Heavy metal pollution increases soil microbial carbon limitation: Evidence from ecological enzyme stoichiometry

Mingzhe Xu, Yongxing Cui, Jingzi Beiyuan, Xia Wang, Chengjiao Duan, Linchuan Fang

PDF(982 KB)
PDF(982 KB)
Soil Ecology Letters ›› 2021, Vol. 3 ›› Issue (3) : 230-241. DOI: 10.1007/s42832-021-0094-2
RESEARCH ARTICLE
RESEARCH ARTICLE

Heavy metal pollution increases soil microbial carbon limitation: Evidence from ecological enzyme stoichiometry

Author information +
History +

Highlights

• The microbial metabolism was limited by soil carbon (C) and phosphorus (P) under heavy metal stress.

• The increase of heavy metal concentration significantly increased the microbial C limitation.

• Heavy metal pollution can increase the loss of soil C by affecting microbial metabolism.

• Microbial metabolism limitation can be used as a potential index to evaluate the toxicity of heavy metals.

Abstract

Heavy metals can exist in soil for a long time and seriously affect soil quality. The coexistence of various heavy metal pollutants leads to biotoxicity and alters the activity of microorganisms. Soil microbial metabolism plays an important role in nutrient cycling and biochemical processes of soil ecosystem. However, the effects of heavy metal contamination on microbial metabolism in soil are still unclear. This study aims to reveal the responses of microbial metabolic limitation to heavy metals using extracellular enzyme stoichiometry, and further to evaluate the potential impacts of heavy metal pollution on soil nutrient cycle. The results showed that soil microbial metabolism reflected by the ecoenzymatic activities had a significant response to soil heavy metals pollution. The metabolism was limited by soil carbon (C) and phosphorus (P) under varied heavy metal levels, and the increase of heavy metal concentration significantly increased the microbial C limitation, while had no effect on microbial P limitation. Microorganisms may increase the energy investment in metabolism to resist heavy metal stress and thus induce C release. The results suggest that energy metabolism selected by microorganisms in response to long-term heavy metal stress could increase soil C release, which is not conducive to the soil C sequestration. Our study emphasizes that ecoenzymatic stoichiometry could be a promising methodology for evaluating the toxicity of heavy metal pollution and its ecological effects on nutrient cycling.

Graphical abstract

Keywords

Heavy metal contamination / Microbial metabolisms / Ecoenzymatic stoichiometry / Soil nutrient limitation

Cite this article

Download citation ▾
Mingzhe Xu, Yongxing Cui, Jingzi Beiyuan, Xia Wang, Chengjiao Duan, Linchuan Fang. Heavy metal pollution increases soil microbial carbon limitation: Evidence from ecological enzyme stoichiometry. Soil Ecology Letters, 2021, 3(3): 230‒241 https://doi.org/10.1007/s42832-021-0094-2

