Recent Advances in Microbial-Assisted Remediation of Cadmium-Contaminated Soil
Abstract
:1. Introduction
2. Review Methodology
3. Sources of Cadmium
4. Cadmium Toxicity and Plants
4.1. Seed Germination and Seedling Growth
4.2. Cadmium-Induced Changes in Growth and Development
4.3. Impact on Amino Acids, Proteins and Organic Osmolytes
4.4. Plant Water Relations
4.5. Impact on Photosynthesis
5. The Role of Microbes in the Bioremediation of Cd-Contaminated Soils
5.1. Remediation of Cd by Bacteria
5.2. Remediation of Cd by Fungi
5.3. Remediation of Cd by Algae
6. Mechanisms Involved in Bioremediation by Microbes
6.1. Direct Mechanisms
6.1.1. Nitrogen Fixation
6.1.2. Phosphate Solubilization
6.1.3. Phytohormone Production
6.1.4. Antagonistic Role of PGPR
6.1.5. Siderophore Secretion
6.1.6. Volatile Organic Compounds
6.2. Indirect Mechanisms
6.2.1. Production of Antibiotics
6.2.2. Production of Exopolysaccharides
6.2.3. Hydrogen Cyanide
6.2.4. Lipo-Chito-Oligosaccharides
7. Factors Affecting PGPR Bioremediation
8. Recent Advancements (Genetic and Metabolic Engineering), (Membrane and Enzyme Technology), (Metagenomics Approaches) and (Nanoparticle Technology)
8.1. Membrane and Enzyme Technology
8.2. Genetic and Metabolic Engineering
8.3. Metagenomics Approaches
8.4. Nanoparticle Technology
9. Challenges and Future Prospects
10. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Plant Species | Level of Cd | Changes/Damages | References |
---|---|---|---|
Seed germination and seedling growth | |||
Pisum sativum L. | 20–500 µM | Inhibition of proteolytic enzymes and restriction of starch metabolism, leading to the failure of protein mobilization in seeds. | [73] |
Ocimum basilicum L. | 20 mg kg−1 | Alterations in the embryo and reductions in the oil contents of seeds. | [74] |
Brassica oleracea L. | 5 mg L−1 | Decreased seed germination with an increase in MDA contents, electrolyte leakage and H2O2 contents. | [75] |
Sassafras tzumu Hemsl. | 100 mg kg−1 | Restricted seedling growth and germination, and impairment of photosynthesis at higher doses. | [63] |
Brassica juncea L. | 15 mg kg−1 | Disintegration occured in roots and shoots, and levels of ROS increased in plant shoots. | [76] |
Oryza sativa L. | 50 μM | Lower seed germination rate due to the hyperaccumulation of Cd. | [53] |
Zea mays L. | 100 mg kg−1 | Reduced seedling growth and activity of cellular antioxidants. | [77] |
Growth and development | |||
Cicer arietinum L. | 50 μM | Reduction in growth and appearance of symptoms of necrosis and chlorosis in leaves. | [78] |
Ipomoea aquatica Forsk | Reduced growth and development of root and shoots. | [79] | |
Lens culinaris | 50 µg g−1 | Increased electrolyte leakage and ROS production, resulting in lower plant growth. | [80] |
Medicago sativa L. | 10 mg kg−1 | Higher concentrations damaged proteins, changed cell wall infrastructure and metabolism, and limited growth. | [81] |
Osmolytes and photosynthesis | |||
Cajanus cajan L. | 10 mg kg−1 | Lower organic osmolytes ultimately caused a disturbance in osmotic adjustments. | [82] |
Vigna angularis | 64 mg L−1 | Cellular antioxidants decreased at higher concentrations, resulting in the lower production of low-molecular-weight osmolytes. | [83] |
