Abstract
Heavy metal contamination is a global environmental concern due to its persistence and toxicity. To explore soil microbial interaction mechanisms and their association with heavy metals on a Pb–Zn waste heap, ecological network analysis tools were used to analyze high-throughput data in microbiology. The microbial network was divided into several modules, but heavy metals were associated with specific modules. The heavy metal-tolerant module (M2) had a more negative than positive relationship with the heavy metal-mid-tolerant modules (M1 and M3). Tight coupling between fungal and bacterial operational taxonomic units (OTUs) within M2 was critical for module stability and heavy metal bioremediation. Additionally, members within M2 needed to form a positive relationship to cope with heavy metal contamination (As, Pb, Zn, Cu, and Cd). The study provides fundamental information for a deeper understanding of heavy metal bioremediation mechanisms in the Pb–Zn waste heap.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Beattie RE, Henke W, Campa MF, Hazen TC, McAliley LR, Campbell JH (2018) Variation in microbial community structure correlates with heavy-metal contamination in soils decades after mining ceased. Soil Biol Biochem 126:57–63. https://doi.org/10.1016/j.soilbio.2018.08.011
Becerra-Castro C, Monterroso C, Prieto-Fernández A, Rodríguez-Lamas L, Loureiro-Viñas M, Acea MJ, Kidd PS (2012) Pseudometallophytes colonising Pb/Zn mine tailings: a description of the plant-microorganism-rhizosphere soil system and isolation of metal-tolerant bacteria. J Hazard Mater 217:350–359. https://doi.org/10.1016/j.jhazmat.2012.03.039
Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45(3):198–207. https://doi.org/10.1006/eesa.1999.1860
Bourceret A, Cébron A, Tisserant E, Poupin P, Bauda P, Beguiristain T, Leyval C (2016) The bacterial and fungal diversity of an aged PAH- and heavy metal-contaminated soil is affected by plant cover and edaphic parameters. Microb Ecol 71(3):711–724. https://doi.org/10.1007/s00248-015-0682-8
Che R, Wang Y, Li K, Xu Z, Hu J, Wang F, Rui Y, Li L, Pang Z, Cui X (2019) Degraded patch formation significantly changed microbial community composition in alpine meadow soils. Soil Tillage Res 195:104426. https://doi.org/10.1016/j.still.2019.104426
Chen X, Zhao Y, Zhao X, Wu J, Zhu L, Zhang X, Wei Z, Liu Y, He P (2020) Selective pressures of heavy metals on microbial community determine microbial functional roles during composting: Sensitive, resistant and actor. J Hazard Mater 398:122858. https://doi.org/10.1016/j.jhazmat.2020.122858
Chun SJ, Kim YJ, Cui Y, Nam KH (2021) Ecological network analysis reveals distinctive microbial modules associated with heavy metal contamination of abandoned mine soils in Korea. Environ Pollut 289:117851. https://doi.org/10.1016/j.envpol.2021.117851
Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350(6261):663–666. https://doi.org/10.1126/science.aad2602
DalCorso G, Fasani E, Manara A, Visioli G, Furini A (2019) Heavy metal pollutions: state of the art and innovation in phytoremediation. Int J Mol Sci 20(14):3412. https://doi.org/10.3390/ijms20143412
de Vries FT, Griffiths RI, Bailey M, Craig H, Girlanda M, Gweon HS, Hallin S, Kaisermann A, Keith AM, Kretzschmar M, Lemanceau P (2018) Soil bacterial networks are less stable under drought than fungal networks. Nat Commun 9(1):1–12. https://doi.org/10.1038/s41467-018-05516-7
Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinform 13(1):1–20. https://doi.org/10.1186/1471-2105-13-113
Epelde L, Lanzen A, Blanco F, Urich T, Garbisu C (2014) Adaptation of soil microbial community structure and function to chronic metal contamination at an abandoned Pb-Zn mine. FEMS Microbiol Ecol 91(1):1–11. https://doi.org/10.1093/femsec/fiu007
Emenike CU, Jayanthi B, Agamuthu P, Fauziah SH (2018) Biotransformation and removal of heavy metals: a review of phytoremediation and microbial remediation assessment on contaminated soil. Environ Rev 26(2):156–168. https://doi.org/10.1139/er-2017-0045
Environmental Protecting Administration of China (1995) E. GB 15618–1995. Environment quality standard for soils; Environmental Protecting Administration of China, EPAC, Beijing, China
Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10(8):538–550. https://doi.org/10.1038/nrmicro2832
Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8(9):e1002687. https://doi.org/10.1371/journal.pcbi.1002687
Guo H, Nasir M, Lv J, Dai Y, Gao J (2017) Understanding the variation of microbial community in heavy metals contaminated soil using high throughput sequencing. Ecotoxicol Environ Saf 144:300–306. https://doi.org/10.1016/j.ecoenv.2017.06.048
Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47(6):453–467. https://doi.org/10.1002/jobm.200700275
Hemmat-Jou MH, Safari-Sinegani AA, Mirzaie-Asl A, Tahmourespour A (2018) Analysis of microbial communities in heavy metals-contaminated soils using the metagenomic approach. Ecotoxicology 27(9):1281–1291. https://doi.org/10.1007/s10646-018-1981-x
Hinojosa MB, Carreira JA, García-Ruíz R, Dick RP (2005) Microbial response to heavy metal–polluted soils. J Environ Qual 34(5):1789–1800. https://doi.org/10.2134/jeq2004.0470
Hou S, Zheng N, Tang L, Ji X, Li Y (2019) Effect of soil pH and organic matter content on heavy metals availability in maize (Zea mays L.) rhizospheric soil of non-ferrous metals smelting area. Environ Monit Assess 191(10):634. https://doi.org/10.1007/s10661-019-7793-5