References

[1]
Alkorta, I., Aizpurua, A., Riga, P., Albizu, I., Amezaga, I., Garbisu, C., 2003. Soil enzyme activities as biological indicators of soil health. Reviews on Environmental Health 18, 65–73
CrossRef Google scholar
[2]
Allison, S.D., Wallenstein, M.D., Bradford, M.A., 2010. Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience 3, 336–340
CrossRef Google scholar
[3]
Aponte, H., Medina, J., Butler, B., Meier, S., Cornejo, P., Kuzyakov, Y., 2020a. Soil quality indices for metal(loid) contamination: An enzymatic perspective. Land Degradation & Development 31, 2700–2719
CrossRef Google scholar
[4]
Aponte, H., Meli, P., Butler, B., Paolini, J., Matus, F., Merino, C., Cornejo, P., Kuzyakov, Y., 2020b. Meta-analysis of heavy metal effects on soil enzyme activities. Science of the Total Environment 737, 12
CrossRef Google scholar
[5]
Baumann, K., Dignac, M.F., Rumpel, C., Bardoux, G., Sarr, A., Steffens, M., Maron, P.A., 2012. Soil microbial diversity affects soil organic matter decomposition in a silty grassland soil. Biogeochemistry 114, 201–212
CrossRef Google scholar
[6]
Beattie, R.E., Henke, W., Campa, M.F., Hazen, T.C., McAliley, L.R., Campbell, J.H., 2018. Variation in microbial community structure correlates with heavy-metal contamination in soils decades after mining ceased. Soil Biology & Biochemistry 126, 57–63
CrossRef Google scholar
[7]
Beiyuan, J., Fang, L., Chen, H., Li, M., Liu, D., Wang, Y., 2020. Nitrogen of EDDS enhanced removal of potentially toxic elements and attenuated their oxidative stress in a phytoextraction process. Environmental Pollution 268, 115719
CrossRef Google scholar
[8]
Berg, J., Brandt, K.K., Al-Soud, W.A., Holm, P.E., Hansen, L.H., Sorensen, S.J., Nybroe, O., 2012. Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term Cu exposure. Applied and Environmental Microbiology 78, 7438–7446
CrossRef Google scholar
[9]
Blagodatskaya, E., Blagodatsky, S., Anderson, T.H., Kuzyakov, Y., 2014. Microbial growth and carbon use efficiency in the rhizosphere and root-free soil. PLoS One 9, 9
CrossRef Google scholar
[10]
Boamponsem, L.K., Adam, J.I., Dampare, S.B., Nyarko, B.J.B., Essumang, D.K., 2010. Assessment of atmospheric heavy metal deposition in the Tarkwa gold mining area of Ghana using epiphytic lichens. Nuclear Instruments & Methods in Physics Research. Section B, Beam Interactions with Materials and Atoms 268, 1492–1501
CrossRef Google scholar
[11]
Bore, E.K., Apostel, C., Halicki, S., Kuzyakov, Y., Dippold, M.A., 2017. Soil microorganisms can overcome respiration inhibition by coupling intra- and extracellular metabolism: C-13 metabolic tracing reveals the mechanisms. ISME Journal 11, 1423–1433
CrossRef Google scholar
[12]
Bremner J., Mulvaney C., 1996. Nitrogen-total. Methods of soil analysis chemical methods part, 72:532–535.
[13]
Cang, L., Zhou, D.M., Wang, Q.Y., Wu, D.Y., 2009. Effects of electrokinetic treatment of a heavy metal contaminated soil on soil enzyme activities. Journal of Hazardous Materials 172, 1602–1607
CrossRef Google scholar
[14]
Chen, L., Feng, Q., Li, C., Wei, Y., Zhao, Y., Feng, Y., Zheng, H., Li, F., Li, H., 2017. Impacts of aquaculture wastewater irrigation on soil microbial functional diversity and community structure in arid regions. Scientific Reports 7, 7
CrossRef Google scholar
[15]
Choppala, G., Saifullah, N., Bolan, S., Bibi, M., Iqbal, Z., Rengel, A., Kunhikrishnan, N., Ashwath, Y.S., Ok, 2014. Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Critical Reviews in Plant Sciences 33, 374–391
CrossRef Google scholar
[16]
Cui, Y., Fang, L., Guo, X., Han, F., Ju, W., Ye, L., Wang, X., Tan, W., Zhang, X., 2019. Natural grassland as the optimal pattern of vegetation restoration in arid and semi-arid regions: Evidence from nutrient limitation of soil microbes. Science of the Total Environment 648, 388–397
CrossRef Google scholar
[17]
Cui, Y., Fang, L., Guo, X., Wang, X., Zhang, Y., Li, P., Zhang, X., 2018. Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biology & Biochemistry 116, 11–21
CrossRef Google scholar
[18]
Diao, Z., 2016. Effects of exogenous heavy metals on soil nutrients and microbial activity of different types. Dissertation. Northwest A&F University (in Chinese).
[19]
Duan, C., Fang, L., Yang, C., Chen, W., Cui, Y., Li, S., 2018. Reveal the response of enzyme activities to heavy metals through in situ zymography. Ecotoxicology and Environmental Safety 156, 106–115
CrossRef Google scholar
[20]
Fang, L., Liu, Y., Tian, H., Chen, H., Wang, Y., Huang, M., 2017. Proper land use for heavy metal-polluted soil based on enzyme activity analysis around a Pb-Zn mine in Feng County, China. Environmental Science and Pollution Research International 24, 28152–28164
CrossRef Google scholar
