Abstract
Soils are impacted globally by several anthropogenic factors, including chemical pollutants. Among those, perfluoroalkyl and polyfluoroalkyl substances (PFAS) are of concern due to their high environmental persistence, and as they might affect soil structure and function. However, data on impacts of PFAS on soil structure and microbially-driven processes are currently lacking. This study explored the effects of perfluorooctanesulfonic acid (PFOS), perfluorooctanoic acid (PFOA) and perfluorobutanesulfonic acid (PFBS) at environmental-relevant concentrations on soil health, using a 6-week microcosm experiment. PFAS (even at 0.5 ng g−1 for PFBS) significantly increased litter decomposition, associated with positive effects on β-glucosidase activities. This effect increased with PFAS concentrations. Soil pH was significantly increased, likely as a direct consequence of increased litter decomposition affected by PFAS. Soil respiration was significantly inhibited by PFAS in week 3, while this effect was more variable in week 6. Water-stable aggregates were negatively affected by PFOS, possibly related to microbial shifts. PFAS affected soil bacterial and fungal abundance, but not microbial and certain enzyme activities. Our work highlights the potential effects of PFAS on soil health, and we argue that this substance class could be a factor of environmental change of potentially broad relevance in terrestrial ecosystem functioning.
Availability of data and material
All data used for analyses and plotting are available online and can be accessed at https://doi.org/10.6084/m9.figshare.19772860.v1.
Change history
28 September 2022
Funding note is missing during initial upload.
References
Ahmed, M.B., Johir, M.A.H., McLaughlan, R., Nguyen, L.N., Xu, B., Nghiem, L.D., 2020. Per- and polyfluoroalkyl substances in soil and sediments: Occurrence, fate, remediation and future outlook. Science of the Total Environment 748, 141251.
Beans, C., 2021. News Feature: How “forever chemicals” might impair the immune system. Proceedings of the National Academy of Sciences 118, e2105018118.
Berg, B., McClaugherty, C., 2014. Plant Litter. Springer Berlin Heidelberg.
Brusseau, M.L., Anderson, R.H., Guo, B., 2020. PFAS concentrations in soils: Background levels versus contaminated sites. Science of the Total Environment 740, 140017.
Buck, R.C., Franklin, J., Berger, U., Conder, J.M., Cousins, I.T., de Voogt, P., Jensen, A.A., Kannan, K., Mabury, S.A., van Leeuwen, S.P., 2011. Perfluoroalkyl and polyfluoroalkyl substances in the environment: Terminology, classification, and origins. Integrated Environmental Assessment and Management 7, 513–541.
Cai, Y., Chen, H., Yuan, R., Wang, F., Chen, Z., Zhou, B., 2019. Toxicity of perfluorinated compounds to soil microbial activity: Effect of carbon chain length, functional group and soil properties. Science of the Total Environment 690, 1162–1169.
Cai, Y., Chen, H., Yuan, R., Wang, F., Chen, Z., Zhou, B., 2020. Metagenomic analysis of soil microbial community under PFOA and PFOS stress. Environmental Research 188, 109838.
Cai, Y., Wang, Q., Zhou, B., Yuan, R., Wang, F., Chen, Z., Chen, H., 2021. A review of responses of terrestrial organisms to perfluorinated compounds. Science of the Total Environment 793, 148565.
Chen, H., Wang, Q., Cai, Y., Yuan, R., Wang, F., Zhou, B., Chen, Z., 2020. Effect of per fl uorooctanoic acid on microbial activity in wheat soil under different fertilization conditions. Environmental Pollution 264, 114784.
Dieleman, C.M., Lindo, Z., McLaughlin, J.W., Craig, A.E., Branfireun, B.A., 2016. Climate change effects on peatland decomposition and porewater dissolved organic carbon biogeochemistry. Biogeochemistry 128, 385–396.
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 and Biochemistry 43, 1387–1397.
He, W., Megharaj, M., Naidu, R., 2016. Toxicity of perfluorooctanoic acid towards earthworm and enzymatic activities in soil. Environmental Monitoring and Assessment 188, 424.
Ho, J., Tumkaya, T., Aryal, S., Choi, H., Claridge-Chang, A., 2019. Moving beyond P values: data analysis with estimation graphics. Nature Methods 16, 565–566.
Hothorn, T., Bretz, F., Westfall, P., 2008. Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.
IUSS Working Group WRB, 2015. World reference base for soil resources 2014 International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports 106. Rome. https://www.fao.org/3/i3794en/I3794en.pdf.
Jin, H., Zhang, Y., Zhu, L., Martin, J.W., 2015. Isomer profiles of perfluoroalkyl substances in water and soil surrounding a chinese fluorochemical manufacturing park. Environmental Science & Technology 49, 4946–4954.
