, Yuxin; Chen, Yongsheng; Shi, Chunmei
- GigaScience, Vol. 7, Issue 1
Alleviation of Heavy Metal Stress in Plants and Remediation of Soil by Rhizosphere Microorganisms
journal, September 2017
- Mishra, Jitendra; Singh, Rachna; Arora, Naveen K.
- Frontiers in Microbiology, Vol. 8
Plants growing in abandoned mines of Portugal are useful for biogeochemical exploration of arsenic, antimony, tungsten and mine reclamation
journal, April 2005
- Pratas, J.; Prasad, M. N. V.; Freitas, H.
- Journal of Geochemical Exploration, Vol. 85, Issue 3
Comparative bacterial genomics: defining the minimal core genome
journal, September 2012
- Huang, C. H.; Hsiang, T.; Trevors, J. T.
- Antonie van Leeuwenhoek, Vol. 103, Issue 2
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016
- Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
- Molecular Biology and Evolution, Vol. 33, Issue 7
Heavy metal contamination in soils and vegetables near an e-waste processing site, south China
journal, February 2011
- Luo, Chunling; Liu, Chuanping; Wang, Yan
- Journal of Hazardous Materials, Vol. 186, Issue 1
Horizontal Gene Transfer in Prokaryotes: Quantification and Classification
journal, October 2001
- Koonin, Eugene V.; Makarova, Kira S.; Aravind, L.
- Annual Review of Microbiology, Vol. 55, Issue 1
Insertion sequence elements in Cupriavidus metallidurans CH34: Distribution and role in adaptation
journal, May 2011
- Mijnendonckx, Kristel; Provoost, Ann; Monsieurs, Pieter
- Plasmid, Vol. 65, Issue 3
Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila
journal, February 2019
- Rech, Gabriel E.; Bogaerts-Márquez, María; Barrón, Maite G.
- PLOS Genetics, Vol. 15, Issue 2
Ecology and Evolution of Plant Microbiomes
journal, September 2019
- Cordovez, Viviane; Dini-Andreote, Francisco; Carrión, Víctor J.
- Annual Review of Microbiology, Vol. 73, Issue 1
Bacterial insertion sequences: their genomic impact and diversity
journal, September 2014
- Siguier, Patricia; Gourbeyre, Edith; Chandler, Mick
- FEMS Microbiology Reviews, Vol. 38, Issue 5
Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils
journal, March 2011
- Ma, Y.; Prasad, M. N. V.; Rajkumar, M.
- Biotechnology Advances, Vol. 29, Issue 2
An efficient algorithm for large-scale detection of protein families
journal, April 2002
- Enright, A. J.
- Nucleic Acids Research, Vol. 30, Issue 7
Complete Genome Sequence of Cd(II)-Resistant Arthrobacter sp. PGP41, a Plant Growth-Promoting Bacterium with Potential in Microbe-Assisted Phytoremediation
journal, May 2018
- Xu, Xihui; Xu, Meng; Zhao, Qiming
- Current Microbiology, Vol. 75, Issue 9
Heavy metal poisoning: the effects of cadmium on the kidney
journal, March 2010
- Johri, Nikhil; Jacquillet, Grégory; Unwin, Robert
- BioMetals, Vol. 23, Issue 5
Microbial technologies for heavy metal remediation: effect of process conditions and current practices
journal, February 2021
- Verma, Shulbhi; Bhatt, Pankaj; Verma, Amit
- Clean Technologies and Environmental Policy
Isolation of plant-growth-promoting and metal-resistant cultivable bacteria from Arthrocnemum macrostachyum in the Odiel marshes with potential use in phytoremediation
journal, September 2016
- Navarro-Torre, S.; Mateos-Naranjo, E.; Caviedes, M. A.
- Marine Pollution Bulletin, Vol. 110, Issue 1
Organic acids in the rhizosphere – a critical review
journal, August 1998
- Jones, David L.
- Plant and Soil, Vol. 205, Issue 1, p. 25-44
Effect of Abscisic Acid on Active Oxygen Species, Antioxidative Defence System and Oxidative Damage in Leaves of Maize Seedlings
journal, November 2001
- Jiang, Mingyi; Zhang, Jianhua
- Plant and Cell Physiology, Vol. 42, Issue 11
Removal of heavy metal ions from wastewaters: A review
journal, March 2011
- Fu, Fenglian; Wang, Qi
- Journal of Environmental Management, Vol. 92, Issue 3
Structure and Functions of the Bacterial Microbiota of Plants
journal, April 2013
- Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn
- Annual Review of Plant Biology, Vol. 64, Issue 1
Plant Growth-Promoting Bacteria: Mechanisms and Applications
journal, January 2012
- Glick, Bernard R.
- Scientifica, Vol. 2012
Measurement of Ozone Injury by Determination of Leaf Chlorophyll Concentration
journal, October 1977
- Knudson, Linda L.; Tibbitts, Theodore W.; Edwards, Gerald E.
- Plant Physiology, Vol. 60, Issue 4