Microbial-driven mechanisms for the effects of heavy metals on soil organic carbon storage: A global analysis
Open accessAbstract
Heavy metal (HM) enrichment is closely related to soil organic carbon (SOC) pools in terrestrial ecosystems, which are deeply intertwined with soil microbial processes. However, the influence of HMs on SOC remains contentious in terms of magnitude and direction. A global analysis of 155 publications was conducted to integrate the synergistic responses of SOC and microorganisms to HM enrichment. A significant increase of 13.6 % in SOC content was observed in soils exposed to HMs. The response of SOC to HMs primarily depends on soil properties and habitat conditions, particularly the initial SOC content, mean annual precipitation (MAP), initial soil pH, and mean annual temperature (MAT). The presence of HMs resulted in significant decreases in the activities of key soil enzymes, including 31.9 % for soil dehydrogenase, 24.8 % for β-glucosidase, 35.8 % for invertase, and 24.3 % for cellulose. HMs also exerted inhibitory effects on microbial biomass carbon (MBC) (26.6 %), microbial respiration (MR) (19.7 %), and the bacterial Shannon index (3.13 %) but elevated the microbial metabolic quotient (qCO 2 ) (20.6 %). The HM enrichment-induced changes in SOC exhibited positive correlations with the response of MBC (r = 0.70, p 2 (r = 0.50, p < 0.01), while it was negatively associated with β-glucosidase activity (r = 0.72, p < 0.01) and MR (r = 0.39, p < 0.01). These findings suggest that the increase in SOC storage is mainly attributable to the inhibition of soil enzymes and microorga…
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Distinct microbial populations possess unique metabolic capabilities, forming organic substances or reducing HMs.
“Distinct microbial populations possess unique metabolic capabilities, forming organic substances or reducing HMs [398].”
From Harnessing bacterial consortia for effective bioremediation: targeted removal of heavy metals, hydrocarbons, and persistent pollutants (2025) · cites this paper as [398]
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A basic introduction to fixed-effect and random-effects models for meta-analysis
Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2010) · Research Synthesis Methods · doi:10.1002/jrsm.12 · Cited by 6,793 · see citing works
Wallace, B. C., Lajeunesse, M. J., Dietz, G., Dahabreh, I. J., Trikalinos, T. A., Schmid, C. H., & Gurevitch, J. (2017) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.12708 · Cited by 421 · see citing works
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Research works printed but not linked: 90
- Aponte, 2020, Meta-analysis of heavy metal effects on soil enzyme activities, Sci. Total Environ., 737, 10.1016/j.scitotenv.2020.139744 · DOI
- Aponte, 2021, Enzyme activities and microbial functional diversity in metal(loid) contaminated soils near to a copper smelter, Sci. Total Environ., 779, 10.1016/j.scitotenv.2021.146423 · DOI
- Baumann, 2013, Soil microbial diversity affects soil organic matter decomposition in a silty grassland soil, Biogeochemistry, 114, 201, 10.1007/s10533-012-9800-6 · DOI
- Beillouin, 2023, A global meta-analysis of soil organic carbon in the Anthropocene, Nat. Commun., 14, 3700, 10.1038/s41467-023-39338-z · DOI
- Bhattacharyya, 2021, Soil organic carbon is significantly associated with the pore geometry, microbial diversity and enzyme activity of the macro-aggregates under different land uses, Sci. Total Environ., 778, 10.1016/j.scitotenv.2021.146286 · DOI
- Bradford, 2013, Empirical evidence that soil carbon formation from plant inputs is positively related to microbial growth, Biogeochemistry, 113, 271, 10.1007/s10533-012-9822-0 · DOI
- Cang, 2009, Effects of electrokinetic treatment of a heavy metal contaminated soil on soil enzyme activities, J. Hazard. Mater., 172, 1602, 10.1016/j.jhazmat.2009.08.033 · DOI
- Chen, 2022, Molecular transformation of dissolved organic carbon of rhizosphere soil induced by flooding and copper pollution, Geoderma, 407, 10.1016/j.geoderma.2021.115563 · DOI
