Linking microbial carbon pump capacity and efficacy to soil organic carbon storage and stability under heavy metal pollution

Xiao Liu, Xia Xu, Tian Ma, Shiwei Zhou, Xiaoli Bi, Hongbo He, Xudong Zhang, Weihuan Li

PDF(768 KB)
PDF(768 KB)
Soil Ecology Letters ›› 2023, Vol. 5 ›› Issue (2) : 220140. DOI: 10.1007/s42832-022-0140-8
RESEARCH ARTICLE
RESEARCH ARTICLE

Linking microbial carbon pump capacity and efficacy to soil organic carbon storage and stability under heavy metal pollution

Author information +
History +

Highlights

● SOC stocks and MCP capacity and efficacy decreased under medium and heavy pollution.

● The decrease in MCP capacity was tightly related to the decline in SOC storage.

● The lower MCP efficacy implied worse SOC stability under the heavier level.

Abstract

Heavy metal pollution can lead to a great loss of soil organic carbon (SOC). However, the microbial mechanisms that link heavy metal pollution to SOC remain poorly understood. Here, we investigated five apple-orchard soils at different distances from a Pb-Zn smelter. After assessing the heavy metal pollution level based on Grade II of the national soil environmental quality standard (China), we found SOC stocks and microbial carbon pump (MCP) capacity (i.e., microbial residue carbon) under medium and heavy pollution levels were significantly lower than those under safe, cordon and light pollution levels. The structural equation model showed causality in the SOC variations linked to pollution level through MCP capacity, which could contribute 77.8% of the variance in SOC storage. This verified MCP capacity can serve as a key parameter for evaluation of SOC storage under heavy metal pollution. Soil MCP efficacy, i.e., the proportion of microbial residue carbon to SOC, also decreased under medium and heavy pollution. This suggested that, with a heavier pollution level, there was a higher rate of reduction of microbial residue carbon in soil than the rate of reduction of SOC. As MCP efficacy can be a useful assessment of SOC stability, the significantly positive relationship between MCP efficacy and clay content in correlation analysis implied that lower MCP efficacy was correlated with SOC stability under the heavier pollution level. Our study provides valuable insights to identify the mechanisms of microbially mediated C transformation processes that are influenced by heavy metal pollution in agroecosystems.

Graphical abstract

Keywords

Microbial residues / Soil microbial carbon pump / Carbon sequestration / Heavy metals / Agricultural soil

Cite this article

Download citation ▾
Xiao Liu, Xia Xu, Tian Ma, Shiwei Zhou, Xiaoli Bi, Hongbo He, Xudong Zhang, Weihuan Li. Linking microbial carbon pump capacity and efficacy to soil organic carbon storage and stability under heavy metal pollution. Soil Ecology Letters, 2023, 5(2): 220140 https://doi.org/10.1007/s42832-022-0140-8

