ORIGINAL RESEARCH
Utilization and Characterization of Microbes
for Heavy Metal Remediation
More details
Hide details
1
College of Engineering, Agriculture Aviation Innovation Lab, South China Agriculture University, Guangzhou, China
2
Ministry of Agriculture, Extension Wing, Govt of Khyber Pakhtunkhwa, Pakistan
3
Department of Agronomy, The University of Agriculture, Peshawar, Pakistan
4
Department of Soil and Environmental Sciences, The University of Agriculture, Peshawar, Pakistan
5
Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
6
Department of Life Sciences, Yeungnam University, Gyeongsan 38541, Republic of Korea
Submission date: 2024-02-20
Final revision date: 2024-03-21
Acceptance date: 2024-04-08
Online publication date: 2024-08-05
Publication date: 2025-01-09
Corresponding author
Wajid Zaman
Department of Life Sciences, Yeungnam University, Gyeongsan 38541, South Korea
Pol. J. Environ. Stud. 2025;34(2):1179-1190
KEYWORDS
TOPICS
ABSTRACT
Heavy metals in forest soils have substantial ecological implications, affecting the soil and the
surrounding ecosystem. These naturally occurring elements, with high atomic weights, become toxic at
elevated concentrations. Notable heavy metals in forest soils include lead, cadmium, mercury, and arsenic.
The profound toxicity of heavy metal pollution poses a significant risk to modern agriculture, with the
potential for accumulation in crops and soils, threatening food security. A crucial aspect of addressing this
challenge involves promptly restoring disrupted agricultural land. This study contributes to agricultural
soil restoration by employing a combination of microorganisms, which have proven effective in alleviating
heavy metal pollution. When paired with Sunflower (Helianthus annus), the combination ensures soil
restoration and enhances food security. The study investigated microorganisms from contaminated soil,
revealing Gram-negative bacilli and cocci arrangements. The colony characteristics, including hues and
diameters, were assessed, with notable findings in samples 1, 2, and 5. The microbial ability to remove
heavy metals (Pb, As, Hg, Ni, and Cd) was quantified, highlighting the diverse capacities among isolates.
Selected isolates (1, 3, 6, 7, and 10) exhibited 25% higher biomass accumulation than the control, extracting
at least 40 mg/L of each metal. Bacterial identification using a Vitek 2 Compact analyzer revealed
Pantoea sp., Achromobacter denitrificans, Klebsiella oxytoca, Rhizobium radiobacter, and Pseudomonas
fluorescens. Biocompatibility testing led to the formation of consortia for soil remediation, with Coalition D
(Achromobacter denitrificans, Klebsiella oxytoca, and Rhizobium radiobacter in a 1:1:2 ratio) confirming
the effective removal of Ni and Pb. Various consortia showed differing performances in removing
composite contaminants, with Coalition D being promising, indicating a potential for phytoremediation.
Optimal cultivation conditions were identified, with Coalition D excelling at metal removal and biomass
accumulation. The temperature, pH, and soil conditions were crucial for Coalition D efficiency, and
combining them with phytoremediation techniques showed promise. Laboratory experiments with
sunflower seedlings confirmed the efficacy of Coalition D in enhancing soil phytoremediation, improving
plant survival, and removing mixed heavy metals.
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
REFERENCES (61)
1.
YAASHIKAA P.R., KUMAR P.S. Bioremediation of hazardous pollutants from agricultural soils: A sustainable approach for waste management towards urban sustainability. *Environmental Pollution*, 312, 120031, 2022. <
https://doi.org/10.1016/j.envp...> PMid:36041569.
2.
RILLIG M.C., RYO M., LEHMANN A., AGUILAR-TRIGUEROS C.A., BUCHERT S., WULF A., IWASAKI A., ROY J., YANG G. The role of multiple global change factors in driving soil functions and microbial biodiversity. *Science*, 366 (6467), 886, 2019. <
https://doi.org/10.1126/scienc...> PMid:31727838 PMCid:PMC6941939.
3.
DEBONNE N., VAN VLIET J., METTERNICHT G., VERBURG P. Agency shifts in agricultural land governance and their implications for land degradation neutrality. *Global Environmental Change*, 66, 102221, 2021. <
https://doi.org/10.1016/j.gloe...>.