- Chen, 2014, Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil, FEMS Microbiol. Ecol., 87, 164, 10.1111/1574-6941.12212 · DOI
- Chen, 2018, Differential responses of carbon-degrading enzyme activities to warming: implications for soil respiration, Glob. Chang. Biol., 24, 4816, 10.1111/gcb.14394 · DOI
- Chen, 2020, Spectroscopic response of soil organic matter in mining area to Pb/Cd heavy metal interaction: A mirror of coherent structural variation, J. Hazard. Mater., 393, 10.1016/j.jhazmat.2020.122425 · DOI
- Chen, 2019, The sensitivity of soil microbial respiration declined due to crop straw addition but did not depend on the type of crop straw, Environ. Sci. Pollut. Res., 26, 30167, 10.1007/s11356-019-06185-9 · DOI
- Chen, 2020, Selective pressures of heavy metals on microbial community determine microbial functional roles during composting: Sensitive, resistant and actor, J. Hazard. Mater., 398, 10.1016/j.jhazmat.2020.122858 · DOI
- Chibuike, 2014, Heavy Metal Polluted Soils: Effect on Plants and Bioremediation Methods, Appl. Environ. Soil Sci., 2014, 1, 10.1155/2014/752708 · DOI · Paper page
- Cui, 2022, Influence of rainfall infiltration on soil colloids-heavy metals co-release and co-migration in infiltration column, Environ. Chem., 41, 2842
- Cui, 2021, Effects of long-term cropping regimes on SOC stability, soil microbial community and enzyme activities in the Mollisol region of Northeast China, Appl. Soil Ecol., 164, 10.1016/j.apsoil.2021.103941 · DOI
- Davenport, 2023, Decomposition decreases molecular diversity and ecosystem similarity of soil organic matter, Proc. Natl. Acad. Sci., 120, 10.1073/pnas.2303335120 · DOI
- de Souza, 2023, Composition of soil organic matter and the structure and diversity of soil bacteria and archaea, in crop systems under no-till in a subtropical ecosystem, Soil Tillage Res., 234, 10.1016/j.still.2023.105813 · DOI
- Du Laing, 2009, Trace metal behaviour in estuarine and riverine floodplain soils and sediments: A review, Sci. Total Environ., 407, 3972, 10.1016/j.scitotenv.2008.07.025 · DOI
- Duval, 2000, Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis, Biometrics, 56, 455, 10.1111/j.0006-341X.2000.00455.x · DOI · Paper page
- Enya, 2020, Effects of heavy metals on organic matter decomposition in inundated soils: microcosm experiment and field examination, Sci. Total Environ., 724, 10.1016/j.scitotenv.2020.138223 · DOI
- Feng, 2023, Trade-offs in carbon-degrading enzyme activities limit long-term soil carbon sequestration with biochar addition, Biol. Rev. Camb. Philos. Soc., 10.1111/brv.12949 · DOI
- Ferreira, 2016, Effects of anthropogenic heavy metal contamination on litter decomposition in streams - A meta-analysis, Environ. Pollut., 210, 261, 10.1016/j.envpol.2015.12.060 · DOI
- German, 2012, The Michaelis-Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study, Glob. Chang. Biol., 18, 1468, 10.1111/j.1365-2486.2011.02615.x · DOI
- Gong, 2022, Effects of different land use types and soil depths on soil mineral elements, soil enzyme activity, and fungal community in Karst Area of Southwest China, Int. J. Environ. Res. Public Health, 19, 10.3390/ijerph19053120 · DOI
- Han, 2016, Some concepts of soil organic carbon characteristics and mineral interaction from a review of literature, Soil Biol. Biochem., 107, 10.1016/j.soilbio.2015.11.023 · DOI
- Hao, 2005, Standard deviation and standard error of arithmetic mean, Acta Editologica, 17, 116
- He, 2023, Global analysis of the perturbation effects of metal-based nanoparticles on soil nitrogen cycling, Glob Chang Biol, 29, 4001, 10.1111/gcb.16735 · DOI
- He, 2023, Microbial carbon use efficiency in different ecosystems: A meta-analysis based on a biogeochemical equilibrium model, Glob. Chang. Biol., 10.1111/gcb.16861 · DOI
- Hedges, 1999, The meta-analysis of response ratios in experimental ecology, Ecology, 80, 1150, 10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2 · DOI · Paper page
- Hu, 2022, Linking bacterial life strategies with soil organic matter accrual by karst vegetation restoration, Soil Biol. Biochem.