Zea mays L. | 150 μM | Reduction in photosynthetic pigments and gas exchange traits. | [58] |
Coriandrum sativum L. | 20 µM L−1 | Inhibited gas exchange traits and biochemical processes. | [45] |
Capsicum annuum L. | 500 ppm | Induction of stomatal closure, resulting in decreased photosynthetic pigments, a smaller stomatal size and reduced transpiration. | [84] |
Mentha arvensis | 150 mg Kg−1 | Reductions in mineral assimilation, photosynthetic attributes and photosynthetic pigments occurred. | [85] |
Experiment | Contamination Level | Microorganisms | Plant | Results | References |
---|---|---|---|---|---|
Pot | 10 mg kg−1 | Pseudomonas fluorescens | Hordeum vulgare | Phyto-stabilization of Cd due to PGPR activity, increased uptake of essential plant nutrients and enhanced plant growth attributes. | [90] |
Greenhouse pot | 10.7 mg kg−1 Cd | Bacillus spp. | Solanum nigrum | Increased plant growth attributes under Cd stress, enhanced absorption of P and Fe as well as increased Cd contents in aerial plant parts. | [91] |
Incubation study | 200 μg/mL | Klebsiella michiganensis | Oryza sativa | Cd bioaccumulation by tolerant bacteria with a concurrent decline in its uptake by plants. | [92] |
Pot | 50 mg kg−1 | Cupriavidus necator, Sphingomonas and Curtobacterium spp. | Brassica napus | Increased plant biomass and growth traits under Cd contamination in inoculated treatments along with enhanced Cd uptake by aerial plant parts. | [93] |
Pot | 0, 50, and 100 mg L−1 | Rhizobium pusense | Glycine max | Decreased soybean root Cd contents by 45.9 and 35.3%, respectively, at contamination levels of 50 and 100 mg L−1. | [94] |
Pot | (0, 25, 50, 75, 100, 150 and 200 mg kg−1) | Enterobacter cloacae, Klebsiella pneumonia and Klebsiella spp. | Pennisetum giganteum | Combined application of rhizobacteria increased the bioaccumulation factor of Cd for plants. | [95] |
Pot | 0, 5, 10, 15 and 20 mg kg−1 | Serratia marcescens | Chrysopogon zizanioides | Increased phytoaccumulation of Cd, soil biological health, as well as antioxidative potential of plants under bacterial inoculation. Maximum Cd phytoextraction in roots (289.47 mg kg−1), leaves (59.38 mg kg−1) and stem (88.33 mg kg−1) with a concomitant increase in plant biomass (9.68–45.99%). | [96] |
Field | 2.2 mg kg−1 | Rhizobium leguminosarum, Bacillus simplex, Luteibacter sp. + Variovorax sp., Pseudomonas fluorescens | Lathyrus sativus | Increased growth attributes as well as nodule number, and plant nutrient uptake, and phytoaccumulation along with reduced rhizosphere concentration of Cd (61%). | [97] |
Pot | 50 and 100 mg kg−1 | Fungi “Funneliformis mosseae” and bacteria Enterobacter sp. and Enterobacter ludwigii | Lycopersicon esculentum | Increased dry weights of shoots (119–154%) and roots (91–173%) under combined inoculation. Furthermore, decreased Cd concentrations in shoots as well as translocation factors under inoculated treatments were observed. | [98] |
Pot | 0, 0.25, 0.5, 0.75 and 1 M CdSO4 | Serratia marcescens | Oryza sativa | Increased Cd removal from soil (66 mg kg−1 after 20 days). | [99] |
Incubation study | 0, 0.25, and 0.5 mM Cd | Stenotrophomonas maltophilia | Capsicum annuum | Under Cd stress, increased root lengths (1.46 times) in the inoculated treatment compared to the control. | [100] |