4.
NIZAMUTDINOV T., SULEYMANOV A., MORGUN E., DINKELAKER N., ABAKUMOV E. Ecotoxicological Analysis of Fallow Soils at the Yamal Experimental Agricultural Station. *Food Processing: Techniques and Technology*, 52 (2), 350, 2022. <
https://doi.org/10.21603/2074-...>.
5.
BEKKERING C.S., PENG C., TIAN L. Advancing Global Learning Through a Collaborative Online International Learning (COIL) Module on the United Nations Sustainable Development Goals (UN SDGs). *CourseSource*, 10, 2023. <
https://doi.org/10.24918/cs.20...>.
6.
UCHIMIYA M., BANNON D., NAKANISHI H., MCBRIDE M.B., WILLIAMS M.A., YOSHIHARA T. Chemical Speciation, Plant Uptake, and Toxicity of Heavy Metals in Agricultural Soils. *Journal of Agricultural and Food Chemistry*, 68 (46), 12856, 2020. <
https://doi.org/10.1021/acs.ja...> PMid:32155055.
7.
JIANG H.-H., CAI L.-M., WEN H.-H., HU G.-C., CHEN L.-G., LUO J. An integrated approach to quantifying ecological and human health risks from different sources of soil heavy metals. *Science of The Total Environment*, 701, 134466, 2020. <
https://doi.org/10.1016/j.scit...> PMid:31704412 PMCid:PMC9983881.
8.
GUAN Q., LIU Z., SHAO W., TTian J., LUO H., NI F., SHAN Y. Probabilistic risk assessment of heavy metals in urban farmland soils of a typical oasis city in northwest China. *Science of The Total Environment*, 833, 155096, 2022. <
https://doi.org/10.1016/j.scit...> PMid:35398134.
9.
YAN A., WANG Y., TAN S.N., MOHD YUSOF M.L., GHOSH S., CHEN Z. Phytoremediation: A Promising Approach for Revegetation of Heavy Metal-Polluted Land. *Frontiers in Plant Science*, 11, 359, 2020. <
https://doi.org/10.3389/fpls.2...> PMid:32425957 PMCid:PMC7203417.
10.
KAPUSTA-DUCH J., LESZCZYŃSKA T., FLORKIEWICZ A., FILIPIAK-FLORKIEWICZ A. Comparison of Lead and Cadmium Contents in Cruciferous Vegetables Grown under Diversified Ecological Conditions: Cracow Region of Poland. *Ecology of Food and Nutrition*, 50 (2), 137, 2011. <
https://doi.org/10.1080/036702...> PMid:21888593.
11.
GONG Y., ZHAO D., WANG Q. An overview of field-scale studies on remediation of soil contaminated with heavy metals and metalloids: Technical progress over the last decade. *Water Research*, 147, 440, 2018. <
https://doi.org/10.1016/j.watr...> PMid:30343201.
12.
SUN R., YANG J., XIA P., WU S., LIN T., YI Y. Contamination features and ecological risks of heavy metals in the farmland along shoreline of Caohai plateau wetland, China. *Chemosphere*, 254, 126828, 2020. <
https://doi.org/10.1016/j.chem...> PMid:32334265.
13.
LI C., ZHOU K., QIN W., TIAN C., QI M., YAN X., HAN W. A Review on Heavy Metals Contamination in Soil: Effects, Sources, and Remediation Techniques. *Soil and Sediment Contamination*, 28 (4), 380, 2019. <
https://doi.org/10.1080/153203...>.
14.
DROZDOVA M., POZDNYAKOVA A., OSINTSEVA M., BUROVA N., MININA V. The microorganism-plant system for remediation of soil exposed to coal mining. *Foods and Raw Materials*, 9 (2), 406, 2021. <
https://doi.org/10.21603/2308-...>.
15.
TWARÓG A., MAMAK M., SECHMAN H., RUSINIAK P., KASPRZAK E., STANEK K. Impact of the landfill of ashes from the smelter on the soil environment: case study from the South Poland, Europe. *Environmental Geochemistry and Health*, 42 (5), 1453, 2020. <
https://doi.org/10.1007/s10653...> PMid:31595481 PMCid:PMC7261277.