References

[1]
Aponte, H., Medina, J., Butler, B., Meier, S., Cornejo, P., Kuzyakov, Y., 2020. Soil quality indices for metal (loid) contamination: An enzymatic perspective. Land Degradation & Development31, 2700–2719.
CrossRef Google scholar
[2]
Bai, X.T., Wang, J., Dong, H., Chen, J.M., Ge, Y., 2021. Relative importance of soil properties and heavy metals/metalloids to modulate microbial community and activity at a smelting site. Journal of Soils and Sediments21, 1–12.
CrossRef Google scholar
[3]
Blagodatskaya, E., Kuzyakov, Y., 2013. Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biology & Biochemistry67, 192–211.
CrossRef Google scholar
[4]
Buckeridge, K.M., Mason, K.E., McNamara, N.P., Ostle, N., Puissant, J., Goodall, T., Griffiths, R.I., Stott, A.W., Whitaker, J., 2020. Environmental and microbial controls on microbial necromass recycling, an important precursor for soil carbon stabilization. Communications Earth and Environment1, 1–9.
CrossRef Google scholar
[5]
Cai, Y., Ma, T., Wang, Y., Jia, J., Jia, Y., Liang, C., Feng, X., 2022. Assessing the accumulation efficiency of various microbial carbon components in soils of different minerals. Geoderma407, 115562.
CrossRef Google scholar
[6]
Chenu, C., Angers, D.A., Barré, P., Derrien, D., Arrouays, D., Balesdent, J., 2019. Increasing organic stocks in agricultural soils: Knowledge gaps and potential innovations. Soil & Tillage Research188, 41–52.
CrossRef Google scholar
[7]
Chodak, M., Gołębiewski, M., Morawska-Płoskonka, J., Kuduk, K., Niklińska, M., 2013. Diversity of microorganisms from forest soils differently polluted with heavy metals. Applied Soil Ecology64, 7–14.
CrossRef Google scholar
[8]
Córdova, S.C., Olk, D.C., Dietzel, R.N., Mueller, K.E., Archontouilis, S.V., Castellano, M.J., 2018. Plant litter quality affects the accumulation rate, composition, and stability of mineral-associated soil organic matter. Soil Biology & Biochemistry125, 115–124.
CrossRef Google scholar
[9]
Dalal, R., 1998. Soil microbial biomass—what do the numbers really mean? Australian Journal of Experimental Agriculture 38, 649–665
[10]
Deng, F., Liang, C., 2022. Revisiting the quantitative contribution of microbial necromass to soil carbon pool: Stoichiometric control by microbes and soil. Soil Biology & Biochemistry165, 108486.
CrossRef Google scholar
[11]
Ding, X., Chen, S., Zhang, B., He, H., Filley, T.R., Horwath, W.R., 2020. Warming yields distinct accumulation patterns of microbial residues in dry and wet alpine grasslands on the Qinghai-Tibetan Plateau. Biology and Fertility of Soils56, 881–892.
CrossRef Google scholar
[12]
Engelking, B., Flessa, H., Joergensen, R.G., 2007. Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biology & Biochemistry39, 2111–2118.
CrossRef Google scholar
[13]
Fan, Z.S., Liang, C., 2015. Significance of microbial asynchronous anabolism to soil carbon dynamics driven by litter inputs. Scientific Reports5, 9575.
CrossRef Google scholar
[14]
Fu, C., Zhang, H., Tu, C., Li, L., Zhou, Q., Li, Y., Luo, Y., 2017. Spatial distribution and dynamics of soil organic carbon and total nitrogen in apple orchards in coastal regions. Acta Pedologica Sinica 55, 857–867 (in Chinese)
[15]
Huang, Y., Wang, L., Wang, W., Li, T., He, Z., Yang, X., 2019. Current status of agricultural soil pollution by heavy metals in China: A meta-analysis. Science of the Total Environment651, 3034–3042.
CrossRef Google scholar
[16]
Joergensen, R.G., 2018. Amino sugars as specific indices for fungal and bacterial residues in soil. Biology and Fertility of Soils54, 559–568.
CrossRef Google scholar
[17]
Lal, R., 2009. Challenges and opportunities in soil organic matter research. European Journal of Soil Science60, 158–169.
CrossRef Google scholar
[18]
Lehmann, J., Kinyangi, J., Solomon, D., 2007. Organic matter stabilization in soil microaggregates: implications from spatial heterogeneity of organic carbon contents and carbon forms. Biogeochemistry85, 45–57.
CrossRef Google scholar
[19]
Li, J., Xue, Q., Wang, P., Li, Z., 2015. Effect of lead (II) on the mechanical behavior and microstructure development of a Chinese clay. Applied Clay Science105–106, 192–199.
CrossRef Google scholar
[20]
Li, L., Wu, H., van Gestel, C.A.M., Peijnenburg, W.J.G.M., Allen, H.E., 2014. Soil acidification increases metal extractability and bioavailability in old orchard soils of Northeast Jiaodong Peninsula in China. Environmental Pollution188, 144–152.
CrossRef Google scholar
[21]
Liang, C., 2020. Soil microbial carbon pump: Mechanism and appraisal. Soil Ecology Letters2, 1–14.
CrossRef Google scholar
[22]
Liang, C., Amelung, W., Lehmann, J., Kästner, M., 2019. Quantitative assessment of microbial necromass contribution to soil organic matter. Global Change Biology25, 3578–3590.
CrossRef Google scholar
[23]
Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology2, 17105.
CrossRef Google scholar
[24]