[21]
Frey, S.D., Gupta, V., Elliott, E.T., Paustian, K., 2001. Protozoan grazing affects estimates of carbon utilization efficiency of the soil microbial community. Soil Biology & Biochemistry 33, 1759–1768
CrossRef Google scholar
[22]
German, D.P., Weintraub, M.N., Grandy, A.S., Lauber, C.L., Rinkes, Z.L., Allison, S.D., 2011. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biology & Biochemistry 43, 1387–1397
CrossRef Google scholar
[23]
Golebiewski, M., Deja-Sikora, E., Cichosz, M., Tretyn, A., Wrobel, B., 2014. 16S rDNA pyrosequencing analysis of bacterial community in heavy metals polluted soils. Microbial Ecology 67, 635–647
CrossRef Google scholar
[24]
Hu, X.F., Jiang, Y., Shu, Y., Hu, X., Liu, L., Luo, F., 2014. Effects of mining wastewater discharges on heavy metal pollution and soil enzyme activity of the paddy fields. Journal of Geochemical Exploration 147, 139–150
CrossRef Google scholar
[25]
Jin, Y., Luan, Y., Ning, Y., Wang, L., 2018. Effects and mechanisms of microbial remediation of heavy metals in Soil: A Critical Review. Applied Sciences-Basel 8, 1336
[26]
Jones, D.L., Kielland, K., Sinclair, F.L., Dahlgren, R.A., Newsham, K.K., Farrar, J.F., Murphy, D.V., 2009. Soil organic nitrogen mineralization across a global latitudinal gradient. Global Biogeochemical Cycles 23, 23
CrossRef Google scholar
[27]
Ju, W., Liu, L., Fang, L., Cui, Y., Duan, C., Wu, H., 2019. Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicology and Environmental Safety 167, 218–226
CrossRef Google scholar
[28]
Kandeler, E., Tscherko, D., Bruce, K.D., Stemmer, M., Hobbs, P.J., Bardgett, R.D., Amelung, W., 2000. Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biology and Fertility of Soils 32, 390–400
CrossRef Google scholar
[29]
Khan, S., Cao, Q., Hesham, A.E.L., Xia, Y., He, J.Z., 2007. Soil enzymatic activities and microbial community structure with different application rates of Cd and Pb. Journal of Environmental Sciences (China) 19, 834–840
CrossRef Google scholar
[30]
Komy, Z.R., 1995. Comparative-study of titrimetric and gravimetric methods for the determination of organic-carbon in soils. International Journal of Environmental Analytical Chemistry 60, 41–47
CrossRef Google scholar
[31]
Kuperman, R.G., Carreiro, M.M., 1997. Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem. Soil Biology & Biochemistry 29, 179–190
CrossRef Google scholar
[32]
Li, X., Meng, D., Li, J., Yin, H., Liu, H., Liu, X., Cheng, C., Xiao, Y., Liu, Z., Yan, M., 2017. Response of soil microbial communities and microbial interactions to long-term heavy metal contamination. Environmental Pollution 231, 908–917
CrossRef Google scholar
[33]
Lin, Y., Ye, Y., Hu, Y., Shi, H., 2019. The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotoxicology and Environmental Safety 180, 557–564
CrossRef Google scholar
[34]
Liu, G., Tao, L., Liu, X., Hou, J., Wang, A., Li, R., 2013. Heavy metal speciation and pollution of agricultural soils along Jishui River in non-ferrous metal mine area in Jiangxi Province, China. Journal of Geochemical Exploration 132, 156–163
CrossRef Google scholar
[35]
Markowicz, A., Cycon, M., Piotrowska-Seget, Z., 2016. Microbial community structure and diversity in long-term hydrocarbon and heavy metal contaminated soils. International Journal of Environmental Research 10, 321–332.
[36]
Mierzwa-Hersztek, M., Gondek, K., Klimkowicz-Pawlas, A., Baran, A., Bajda, T., 2018. Sewage sludge biochars management-ecotoxicity, mobility of heavy metals, and soil microbial biomass. Environmental Toxicology and Chemistry 37, 1197–1207
CrossRef Google scholar
[37]
Moorhead, D.L., Rinkes, Z.L., Sinsabaugh, R.L., Weintraub, M.N., 2013. Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Frontiers in Microbiology 4, 4
CrossRef Google scholar
[38]
Moorhead, D.L., Sinsabaugh, R.L., Hill, B.H., Weintraub, M.N., 2016. Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biology & Biochemistry 93, 1–7
CrossRef Google scholar
[39]
Oliveira, A., Pampulha, M.E., 2006. Effects of long-term heavy metal contamination on soil microbial characteristics. Journal of Bioscience and Bioengineering 102, 157–161
CrossRef Google scholar
[40]
Page, A.L., Miller, R.H., Keeney, D.R., 1982. Methods of Soil Analysis: Chemical and Microbiological Properties. American Society of Agronomy Inc & Soil ence Society of America Inc, Madison, Wisconsin.
[41]
Peng, X., Wang, W., 2016. Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biology & Biochemistry 98, 74–84
CrossRef Google scholar
[42]
Saiya-Cork, K.R., Sinsabaugh, R.L., Zak, D.R., 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry 34, 1309–1315
CrossRef Google scholar
[43]