16.
ZHOU Y., JIANG D., DING D., WU Y., WEI J., KONG L., LONG T., FAN T., DENG S. Ecological-health risks assessment and source apportionment of heavy metals in agricultural soils around a super-sized lead-zinc smelter with a long production history, in China. *Environmental Pollution*, 307, 119487, 2022. <
https://doi.org/10.1016/j.envp...> PMid:35597487.
17.
GUAN D.-X., SUN F.-S., YU G.-H., POLIZZOTTO M.L., LIU Y.-G. Total and available metal concentrations in soils from six long-term fertilization sites across China. *Environmental Science and Pollution Research*, 25 (31), 31666, 2018. <
https://doi.org/10.1007/s11356...> PMid:30209764.
18.
DEFARGE N., SPIROUX DE VENDÔMOIS J., SÉRALINI G.E. Toxicity of formulants and heavy metals in glyphosate-based herbicides and other pesticides. *Toxicology Reports*, 5, 156, 2017. <
https://doi.org/10.1016/j.toxr...> PMid:29321978 PMCid:PMC5756058.
19.
BAI L.Y., ZENG X.B., SU S.M., DUAN R., WANG Y.N., GAO X. Heavy metal accumulation and source analysis in greenhouse soils of Wuwei District, Gansu Province, China. *Environmental Science and Pollution Research*, 22 (7), 5359, 2014. <
https://doi.org/10.1007/s11356...> PMid:25430008.
20.
KHALID S., SHAHID M., NIAZI N.K., MURTAZA B., BIBI I., DUMAT C. A comparison of technologies for remediation of heavy metal contaminated soils. *Journal of Geochemical Exploration*, 182, 247, 2017. <
https://doi.org/10.1016/j.gexp...>.
21.
RAHMAN Z., SINGH V.P. Bioremediation of toxic heavy metals (THMs) contaminated sites: concepts, applications and challenges. *Environmental Science and Pollution Research*, 27 (22), 27563, 2020. <
https://doi.org/10.1007/s11356...> PMid:32418096.
22.
AYANGBENRO A.S., BABALOLA O.O. A New Strategy for Heavy Metal Polluted Environments: A Review of Microbial Biosorbents. *International Journal of Environmental Research and Public Health*, 14 (1), 94, 2017. <
https://doi.org/10.3390/ijerph...> PMid:28106848 PMCid:PMC5295344.
23.
FAJARDO C., COSTA G., NANDE M., BOTÍAS P., GARCÍA-CANTALEJO J., MARTÍN M. Pb, Cd, and Zn soil contamination: Monitoring functional and structural impacts on the microbiome. *Applied Soil Ecology*, 135, 56, 2019. <
https://doi.org/10.1016/j.apso...>.
24.
HAQUE S., SRIVASTAVA N., PAL D.B., ALKHANANI M.F., ALMALKI A.H., AREESHI M.Y., NAIDU R., GUPTA V.K. Functional microbiome strategies for the bioremediation of petroleum-hydrocarbon and heavy metal contaminated soils: A review. *Science of The Total Environment*, 833, 155222, 2022. <
https://doi.org/10.1016/j.scit...> PMid:35421499.
25.
QIU S., YANG H., ZHANG S., HUANG S., ZHAO S., XU X., BANWART S.A. Carbon storage in an arable soil combining field measurements, aggregate turnover modeling and climate scenarios. *CATENA*, 220, 106708, 2023. <
https://doi.org/10.1016/j.cate...>.
26.
ZHU G., YONG L., ZHAO X., LIU Y., ZHANG Z., XU Y., WANG L. Evaporation, infiltration and storage of soil water in different vegetation zones in the Qilian Mountains: a stable isotope perspective. *Hydrology and Earth System Sciences*, 26 (14), 3771, 2022. <
https://doi.org/10.5194/hess-2...>.
27.
ZHAO Y., DONG Y., CHEN X., WANG Z., CUI Z., NI S. Using sulfide as nitrite oxidizing bacteria inhibitor for the successful coupling of partial nitrification-anammox and sulfur autotrophic denitrification in one reactor. *Chemical Engineering Journal*, 475, 146286, 2023. <
https://doi.org/10.1016/j.cej....>.