Liu, Y.Z., Zhou, T., Crowley, D., Li, L.Q., Liu, D.W., Zheng, J.W., Yu, X.Y., Pan, G.X., Hussain, Q., Zhang, X.H., Zheng, J.F., 2012. Decline in topsoil microbial quotient, fungal abundance and C utilization efficiency of rice paddies under heavy metal pollution across South China. PLoS One7, e38858.
CrossRef Google scholar
[25]
Micó, C., Recatalá, L., Peris, M., Sánchez, J., 2006. Assessing heavy metal sources in agricultural soils of an European Mediterranean area by multivariate analysis. Chemosphere65, 863–872.
CrossRef Google scholar
[26]
Nemerow, N.L., 1974. Scientific Stream Pollution Analysis. Scripta Book Company, Washington DC
[27]
Nosrati, S.A., Negahdar, A., Negahdar, H., 2021. Stabilizing the clayey sand contaminated with heavy metals by zeolite and rice husk ash absorbents. Arabian Journal of Geosciences14, 1907.
CrossRef Google scholar
[28]
Nwachukwu, O., Pulford, I., 2011. Microbial respiration as an indication of metal toxicity in contaminated organic materials and soil. Journal of Hazardous Materials185, 1140–1147.
CrossRef Google scholar
[29]
Parmar, P., Kumari, N., Sharma, V., 2013. Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Botanical Studies54, 45.
CrossRef Google scholar
[30]
Schermelleh-Engel, K., Moosbrugger, H., Müller, H., 2003. Evaluating the fit of structural equation models: Tests of significance and descriptive goodness-of-fit measures. Methods of Psychological Research Online8, 23–74.
[31]
Schimel, J., Schaeffer, S., 2012. Microbial control over carbon cycling in soil. Frontiers in Microbiology3, 348.
CrossRef Google scholar
[32]
Shuaib, M., Azam, N., Bahadur, S., Romman, M., Yu, Q., Xuexiu, C., 2021. Variation and succession of microbial communities under the conditions of persistent heavy metal and their survival mechanism. Microbial Pathogenesis150, 104713.
CrossRef Google scholar
[33]
Sokol, N.W., Sanderman, J., Bradford, M.A., 2019. Pathways of mineral-associated soil organic matter formation: Integrating the role of plant carbon source, chemistry, and point of entry. Global Change Biology25, 12–24.
CrossRef Google scholar
[34]
Song, J., Shen, Q., Wang, L., Qiu, G., Shi, J., Xu, J., Brookes, P.C., Liu, X., 2018. Effects of Cd, Cu, Zn and their combined action on microbial biomass and bacterial community structure. Environmental Pollution243, 510–518.
CrossRef Google scholar
[35]
Wang, C., Qu, L., Yang, L., Liu, D., Morrissey, E., Miao, R., Liu, Z., Wang, Q., Fang, Y., Bai, E., 2021. Large-scale importance of microbial carbon use efficiency and necromass to soil organic carbon. Global Change Biology27, 2039–2048.
CrossRef Google scholar
[36]
Wang, C., Wang, X., Pei, G., Xia, Z., Peng, B., Sun, L., Wang, J., Gao, D., Chen, S., Liu, D., Dai, W., Jiang, P., Fang, Y., Liang, C., Wu, N., Bai, E., 2020. Stabilization of microbial residues in soil organic matter after two years of decomposition. Soil Biology & Biochemistry141, 107687.
CrossRef Google scholar
[37]
Xu, M., Cui, Y., Beiyuan, J., Wang, X., Duan, C., Fang, L., 2021. Heavy metal pollution increases soil microbial carbon limitation: Evidence from ecological enzyme stoichiometry. Soil Ecology Letters3, 230–241.
CrossRef Google scholar
[38]
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 International125, 478–488.
CrossRef Google scholar
[39]
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 Environment621, 148–159.
CrossRef Google scholar
[40]
Yang, Q., Li, Z., Lu, X., Duan, Q., Huang, L., Bi, J., 2018. A review of soil heavy metal pollution from industrial and agricultural regions in China: Pollution and risk assessment. Science of the Total Environment642, 690–700.
CrossRef Google scholar
[41]
Yantai Soil Census Office, 1985. Yantai Soil. Yantai Agricultural PressYantai.
[42]
Zhang, C., Nie, S., Liang, J., Zeng, G., Wu, H., Hua, S., Liu, J., Yuan, Y., Xiao, H., Deng, L., Xiang, H., 2016. Effects of heavy metals and soil physicochemical properties on wetland soil microbial biomass and bacterial community structure. Science of the Total Environment557–558, 785–790.
CrossRef Google scholar
[43]
Zhang, X., Amelung, W., 1996. Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biology & Biochemistry28, 1201–1206.
CrossRef Google scholar
[44]
Zhu, X., Jackson, R.D., DeLucia, E.H., Tiedje, J.M., Liang, C., 2020. The soil microbial carbon pump: From conceptual insights to empirical assessments. Global Change Biology26, 6032–6039.
CrossRef Google scholar

Acknowledgements

This work was supported by the Natural Science Foundation of Shandong Province (ZR2019PD022), the Central Public-interest Scientific Institution Basal Research Fund (FIRI20210401), the Major Scientific and Technological Innovation Projects of Key Research and Development Program in Shandong Province (2019JZZY010717).

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-022-0140-8 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2023 Higher Education Press
AI Summary AI Mindmap
PDF(768 KB)

Accesses

Citations

Detail

Sections
Recommended

/