Pot | 15 mg kg−1 | Variovorax paradoxus, Rhizobium leguminosarum and fungus Glomus spp. | Pisum sativum and Brassica juncea | More prominent positive effect of consortium inoculation on Pisum sativum rather than Brassica juncea, in terms of growth, nutrient uptake and increased seed Cd concentration. | [101] |
Greenhouse pot | 2.12 mg kg−1 | Bacillus megaterium, Glomus mosseae, and Piriformospora indica | Solanum nigrum | Cd accumulation (104%) observed under the combined application of Bacillus megaterium and Glomus mosseae in addition to increased soil biological health under contaminated conditions. | [102] |
Pot | 100 mg kg−1 | Bacillus sp. | Oryza sativa | Reduced bioavailable Cd concentration (39.3%), increased phytoextraction efficiency of rice for Cd (48.2%) and increased rice growth and yield traits under inoculation compared to the control. | [103] |
Greenhouse | 0.064 mg L−1 | Klebsiella huaxiensis and Pantoea cypripedii | Pennisetum purpurenum | Enhanced Cd phytoaccumulation in all variants of the tested plant (28.43–38.07 mg kg−1). | [104] |
Pot | 30 μmol L−1 | Enterobacter cloacae | Solanum nigrum | Increased soil Cd phytoextraction by plants along with increased plant growth under Cd stress. | [105] |
Pot | 0, 0.25, and 0.50 mg kg−1 | Bacillus spp. | Oryza sativa | Increased Cd immobilization in soil by its surface adsorption concomitant with increased plant growth. | [106] |
Incubation | 0.4 mM CdCl2 | Pseudomonas aeruginosa and Burkholderia gladioli | Solanum lycopersicum | Alleviation of Cd toxicity in plants was evident by an increase in phenolic compounds, osmolytes and low-molecular-weight organic acids. | [107] |
Growth room trial | 0–400 μg/mL | Enterobacter cloacae | Oryza sativa | Increased Cd removal efficiency (72.11%) against a contamination level of 400 μg/mL | [108] |
Pot | 2 g | Curtobacterium oceanosedimentum | Capsicum frutescens | Increased root (58%) and shoot (60%) lengths, enhanced accumulation of Cd in roots compared to shoots under bacterial inoculation. | [109] |
Pot | 1.68 mg kg−1 | Buttiauxella, Pedobacter, Aeromonas eucrenophila, and Ralstonia pickettii | Sedum plumbizincicola | Inoculation led to reduced reducible and residual Cd and increased Cd availability coefficients by 1.15–6.41 units. Cd contents in shoots (29.63–46.01%) and roots (11.42–84.47%), bioconcentration factor (2.13–2.72) and Cd removal rate (48.25%) compared to the control treatment | [110] |
Species name | Initial Cd Concentration | Experimental Medium | Cd Remediation Efficiency | References |
---|---|---|---|---|
Bacterial species | ||||
Pseudomonas fluorescens and Bacillus subtilis | 150 mg L−1 | Soil | 16.7 | [162] |
Pseudomonas sp. DDT-1 | 0.9 mg kg−1 | Soil | 40.3 | [163] |
Kocuria rhizophila | 150 mg L−1 | Aqueous | 9.07 mg g−1 | [164] |
Klebsiella michiganensis | 1000 µg ml−1 | Soil | 97% | [165] |
Enterobacter sp | 3500 µg ml−1 | Soil | 95% | [166] |
Rhodobacter sphaeroides | 65.33 mg kg−1 | Soil | 30.7 | [167] |
Bacillus aryabhattai and Bacillus amyloliquefaciens | 250 mg L−1 | Soil | 96% | [168] |
Aspergillus sydowii | 50 mg kg−1 | Soil | 10.44% | [169] |