28.
JIA Q., SUN J., GAN Q., SHI N., FU S. Zea mays cultivation, biochar, and arbuscular mycorrhizal fungal inoculation influenced lead immobilization. *Microbiology Spectrum*, 12, 165267, 2024. <
https://doi.org/10.1128/spectr...> PMid:38393320 PMCid:PMC10986566.
29.
LIU J., HE T., YANG Z., PENG S., ZHU Y., LI H., WEI Y. Insight into the mechanism of nano‑TiO₂‑doped biochar in mitigating cadmium mobility in soil‑pak choi system. *Science of The Total Environment*, 916, 169996, 2024. <
https://doi.org/10.1016/j.scit...> PMid:38224887.
30.
MA J., QIU Y., ZHAO J., OUYANG X., ZHAO Y., WENG L., LI Y. Effect of agricultural organic inputs on nanoplastics transport in saturated goethite‑coated porous media: particle size selectivity and role of dissolved organic matter. *Environmental Science & Technology*, 56 (6), 3524, 2022. <
https://doi.org/10.1021/acs.es...> PMid:35226472 PMCid:PMC8928475.
31.
KHAN I., AFTAB M., SHAKIR S., ALI M., QAYYUM S., REHMAN M.U., HALEEM K.S., TOUSEEF I. Mycoremediation of heavy metal (Cd and Cr)-polluted soil through indigenous metallotolerant fungal isolates. *Environmental Monitoring and Assessment*, 191 (9), 2019. <
https://doi.org/10.1007/s10661...> PMid:31440913.
32.
SUN S.-C., CHEN J.-X., WANG Y.-G., LENG F.-F., ZHAO J., CHEN K., ZHANG Q.-C. Molecular mechanisms of heavy metals resistance of *Stenotrophomonas rhizophila* JC1 by whole genome sequencing. *Archives of Microbiology*, 203 (5), 2699, 2021. <
https://doi.org/10.1007/s00203...> PMid:33715030.
33.
LI Y., YU X., CUI Y., TU W., SHEN T., YAN M., WEI Y., CHEN X., WANG Q., CHEN Q., GU Y., ZHAO K., XIANG Q., ZOU L., MA M. The potential of cadmium ion‑immobilized *Rhizobium pusense* KG2 to prevent soybean root from absorbing cadmium in contaminated soil. *Journal of Applied Microbiology*, 126 (3), 919, 2019. <
https://doi.org/10.1111/jam.14...> PMid:30489679.
34.
MO F., LI H., LI Y., CUI W., WANG M., LI Z., CHAI R., WANG H. Toxicity of Ag⁺ on microstructure, biochemical activities and genic material of *Trifolium pratense* L. seedlings with special reference to phytoremediation. *Ecotoxicology and Environmental Safety*, 195, 110499, 2020. <
https://doi.org/10.1016/j.ecoe...> PMid:32208213.
35.
ZENG X., XU H., LU J., CHEN Q., LI W., WU L., TANG J., MA L. The immobilization of soil cadmium by the combined amendment of bacteria and hydroxyapatite. *Scientific Reports*, 10 (1), 2189, 2020. <
https://doi.org/10.1038/s41598...> PMid:32041971 PMCid:PMC7010816.
36.
SARKAR S., PATRA S.K. Evaluation of chemical extraction methods for determining plant‑available potassium in some soils of West Bengal, India. *Communications in Soil Science and Plant Analysis*, 48 (9), 1008, 2017. <
https://doi.org/10.1080/001036...>.
37.
BAI B., CHEN J., BAI F., NIE Q., JIA X. Corrosion effect of acid/alkali on cementitious red mud‑fly ash materials containing heavy metal residues. *Environmental Technology & Innovation*, 33, 103485, 2024. <
https://doi.org/10.1016/j.eti....>.
38.
BAI B., XU T., NIE Q., LI P. Temperature‑driven migration of heavy metal Pb²⁺ along with moisture movement in unsaturated soils. *International Journal of Heat and Mass Transfer*, 153, 119573, 2020. <
https://doi.org/10.1016/j.ijhe...>.