Kemper, W.D., Rosenau, R.C. 1986. Aggregate Stability and Size Dlstributlon. In: Klute, A., ed. Methods of Soil Analysis: Part 1 Physical and Mineralogical Methods. American Society of Agronomy, Inc., Soil Science Society of America, Inc. Madison, Wisconsin USA.
Lehmann, A., Leifheit, E.F., Feng, L., Bergmann, J., Wulf, A., Rillig, M.C., 2020. Microplastic fiber and drought effects on plants and soil are only slightly modified by arbuscular mycorrhizal fungi. Soil Ecology Letters 4, 32–44.
Lehmann, A., Zheng, W. & Rillig, M.C., 2017. Soil biota contributions to soil aggregation. Nature Ecology and Evolution 1, 1828–1835.
Liang, Y., Lehmann, A., Ballhausen, M.B., Muller, L., Rillig, M.C., 2019. Increasing temperature and microplastic fibers jointly influence soil aggregation by saprobic fungi. Frontiers in Microbiology 10, 1–10.
Lim, X., 2019. Tainted water: the scientists tracing thousands of fluorinated chemicals in our environment. Nature 566, 26–29.
Liu, C.M., Kachur, S., Dwan, M.G., Abraham, A.G., Aziz, M., Hsueh, P.R., Huang, Y.T., Busch, J.D., Lamit, L.J., Gehring, C.A., Keim, P., Price, L.B., 2012. FungiQuant: A broad-coverage fungal quantitative real-time PCR assay. BMC Microbiology 12, 255.
Lynch, J.M., Bragg, E., 1985. Microorganisms and soil aggregate stabililty. Advances in Soil Science 2, 133–171.
Ma, D., Zhong, H., Lv, J., Wang, Y., Jiang, G., 2022. Levels, distributions, and sources of legacy and novel per- and perfluoroalkyl substances (PFAS) in the topsoil of Tianjin, China. Journal of Environmental Sciences (China) 112, 71–81.
Milinovic, J., Lacorte, S., Vidal, M., Rigol, A., 2015. Sorption behaviour of perfluoroalkyl substances in soils. Science of the Total Environment 511, 63–71.
Morgado, R.G., Loureiro, S., González-Alcaraz, M.N., 2018. Changes in soil ecosystem structure and functions due to soil contamination. Soil Pollution: From monitoring to Remediation. Academic Press, Pittsburgh. pp. 59–87.
Muff, S., Nilsen, E.B., O’Hara, R.B., Nater, C.R., 2022. Rewriting results sections in the language of evidence. Trends in Ecology & Evolution 37, 203–210.
Qiao, W., Xie, Z., Zhang, Y., Liu, X., Xie, S., Huang, J., Yu, L., 2018. Perfluoroalkyl substances (PFASs) influence the structure and function of soil bacterial community: Greenhouse experiment. Science of the Total Environment 642, 1118–1126.
R Core Team, 2020. R: A Language and Environment for Statistical Computing. https://www.r-project.org/.
Rillig, M.C., Mardatin, N.F., Leifheit, E.F., Antunes, P.M., 2010. Mycelium of arbuscular mycorrhizal fungi increases soil water repellency and is sufficient to maintain water-stable soil aggregates. Soil Biology & Biochemistry 42, 1189–1191.
Rillig, M.C., Ryo, M., Lehmann, A., 2021. Classifying human influences on terrestrial ecosystems. Global Change Biology 27, 2273–2278.
Rillig, M.C., Ryo, M., Lehmann, A., Aguilar-Trigueros, C.A., Buchert, S., Wulf, A., Iwasaki, A., Roy, J., Yang, G., 2019. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366, 886–890.
Rousk, J., Brookes, P.C., Bååth, E., 2010. Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil. Soil Biology and Biochemistry 42, 926–934.
Sokol, N.W., Slessarev, E., Marschmann, G.L., Nicolas, A., Blazewicz, S.J., Brodie, E.L., Firestone, M.K., Foley, M.M., Hestrin, R., Hungate, B.A., Koch, B.J., Stone, B.W., Sullivan, M.B., Zablocki, O., Trubl, G., McFarlane, K., Stuart, R., Nuccio, E., Weber, P., Jiao, Y., Zavarin, M., Kimbrel, J., Morrison, K., Adhikari, D., Bhattacharaya, A., Nico, P., Tang, J., Didonato, N., Paša-Tolic, L., Greenlon, A., Sieradzki, E.T., Dijkstra, P., Schwartz, E., Sachdeva, R., Banfield, J., Pett-Ridge, J., 2022. Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nature Reviews Microbiology, https://doi.org/10.1038/s41579-022-00695-z.
Sparling, G.P., McLay, C.D.A., Tang, C., Raphael, C., 1999. Effect of short-term legume residue decomposition on soil acidity. Soil Research 37, 561.
Tang, C., Yu, Q., 1999. Impact of chemical composition of legume residues and initial soil pH on pH change of a soil after residue incorporation. Plant and Soil 215, 29–38.