- Huang, 2022, Acidification of soil due to forestation at the global scale, For. Ecol. Manage., 505, 10.1016/j.foreco.2021.119951 · DOI
- Ji, 2014, Climatic and edaphic controls on soil pH in alpine grasslands on the Tibetan Plateau, China: a quantitative analysis, Pedosphere, 24, 39, 10.1016/S1002-0160(13)60078-8 · DOI
- Jia, 2020, A new perspective on functional redundancy and phylogenetic niche conservatism in soil microbial communities, Pedosphere, 30, 18, 10.1016/S1002-0160(19)60826-X · DOI
- Jin, 2018, Effects and mechanisms of microbial remediation of heavy metals in soil: a critical review, Appl. Sci.-Basel, 8
- Keiblinger, 2018, Assessment of Cu applications in two contrasting soils-effects on soil microbial activity and the fungal community structure, Ecotoxicology, 27, 217, 10.1007/s10646-017-1888-y · DOI
- Li, 2021, Functional redundancy and specific taxa modulate the contribution of prokaryotic diversity and composition to multifunctionality, Mol. Ecol., 30, 2915, 10.1111/mec.15935 · DOI
- Li, 2023, Soil nutrients shape the composition and function of fungal communities in abandoned ancient rice terraces, J. Environ. Manage., 329, 10.1016/j.jenvman.2022.117064 · DOI
- Li, 2015, Field-based evidence for consistent responses of bacterial communities to copper contamination in two contrasting agricultural soils, Front. Microbiol., 6
- Lin, 2022, Influence of different types of nanomaterials on soil enzyme activity: A global meta-analysis, Nano Today, 42, 10.1016/j.nantod.2021.101345 · DOI
- Liu, 2020, The responses of soil enzyme activities, microbial biomass and microbial community structure to nine years of varied zinc application rates, Sci Total Environ, 737, 10.1016/j.scitotenv.2020.140245 · DOI
- Liu, 2018, Canopy gaps accelerate soil organic carbon retention by soil microbial biomass in the organic horizon in a subalpine fir forest, Appl. Soil Ecol., 125, 169, 10.1016/j.apsoil.2018.01.002 · DOI
- Lv, 2023, Global magnitude of rhizosphere effects on soil microbial communities and carbon cycling in natural terrestrial ecosystems, Sci. Total Environ., 856, 10.1016/j.scitotenv.2022.158961 · DOI
- Ma, 2021, Heavy metal pollution increases CH4 and decreases CO2 emissions due to soil microbial changes in a mangrove wetland: Microcosm experiment and field examination, Chemosphere, 269, 10.1016/j.chemosphere.2020.128735 · DOI
- Margida, 2020, Estimating relative cellulolytic and ligninolytic enzyme activities as functions of lignin and cellulose content in decomposing plant litter, Soil Biol. Biochem., 141, 10.1016/j.soilbio.2019.107689 · DOI
- Maron, 2018, High microbial diversity promotes soil ecosystem functioning, Appl. Environ. Microbiol., 84, 10.1128/AEM.02738-17 · DOI
- Mganga, 2022, Microbial carbon use efficiency along an altitudinal gradient, Soil Biol. Biochem., 10.1016/j.soilbio.2022.108799 · DOI
- Morrissey, 2023, Carbon acquisition ecological strategies to connect soil microbial biodiversity and carbon cycling, Soil Biol. Biochem., 177, 10.1016/j.soilbio.2022.108893 · DOI
- Niu, 2020, Effects of heavy metal pollution on the carbon content of surface sediments of mangroves in the Pearl River Estuary, Acta Ecol. Sin., 40, 8549
- Pellegrino, 2021, Eukaryotes in soil aggregates across conservation managements: Major roles of protists, fungi and taxa linkages in soil structuring and C stock, Soil Biol. Biochem., 163, 10.1016/j.soilbio.2021.108463 · DOI
- Peter, 2011, Function-specific response to depletion of microbial diversity, ISME J., 5, 351, 10.1038/ismej.2010.119 · DOI
- Prommer, 2020, Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity, Glob. Chang. Biol., 26, 669, 10.1111/gcb.14777 · DOI
- Raiesi, 2019, Interactive effect of salinity and cadmium toxicity on soil microbial properties and enzyme activities, Ecotoxicol. Environ. Saf., 168, 221, 10.1016/j.ecoenv.2018.10.079 · DOI
- Rajkumar, 2013, Climate change driven plant-metal-microbe interactions, Environ. Int., 53, 74, 10.1016/j.envint.2012.12.009 · DOI