Cupriavidus sp. | 13.82 mg kg−1 | Soil | 58.2% | [170] |
Paenibacillus sp. and Bacillus sp. | 20 mg L−1 | Soil | 128.50% | [171] |
Bacillus sp. TZ5 | 150 mg L−1 | Soil | 48.49% | [172] |
Acidithiobacillus caldus DX, Acidithiobacillus thiooxidans DX, Acidithiobacillus thiooxidans ZJ, Acidithiobacillus thiooxidans AO1, Ferroplasma acidiphilum DX, Acidithiobacillus caldus S1 and Leptospirillum ferriphilum DX | 9.09 mg kg−1 | Soil | 32.09% | [173] |
Cupriavidus sp. (KU168590), Ensifer sp. (KU168586), Burkholderia sp. (KU168588), and Paenibacillus sp. (KU168587) | 0.21 mg kg−1 | Soil | 33.0% | [174] |
Enterobacter cloacae, Pseudomonas aeruginosa, and Klebsiella Edwardsii | 50 mg L−1 | Soil | 58.80% | [175] |
Bacillus subtilis | 147.75 mg kg−1 | Soil | 35.17% | [176] |
Burkholderia sp. and Bacillus sp. | 5 mM | Soil | 84.17% | [177] |
Bacillus sp. | 49 mg kg−1 | Soil | 43.53% | [178] |
Bacillus subtilis | 147.75 mg kg−1 | Soil | 18.56% | [179] |
Firmicutes sp. and Proteobacteria sp. | 14.9 mg kg−1 | Soil | 40.0 | [180] |
Enterobacter hormaechei SFC3 | 100 µg ml−1 | Soil | 90.21% | [181] |
Streptomyces pactum Act12 and Streptomyces Roche D74 | 1.62 mg kg−1 | Soil | 56.39% | [182] |
Bacillus velezensis | - | Soil | 1.65 μg g−1 | [183] |
Fungi | ||||
Aspergillus niger, Aspergillus fumigatus, and Penicillium rubens | 0.6 mg L−1 | Soil | 79% | [184] |
Simplicillium chinense | 400 mg L−1 | Soil | 88% | [185] |
Aspergillus flflavus, Aspergillus gracilis, Aspergillus penicillioides, Aspergillus restrictus, and Sterigmatomyces halophilus | 1000 mg L−1 | Soil | 95% | [186] |
Phanerochaete chrysosporium | 25 mg L−1 | Soil | 96% | [187] |
Agaricus bisporus, Pleurotus platypus, and Calocybe indica | - | - | 98.97 | [188] |
Lactarius piperatus and Agaricus bisporus | 265 mg L−1 | Aqueous | 95% | [189] |
Rhizophagus intraradices | - | Soil | 38% | [190] |
Trichoderma harzianum | 147.75 mg kg−1 | Soil | 47.69% | [176] |
Algae/cyanobacteria | ||||
Asparagopsis armata | 150 mg L−1 | Aqueous | 10.6% | [191] |
Chaetoceros calcitrans and Tetracelmis chuii | - | Aqueous | - | [192] |
Ulva lactuca | 80 mg L−1 | Aqueous | 41.0% | [193] |
Chara aculeolate | - | Aqueous | 23 mg g−1 | [194] |
Chlorella pyrenoidosa | 1.5 mg L−1 | Aqueous | 45.45 | [195] |
Scenedesmus acutus | 1.5 mg L−1 | Aqueous | 57.14 | [195] |
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Zulfiqar, U.; Haider, F.U.; Maqsood, M.F.; Mohy-Ud-Din, W.; Shabaan, M.; Ahmad, M.; Kaleem, M.; Ishfaq, M.; Aslam, Z.; Shahzad, B. Recent Advances in Microbial-Assisted Remediation of Cadmium-Contaminated Soil. Plants 2023, 12, 3147. https://doi.org/10.3390/plants12173147
Zulfiqar U, Haider FU, Maqsood MF, Mohy-Ud-Din W, Shabaan M, Ahmad M, Kaleem M, Ishfaq M, Aslam Z, Shahzad B. Recent Advances in Microbial-Assisted Remediation of Cadmium-Contaminated Soil. Plants. 2023; 12(17):3147. https://doi.org/10.3390/plants12173147
Chicago/Turabian StyleZulfiqar, Usman, Fasih Ullah Haider, Muhammad Faisal Maqsood, Waqas Mohy-Ud-Din, Muhammad Shabaan, Muhammad Ahmad, Muhammad Kaleem, Muhammad Ishfaq, Zoya Aslam, and Babar Shahzad. 2023. "Recent Advances in Microbial-Assisted Remediation of Cadmium-Contaminated Soil" Plants 12, no. 17: 3147. https://doi.org/10.3390/plants12173147