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

Soil Ecology Letters ›› 2023, Vol. 5 ›› Issue (2) : 220140

PDF (768KB)
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 +
PDF (768KB)

Abstract

● 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.

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 DOI:10.1007/s42832-022-0140-8

登录浏览全文

4963

注册一个新账户 忘记密码

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.

[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.

[3]

Blagodatskaya, E., Kuzyakov, Y., 2013. Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biology & Biochemistry67, 192–211.

[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.

[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.

[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.

[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.

[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.

[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.

[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.

[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.

[13]

Fan, Z.S., Liang, C., 2015. Significance of microbial asynchronous anabolism to soil carbon dynamics driven by litter inputs. Scientific Reports5, 9575.

[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.

[16]

Joergensen, R.G., 2018. Amino sugars as specific indices for fungal and bacterial residues in soil. Biology and Fertility of Soils54, 559–568.

[17]

Lal, R., 2009. Challenges and opportunities in soil organic matter research. European Journal of Soil Science60, 158–169.

[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.

[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.

[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.

[21]

Liang, C., 2020. Soil microbial carbon pump: Mechanism and appraisal. Soil Ecology Letters2, 1–14.

[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.

[23]

Liang, C., Schimel, J.P., Jastrow, J.D., 2017. The importance of anabolism in microbial control over soil carbon storage. Nature Microbiology2, 17105.

[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.

[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.

[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.

[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.

[29]

Parmar, P., Kumari, N., Sharma, V., 2013. Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Botanical Studies54, 45.

[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.

[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.

[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.

[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.

[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.

[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.

[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.

[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.

[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.

[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.

[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.

[43]

Zhang, X., Amelung, W., 1996. Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biology & Biochemistry28, 1201–1206.

[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.

RIGHTS & PERMISSIONS

Higher Education Press

AI Summary AI Mindmap
PDF (768KB)

Supplementary files

Supporting Information

1121

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/