- Sinkko, 2013, Bacteria contribute to sediment nutrient release and reflect progressed eutrophication-driven hypoxia in an organic-rich continental sea, PLoS One, 8, 10.1371/journal.pone.0067061 · DOI
- Smith, 2016, Global change pressures on soils from land use and management, Glob Chang Biol, 22, 1008, 10.1111/gcb.13068 · DOI
- Soong, 2020, Microbial carbon limitation: The need for integrating microorganisms into our understanding of ecosystem carbon cycling, Glob. Chang. Biol., 26, 1953, 10.1111/gcb.14962 · DOI
- Stefanowicz, 2020, Soil organic matter prevails over heavy metal pollution and vegetation as a factor shaping soil microbial communities at historical Zn-Pb mining sites, Chemosphere, 240, 10.1016/j.chemosphere.2019.124922 · DOI
- Sun, 2023, Soil organic carbon content increase in the east and south of China is accompanied by soil acidification, Sci. Total Environ., 857, 10.1016/j.scitotenv.2022.159253 · DOI
- Tan, 2023, Research progresses on soil enzymes as indicators of soil health and their responses to heavy metal pollution, Acta Pedol. Sin., 60, 50
- Tang, 2022, Distribution characteristics and risk assessment of heavy metals in sediments of Shenzhen nearshore, Trans. Oceanol. Limnol., 44, 67
- Tang, 2022, Effects of heavy metals on microorganisms and enzymes in soils of lead-zinc tailing ponds, Environ. Res., 207, 10.1016/j.envres.2021.112174 · DOI
- Tang, 2019, Diagnosis of soil contamination using microbiological indices: A review on heavy metal pollution, J. Environ. Manage., 242, 121, 10.1016/j.jenvman.2019.04.061 · DOI
- Tian, 2008, Microbial biomass and activity along a natural pH gradient in forest soils in a karst region of the upper Yangtze River, China, J. For. Res., 13, 205, 10.1007/s10310-008-0073-9 · DOI
- Vicena, 2022, The effect of microbial diversity and biomass on microbial respiration in two soils along the soil chronosequence, Microorganisms, 10, 10.3390/microorganisms10101920 · DOI
- Wang, 2023, Seasonal variation modifies the spatial patterns of soil microbial community structure and enzyme activity in a meadow steppe, Appl. Soil Ecol., 182, 10.1016/j.apsoil.2022.104686 · DOI
- Wang, 2023, Effects of winter warming on the migration characteristics and pollution risk assessment of Zn, Cu, and Pb in the snow-soil continuum in seasonal snow cover area, Environ. Technol. Innov., 31, 10.1016/j.eti.2023.103159 · DOI
- Wang, 2021, Effects of marine pollution, climate, and tidal range on biomass and sediment organic carbon in Chinese mangrove forests, Catena, 202, 10.1016/j.catena.2021.105270 · DOI
- Wang, 2021, Correlation analysis between concentrations of soil heavy metal species and organic carbon in different land use types, J. Southern Agric., 52, 2417
- Wang, 2021, Soil enzyme stoichiometry is tightly linked to microbial community composition in successional ecosystems after glacier retreat, Soil Biol. Biochem., 162, 10.1016/j.soilbio.2021.108429 · DOI
- Wertz, 2006, Maintenance of soil functioning following erosion of microbial diversity, Environ. Microbiol., 8, 2162, 10.1111/j.1462-2920.2006.01098.x · DOI
- Wierzba, 2015, Biosorption of lead(II), zinc(II) and nickel(II) from industrial wastewater by Stenotrophomonas maltophilia and Bacillus subtilis, Pol. J. Chem. Technol., 17, 79, 10.1515/pjct-2015-0012 · DOI
- Wong, 2007, The sorption of Cd and Zn by different soils in the presence of dissolved organic matter from sludge, Geoderma, 137, 310, 10.1016/j.geoderma.2006.08.026 · DOI
- Wood, 2016, Microbial associated plant growth and heavy metal accumulation to improve phytoextraction of contaminated soils, Soil Biol. Biochem., 103, 131, 10.1016/j.soilbio.2016.08.021 · DOI
- Wu, 2022, Meta-analysis of the impacts of phosphorus addition on soil microbes, Agr Ecosyst Environ, 340, 10.1016/j.agee.2022.108180 · DOI
- Xu, 2021, Heavy metal pollution increases soil microbial carbon limitation: Evidence from ecological enzyme stoichiometry, Soil Ecology Lett., 3, 230, 10.1007/s42832-021-0094-2 · DOI