Khan I, Awan SA, Rizwan M, Ali S, Hassan MJ, Brestic M, Zhang X, Huang L (2021) Effects of silicon on heavy metal uptake at the soil-plant interphase: a review. Ecotoxicol Environ Saf 222:112510. https://doi.org/10.1016/j.ecoenv.2021.112510
Kolde R (2018) Pretty Heatmaps: implementation of heatmaps that offers more control over dimensions and appearance. R package version 2.1.9. https://CRAN.R-project.org/package=pheatmap. Accessed 25 Oct 2021
Li MS (2006) Ecological restoration of mineland with particular reference to the metalliferous mine wasteland in China: a review of research and practice. Sci Total Environ 357(1–3):38–53. https://doi.org/10.1016/j.scitotenv.2005.05.003
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. Environ Pollut 231:908–917. https://doi.org/10.1016/j.envpol.2017.08.057
Li S, Wu J, Huo Y, Zhao X, Xue L (2021) Profiling multiple heavy metal contamination and bacterial communities surrounding an iron tailing pond in Northwest China. Sci Total Environ 752:141827. https://doi.org/10.1016/j.scitotenv.2020.141827
Luo Y, Wu Y, Qiu J, Wang H, Yang L (2019) Suitability of four woody plant species for the phytostabilization of a zinc smelting slag site after 5 years of assisted revegetation. J Soils Sediments 19(2):702–715. https://doi.org/10.1007/s11368-018-2082-4
Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27(2–3):313–339. https://doi.org/10.1016/S0168-6445(03)00048-2
Ojuederie OB, Babalola OO (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14(12):1504. https://doi.org/10.3390/ijerph14121504
Qurbani K, Hamzah H (2020) Intimate communication between Comamonas aquatica and Fusarium solani in remediation of heavy metal-polluted environments. Arch Microbiol 202(6):1397–1406
Rajkumar M, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3):142–149. https://doi.org/10.1016/j.tibtech.2009.12.002
Ranjard L, Lignier L, Chaussod R (2006) Cumulative effects of short-term polymetal contamination on soil bacterial community structure. Appl Environ Microbiol 72(2):1684–1687. https://doi.org/10.1128/AEM.72.2.1684-1687.2006
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 28 Oct 2021
Shen F, Li Y, Zhang M, Awasthi MK, Ali A, Li R, Wang Q, Zhang Z (2016) Atmospheric deposition-carried Zn and Cd from a zinc smelter and their effects on soil microflora as revealed by 16S rDNA. Sci Rep 6(1):39148. https://doi.org/10.1038/srep39148
Uehling JK, Entler MR, Meredith HR, Millet LJ, Timm CM, Aufrecht JA, Bonito GM, Engle NL, Labbé JL, Doktycz MJ, Retterer ST (2019) Microfluidics and metabolomics reveal symbiotic bacterial–fungal interactions between Mortierella elongata and Burkholderia include metabolite exchange. Front Microbiol. https://doi.org/10.3389/fmicb.2019.02163
Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21(12):1–20
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York
Yan J, Wang L, Hu Y, Tsang YF, Zhang Y, Wu J, Fu X, Sun Y (2018) Plant litter composition selects different soil microbial structures and in turn drives different litter decomposition pattern and soil carbon sequestration capability. Geoderma 319:194–203. https://doi.org/10.1016/j.geoderma.2018.01.009
Yang Y, Li S, Bi X, Wu P, Liu T, Li F, Liu C (2010) Lead, Zn, and Cd in slags, stream sediments, and soils in an abandoned Zn smelting region, southwest of China, and Pb and S isotopes as source tracers. J Soils Sediments 10(8):1527–1539. https://doi.org/10.1007/s11368-010-0253-z
Yang S, Cao J, Li F, Peng X, Peng Q, Yang Z, Chai L (2016) Field evaluation of the effectiveness of three industrial by-products as organic amendments for phytostabilization of a Pb/Zn mine tailings. Environ Sci: Processes Impacts 18(1):95–103. https://doi.org/10.1039/C5EM00471C
Zaefarian F, Rezvani M, Rejali F, Ardakani MR, Noormohammadi G (2011) Effect of heavy metals and arbuscular mycorrhizal fungal on growth and nutrients (N, P, K, Zn, Cu and Fe) accumulation of Alfalfa (Medicago sativa L.). Am Eurasian J Agric Environ Sci 11(3):346–352
Zhao X, Sun Y, Huang J, Wang H, Tang D (2020) Effects of soil heavy metal pollution on microbial activities and community diversity in different land use types in mining areas. Environ Sci Pollut Res 27(16):20215–20226. https://doi.org/10.1007/s11356-020-08538-1
Funding
This work was financially supported by the China Postdoctoral Science Foundation (2020M683373), Science and Technology Foundation of Guizhou Province, China ([2020]1Y192), National Natural Sciences Foundation of China (41967058), United Found of the Guizhou Province Government and the Natural Science Foundation of China (No. U1612442), High-Level Talent Training Program in Guizhou ([2016]5664).
Author information
Authors and Affiliations
Contributions
CS: writing original draft, formal analysis, data analysis. PW: resources, project administration, funding acquisition. GW: investigation, data curation; XK: visualization, writing-review review& editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sun, C., Wu, P., Wang, G. et al. Heavy Metals Contained Within a Pb–Zn Waste Heap Exhibit Selective Association with Microbial Modules as Revealed by Network Analysis. Bull Environ Contam Toxicol 109, 1067–1074 (2022). https://doi.org/10.1007/s00128-022-03499-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-022-03499-2