Sheik, C.S., Mitchell, T.W., Rizvi, F.Z., Rehman, Y., Faisal, M., Hasnain, S., McInerney, M.J., Krumholz, L.R., 2012. Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PLoS One 7, 7
CrossRef Google scholar
[44]
Shen, F., Liao, R., Ali, A., Mahar, A., Guo, D., Li, R., Sun, X., Awasthi, M.K., Wang, Q., Zhang, Z., 2017. Spatial distribution and risk assessment of heavy metals in soil near a Pb/Zn smelter in Feng County, China. Ecotoxicology and Environmental Safety 139, 254–262
CrossRef Google scholar
[45]
Stuczynski, T.I., McCarty, G.W., Siebielec, G., 2003. Response of soil microbiological activities to cadmium, lead, and zinc salt amendments. Journal of Environmental Quality 32, 1346–1355
CrossRef Google scholar
[46]
Tang, J., Zhang, J., Ren, L., Zhou, Y., Gao, J., Luo, L., Yang, Y., Peng, Q., Huang, H., Chen, A., 2019. Diagnosis of soil contamination using microbiological indices: A review on heavy metal pollution. Journal of Environmental Management 242, 121–130
CrossRef Google scholar
[47]
Tripathy, S., Bhattacharyya, P., Mohapatra, R., Som, A., Chowdhury, D., 2014. Influence of different fractions of heavy metals on microbial ecophysiological indicators and enzyme activities in century old municipal solid waste amended soil. Ecological Engineering 70, 25–34
CrossRef Google scholar
[48]
Vanremortel, R., Shields, D., 1993. Comparison of clod and core methods for determination of soil bulk-density. Communications in Soil Science and Plant Analysis 24, 2517–2528
CrossRef Google scholar
[49]
Wang, F., Yao, J., Tian, L., Zhou, Y., Chen, H., Chen, H., Gai, N., Chen, Y., Zhuang, R., Zaray, G., Maskow, T., Bramanti, E., 2008. Microcalorimetric investigation of the toxic action of ammonium ferric(III) sulfate on the metabolic activity of pure microbes. Environmental Toxicology and Pharmacology 25, 351–357
CrossRef Google scholar
[50]
Wang, X., Cui, Y., Zhang, X., Ju, W., Duan, C., Wang, Y., Fang, L., 2020. A novel extracellular enzyme stoichiometry method to evaluate soil heavy metal contamination: Evidence derived from microbial metabolic limitation. Science of the Total Environment 738, 139709
CrossRef Google scholar
[51]
Wang, Y., Guo, J., Liu, R., 2001. Biosorption of heavy metals by bacteria isolated from activated sludge. Huan Jing Ke Xue 22, 72–75.
[52]
Wyszkowska, J., Kucharski, J., Lajszner, W., 2006. The effects of copper on soil biochemical properties and its interaction with other heavy metals. Polish Journal of Environmental Studies 15, 927–934.
[53]
Xian, Y., Wang, M., Chen, W., 2015. Quantitative assessment on soil enzyme activities of heavy metal contaminated soils with various soil properties. Chemosphere 139, 604–608
CrossRef Google scholar
[54]
Xiao, R., Shen, F., Du, J., Li, R., Lahori, A.H., Zhang, Z., 2018. Screening of native plants from wasteland surrounding a Zn smelter in Feng County China, for phytoremediation. Ecotoxicology and Environmental Safety 162, 178–183
CrossRef Google scholar
[55]
Xiao, X.Y., Wang, M.W., Zhu, H.W., Guo, Z.H., Han, X.Q., Zeng, P., 2017. Response of soil microbial activities and microbial community structure to vanadium stress. Ecotoxicology and Environmental Safety 142, 200–206
CrossRef Google scholar
[56]
Xu, Y., Seshadri, B., Bolan, N., Sarkar, B., Ok, Y.S., Zhang, W., Rumpel, C., Sparks, D., Farrell, M., Hall, T., Dong, Z., 2019. Microbial functional diversity and carbon use feedback in soils as affected by heavy metals. Environment International 125, 478–488
CrossRef Google scholar
[57]
Xu, Y., Seshadri, B., Sarkar, B., Wang, H., Rumpel, C., Sparks, D., Farrell, M., Hall, T., Yang, X., Bolan, N., 2018. Biochar modulates heavy metal toxicity and improves microbial carbon use efficiency in soil. Science of the Total Environment 621, 148–159
CrossRef Google scholar
[58]
Yang, J., Yang, F., Yang, Y., Xing, G., Deng, C., Shen, Y., Luo, L., Li, B., Yuan, H., 2016. A proposal of “core enzyme” bioindicator in long-term Pb-Zn ore pollution areas based on topsoil property analysis. Environmental Pollution 213, 760–769
CrossRef Google scholar
[59]
Zhang, J., Wang, L.H., Yang, J.C., Liu, H., Dai, J.L., 2015. Health risk to residents and stimulation to inherent bacteria of various heavy metals in soil. Science of the Total Environment 508, 29–36
CrossRef Google scholar

Acknowledgments

This work was financially supported by the Science Foundation for Distinguished Youth of Shaanxi Province (2020JC-31), the National Natural Science Foundation of China (41977031), CAS “Light of West China” Program (XAB2016A03) and Program of State Key Laboratory of Loess and Quaternary Geology CAS (SKLLQGZR1803).

Declaration of competing 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.

RIGHTS & PERMISSIONS

2021 Higher Education Press
AI Summary AI Mindmap
PDF(982 KB)

Accesses

Citations

Detail

Sections
Recommended

/