UNEP, 2019. Stockholm Convention on persistent organic pollutants (POPS) — Texts and Annexes. United Nations Environment Programme (UNEP).
Valentin, L., Nousiainen, A., Mikkonen, A., 2013. Introduction to Organic Contaminants in Soil: Concepts and Risks. In: Vicent, T., Caminal, G., Eljarrat, E., Barceló, D., eds. Emerging Organic Contaminants in Sludges. The Handbook of Environmental Chemistry. Springer, Berlin, Heidelberg. pp. 1–29.
Wang, C., Wang, F., Zhang, Q., Liang, W., 2016. Individual and combined effects of tebuconazole and carbendazim on soil microbial activity. European Journal of Soil Biology 72, 6–13.
Wei, T., Simko, V., 2017. R package “corrplot”: Visualization of a Correlation Matrix. https://github.com/taiyun/corrplot.
Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York.
Xiao, W., Ge, X., Zeng, L., Huang, Z., Lei, J., Zhou, B., Li, M., 2014. Rates of litter decomposition and soil respiration in relation to soil temperature and water in different-aged pinus massoniana forests in the Three Gorges Reservoir Area, China (D Hui, Ed). PLoS ONE 9, e101890.
Xiong, D., Li, Y., Xiong, Y., Li, X., Xiao, Y., Qin, Z., Xiao, Y., 2014. Influence of boscalid on the activities of soil enzymes and soil respiration. European Journal of Soil Biology 61, 1–5.
Xu, J.M., Tang, C., Chen, Z.L., 2006. The role of plant residues in pH change of acid soils differing in initial pH. Soil Biology and Biochemistry 38, 709–719.
Xu, R., Tao, W., Lin, H., Huang, D., Su, P., Gao, P., Sun, X., Yang, Z., Sun, W., 2022. Effects of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonic acid (PFOS) on soil microbial community. Microbial Ecology, 83, 929–941.
Zhang, B., Zhang, H., Jin, B., Tang, L., Yang, J., Li, B., Zhuang, G., Bai, Z., 2008. Effect of cypermethrin insecticide on the microbial community in cucumber phyllosphere. Journal of Environmental Sciences 20, 1356–1362.
Zhang, D.Q., Wang, M., He, Q., Niu, X. & Liang, Y., 2020. Distribution of perfluoroalkyl substances (PFASs) in aquatic plant-based systems: From soil adsorption and plant uptake to effects on microbial community. Environmental Pollution 257, 113575.
Zhang, W., Wang, J., Wang, J., Zhu, L., Lv, N., Wang, R., Ahmad, Z., 2019. New insights into dose- and time-dependent response of five typical PPCPs on soil microbial respiration. Bulletin of Environmental Contamination and Toxicology 103, 193–198.
Zhao, T., Lozano, Y.M., Rillig, M.C., 2021. Microplastics Increase Soil pH and decrease microbial activities as a function of microplastic shape, polymer type, and exposure time. Frontiers in Environmental Science 9, 1.
Zhu, Y.G., Penuelas, J., 2020. Changes in the environmental microbiome in the Anthropocene. Global Change Biology 26, 3175–3177.
Acknowledgements
B.X. thanks the China Scholarship Council and Deutscher Akademischer Austauschdienst (CSC-DAAD) for a postdoctoral scholarship. M.C.R. acknowledges support from an ERC Advanced Grant (694368). We thank Daniel Lammel, Yun Liang, Tingting Zhao, and Lili Rong for their help with experimental measurements. We thank Rosolino Ingraffia for providing soil samples.
Funding
Open Access funding enabled and organized by Projekt DEAL.
Author information
Authors and Affiliations
Contributions
B.X. and M.C.R. conceived the idea and designed experiments; B.X. conducted experiment and drafted the manuscript; G.Y assisted in measurements of soil function; A.L. assisted in data analysis and presentation; S.R. assisted in the determination of PFAS concentrations; All authors contributed to the final version of this manuscript.
Corresponding author
Ethics declarations
We declare that there is no conflict of interest.
Additional information
Highlights
• PFAS significantly increased litter decomposition and soil pH.
• Soil respiration was significantly inhibited by PFAS.
• Perfluorooctanesulfonic acid suppressed soil water-stable aggregates.
• Three PFAS exerted varying degrees of impact on soil health.
Supporting information (SI) for
Rights and permissions
Open access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Xu, B., Yang, G., Lehmann, A. et al. Effects of perfluoroalkyl and polyfluoroalkyl substances (PFAS) on soil structure and function. Soil Ecol. Lett. 5, 108–117 (2023). https://doi.org/10.1007/s42832-022-0143-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42832-022-0143-5
Keywords
- Litter decomposition
- Soil respiration
- Water-stable aggregates
- Soil microbial abundance
- Perfluorobutanesulfonic acid (PFBS)
- Perfluorooctanesulfonic acid (PFOS)