- Xu, 2019, Microbial functional diversity and carbon use feedback in soils as affected by heavy metals, Environ. Int., 125, 478, 10.1016/j.envint.2019.01.071 · DOI
- Yang, 2022, Nitrogen fertilization weakens the linkage between soil carbon and microbialdiversity: a global meta-analysis, Glob. Chang. Biol., 10.1111/gcb.16361 · DOI
- Yang, 2022, Differential responses of soil extracellular enzyme activities to salinization: implications for soil carbon cycling in tidal wetlands, Global Biogeochem. Cycles, 36, 10.1029/2021GB007285 · DOI
- Yang, 2022, Multiple anthropogenic pressures eliminate the effects of soil microbial diversity on ecosystem functions in experimental microcosms, Nat. Commun., 13
- Yang, 2022, Soil Heavy metal content and enzyme activity in Uncaria rhynchophylla-producing areas under different land use patterns, Int. J. Environ. Res. Public Health, 19, 10.3390/ijerph191912220 · DOI
- Yin, 2023, Soil bacterial community structure in the habitats with different levels of heavy metal pollution at an abandoned polymetallic mine, J. Hazard. Mater., 442, 10.1016/j.jhazmat.2022.130063 · DOI
- Zamulina, 2021, The influence of long-term Zn and Cu contamination in Spolic Technosols on water-soluble organic matter and soil biological activity, Ecotoxicol. Environ. Saf., 208, 10.1016/j.ecoenv.2020.111471 · DOI
- Zeng, 2011, The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants, Environ. Pollut., 159, 84, 10.1016/j.envpol.2010.09.019 · DOI
- Zheng, 2019, The inhibitory effect of cadmium and/or mercury on soil enzyme activity, basal respiration, and microbial community structure in coal mine-affected agricultural soil, Ann. Microbiol., 69, 849, 10.1007/s13213-019-01478-3 · DOI
- Zhou, 2020, Vertical distribution and controlling factors exploration of Sc, V Co, Ni, Mo and Ba in Six Soil profiles of the Mun River Basin, Northeast Thailand, Int. J. Environ. Res. Public Health, 17, 10.3390/ijerph17051745 · DOI
- Zhou, 2016, Changes in organic carbon and nitrogen in soil with metal pollution by Cd, Cu, Pb and Zn: a meta-analysis, Eur. J. Soil Sci., 67, 237, 10.1111/ejss.12327 · DOI
- Zhou, 2023, Microbial necromass in cropland soils: A global meta-analysis of management effects, Glob. Chang. Biol., 29, 1998, 10.1111/gcb.16613 · DOI
- Zou, 2021, Spatial variation in microbial community in response to As and Pb contamination in paddy soils near a Pb-Zn mining site, Front. Environ. Sci., 9, 10.3389/fenvs.2021.630668 · DOI
- Zuccarini, 2023, Altered activities of extracellular soil enzymes by the interacting global environmental changes, Glob. Chang. Biol., 29, 2067, 10.1111/gcb.16604 · DOI
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Qattan, S. Y. A. (2025) · Environmental Sciences Europe · doi:10.1186/s12302-025-01103-y · Cited by 109 · see citing works
- Authors
- Zeng, K., Huang, X., Guo, J., Dai, C., He, C., Chen, H., & Xin, G.
- Affiliations
- Sun Yat-sen University (CN)
- Corresponding author
- Guo, Junjie
- Xin, Guorong
- Venue
- Environment International
- Publisher
- Elsevier BV
- Published
- 2024-02
- Volume
- 184
- Pages
- 108467
- ISSN
- 0160-4120 (ISSN-L)
- OpenAlex
- W4391346250
- Cited by
- 69
- References
- 2
- Citations by year
- 2026: 27 · 2025: 33 · 2024: 9
- FWCI
- 1.96
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Environment International (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Natural Science Foundation of China (32171683, 32372808, 42007047)
- Science, Technology and Innovation Commission of Shenzhen Municipality (JCYJ20220530145606015, JCYJ20230807111217035)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
- Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- heavy metals, soil organic carbon, soil carbon storage, soil microbial processes, soil enzyme activity, microbial biomass carbon, microbial respiration, microbial metabolic quotient, soil carbon dynamics, soil pH, precipitation, soil temperature, soil contamination
- MeSH terms
- Carbon, Soil, Soil Microbiology, Ecosystem, Metals, Heavy, Cellulases
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