39.
DU K., HUANG J., WANG W., ZENG Y., LI X., ZHAO F. Monitoring low‑temperature stress in winter wheat using TROPOMI solar‑induced chlorophyll fluorescence. *IEEE Transactions on Geoscience and Remote Sensing*, 62, 1, 2024. <
https://doi.org/10.1109/TGRS.2...>.
40.
HE M.-Y., DONG J.-B., JIN Z., LIU C.-Y., XIAO J., ZHANG F., SUN H., ZHAO Z.-Q., GOU L.-F., LIU W\.-G., LUO C.-G., SONG Y.-G., MA L., DENG L. Pedogenic processes in loess‑paleosol sediments: Clues from Li isotopes of leachate in Luochuan loess. *Geochimica et Cosmochimica Acta*, 299, 151, 2021. <
https://doi.org/10.1016/j.gca....>.
41.
HE M.-Y., REN T.X., JIN Z.D., DENG L., LIU H.J., CHENG Y.Y., LI Z.Y., LIU X.X., YANG Y., CHANG H. Precise analysis of potassium isotopic composition in plant materials by multi‑collector ICP‑MS. *Spectrochimica Acta Part B*, 209, 106781, 2023. <
https://doi.org/10.1016/j.sab....>.
42.
WANG X., WANG T., XU J., SHEN Z., YANG Y., CHEN A., WANG S., LIANG E., PIAO S. Enhanced habitat loss of the Himalayan endemic flora driven by warming‑forced upslope tree expansion. *Nature Ecology & Evolution*, 6 (7), 890, 2022. <
https://doi.org/10.1038/s41559...> PMid:35654898.
43.
ZHANG T., SONG B., HAN G., ZHAO H., HU Q., ZHAO Y., LIU H. Effects of coastal wetland reclamation on soil organic carbon, total nitrogen, and total phosphorus in China: A meta‑analysis. *Land Degradation & Development*, 34 (11), 3340, 2023. <
https://doi.org/10.1002/ldr.46...>.
44.
JIANG C., WANG Y., YANG Z., ZHAO Y. Do adaptive policy adjustments deliver ecosystem‑agriculture‑economy co‑benefits in land degradation neutrality efforts? Evidence from southeast coast of China. *Environmental Monitoring and Assessment*, 195 (10), 2023. <
https://doi.org/10.1007/s10661...> PMid:37713117.
45.
MOGAL C.S., SOLANKI V.H., KANSARA R.V., JHA S., SINGH S., PAREKH V.B., RAJKUMAR B.K. UHPLC‑MS/MS and qRT‑PCR profiling of PGP agents and *Rhizobium* spp. of induced phytohormones for growth promotion in mungbean (var. Co4). *Heliyon*, 8 (5), e09532, 2022. <
https://doi.org/10.1016/j.heli...> PMid:35663748 PMCid:PMC9160038.
46.
BAI B., BAI F., NIE Q., JIA X. A high‑strength red mud‑fly ash geopolymer and the implications of curing temperature. *Powder Technology*, 416, 118242, 2023. <
https://doi.org/10.1016/j.powt...>.
47.
NIE Q., WANG W., GUO W., LI H. Experimental Study on the Coupled Heat‑Moisture‑Heavy Metal Pollutant Transfer Process in Soils. *Advances in Civil Engineering*, 2021, 1, 2021. <
https://doi.org/10.1155/2021/5...>.
48.
WANG Y.-N., WANG Q., LI Y., WANG H., GAO Y., SUN Y., WANG B., BIAN R., LI W., ZHAN M. Impact of incineration slag co‑disposed with municipal solid waste on methane production and methanogens ecology in landfills. *Bioresource Technology*, 377, 128978, 2023. <
https://doi.org/10.1016/j.bior...> PMid:36990329.
49.
ZHANG X., HUANG J., GONG Y., ZHANG L., HUANG F. Climate influence on zinc isotope variations in a loess‑paleosol sequence of the Chinese Loess Plateau. *Geochimica et Cosmochimica Acta*, 321, 115, 2022. <
https://doi.org/10.1016/j.gca....>.
50.
LI X., HAN G., ZHANG Q., QU R., MIAO Z. Accurate lithium isotopic analysis of twenty geological reference materials by multi‑collector ICP‑MS. *Spectrochimica Acta Part B*, 188, 106348, 2022. <
https://doi.org/10.1016/j.sab....>.
51.
ZHANG S., BAI X., ZHAO C., TAN Q., LUO G., WANG J., LI Q., WU L., CHEN F., LI C., DENG Y., YANG Y., XI H. Global CO consumption by silicate rock chemical weathering: its past and future. *Earth's Future*, 9 (5), 2021. <
https://doi.org/10.1029/2020EF...>.
52.
ZHAO Y., HAO Y., CHENG K., WANG L., DONG W., LIU Z., YANG F. Artificial humic acid mediated migration of phosphorus in soil: Experiment and modelling. *CATENA*, 238, 107896, 2024. <
https://doi.org/10.1016/j.cate...>.
53.
YU Z., XU X., GUO L., YUZUAK S., LU Y. Physiological and biochemical effects of polystyrene micro/nano plastics on *Arabidopsis thaliana*. *Journal of Hazardous Materials*, 469, 133861, 2024. <
https://doi.org/10.1016/j.jhaz...> PMid:38430596.
54.
LIU J., WANG Y., LI Y., PEÑUELAS J., ZHAO Y., SARDANS J., TETZLAFF D., LIU J., LIU X., YUAN H., LI Y., CHEN J., WU J. Soil ecological stoichiometry synchronously regulates stream nitrogen and phosphorus concentrations and ratios. *CATENA*, 231, 107357, 2023. <
https://doi.org/10.1016/j.cate...>.
55.
HU Q., ZHAO Y., HU X., QI J., SUO L., PAN Y., SONG B., CHEN X. Effect of saline land reclamation by constructing the "Raised Field‑Shallow Trench" pattern on agroecosystems in Yellow River Delta. *Agricultural Water Management*, 261, 107345, 2022. <
https://doi.org/10.1016/j.agwa...>.
56.
TONG J., HU Y., DU Z., YANG X. Effects of land use and cover change on soil organic carbon and total nitrogen in southwest China Karst region: A Meta‑analysis. *Authorea, Inc.*, 2020. <
https://doi.org/10.22541/au.15...>.
57.
SINGH K., TRIPATHI S., CHANDRA R. Bacterial assisted phytoremediation of heavy metals and organic pollutants by *Cannabis sativa* as accumulator plants growing on distillery sludge for ecorestoration. *Journal of Environmental Management*, 332, 117294, 2023. <
https://doi.org/10.1016/j.jenv...> PMid:36708597.
58.
MITRA S., PRAMANIK K., GHOSH P.K., SOREN T., SARKAR A., DEY R.S., PANDEY S., MAITI T.K. Characterization of Cd‑resistant *Klebsiella michiganensis* MCC3089 and its potential for rice seedling growth promotion under Cd stress. *Microbiological Research*, 210, 12, 2018. <
https://doi.org/10.1016/j.micr...> PMid:29625654.
59.
DE OLIVEIRA V.H., ULLAH I., DUNWELL J.M., TIBBETT M. Bioremediation potential of Cd by transgenic yeast expressing a metallothionein gene from *Populus trichocarpa*. *Ecotoxicology and Environmental Safety*, 202, 110917, 2020. <
https://doi.org/10.1016/j.ecoe...> PMid:32800252.
60.
BABU A.G., SHEA P.J., SUDHAKAR D., JUNG I.-B., OH B.-T. Potential use of *Pseudomonas koreensis* AGB‑1 in association with *Miscanthus sinensis* to remediate heavy metal(loid)‑contaminated mining site soil. *Journal of Environmental Management*, 151, 160, 2015. <
https://doi.org/10.1016/j.jenv...> PMid:25575343.
61.
DURAND A., PIUTTI S., RUE M., MOREL J.L., ECHEVARRIA G., BENIZRI E. Improving nickel phytoextraction by co‑cropping hyperaccumulator plants inoculated with plant‑growth‑promoting rhizobacteria. *Plant and Soil*, 399 (1‑2), 179, 2015. <
https://doi.org/10.1007/s11104...>.