Abstract
Recovery of belowground microbial biodiversity is important for soil restoration after mining exploitation. We aimed to compare microbial communities of a mine rehabilitation site to those with native vegetation. Community structure and metabolic potential of soil microbial communities were analyzed in an inactive open-pit coal mine located in northeastern Colombia using GeoChip and high-throughput sequencing techniques. Sites included (1) a spoil dump closed in 2010 with a mix of mesquite trees and native vegetation, and (2) a native dry forest next to the mining area. Most samples had an alkaline pH, high sulfur, zinc, and magnesium contents, and high cation exchange capacity as well as low calcium content. A total of 61,384 bacterial amplicon sequence variants (ASVs) and 402 Eukarya ASVs were obtained. Overall, the most abundant bacterial/archaeal phyla (0.1%) were Acidobacteria, Actinobacteria, Bacteroidetes, and Chlorolexi. The fungal genus Cladosporium dominated all treatments, while Volutella was observed only in the inactive dump. Bacterial alpha diversity was surprisingly higher in the inactive spoil dump than in the forest, while fungal alpha diversity was similar between that treatment and the native dry forest. Fungal genera might be more sensitive to the different treatments, as their abundances were highly influenced by their location compared to bacterial genera. There were no significant differences regarding the metabolic potential of bacterial communities. The GeoChip 5.0S analysis showed that the native dry forest had a higher number of genes related to C, N, P, and Z cycles, metal homeostasis, and organic remediation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agencia Nacional de Mineria (2017) Producción de carbón en ascenso. Available via ANM. https://www.anm.gov.co/?q=produccion_de_carbon_en_ascenso_boletin_prensa. Accessed June 2017
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075
Andrés P, Mateos E (2006) Soil mesofaunal responses to post-mining restoration treatments. Appl Soil Ecol 33:67–78. https://doi.org/10.1016/j.apsoil.2005.08.007
Benidire L, Pereira SI, Naylo A, Castro PM, Boularbah A (2020) Do metal contamination and plant species affect microbial abundance and bacterial diversity in the rhizosphere of metallophytes growing in mining areas in a semiarid climate? J Soils Sediments 20:1003–1017. https://doi.org/10.1007/s11368-019-02475-4
Betancur EO, Escobar JMM (2013) Legislación Colombiana de Cierre de Minas. ¿Es realmente necesaria? Boletín De Ciencias De La Tierra 34:51–64
Bhattacharyya P, Chakrabarti K, Chakraborty A (2003) Effect of MSW compost on microbiological and biochemical soil quality indicators. Compost Sci Util 11:220–227. https://doi.org/10.1080/1065657X.2003.10702130
Bouyoucos GJ (1936) Directions for making mechanical analysis of soils by the hydrometer method. Soil Sci 4:225–228. https://doi.org/10.1097/00010694-193609000-00007
Bundy JG, Davey MP, Viant MR (2009) Environmental metabolomics: a critical review and future perspectives. Metabolomics 5:3. https://doi.org/10.1007/s11306-008-0152-0
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Delgado-Baquerizo M, Oliverio AM, Brewer TE et al (2018) A global atlas of the dominant bacteria found in soil. Science 359:320–325. https://doi.org/10.1126/science.aap9516
Díaz LC, Arranz JC, Mesa G (2013) Caracterización físico-química y mineralógica de suelos en zona carbonífera del Cesar Colombia. Interciencia 38:42–47
Dolgopolova A, Weiss DJ, Seltmann R, Stanley C, Coles B, Cheburkin AK (2004) Closed-vessel microwave digestion technique for lichens and leaves prior to determination of trace elements (Pb, Zn, Cu) and stable Pb isotope ratios. Int J Environ Anal Chem 84:889–899. https://doi.org/10.1080/03067310410001729006
Doong RA, Lei WG (2003) Solubilization and mineralization of polycyclic aromatic hydrocarbons by Pseudomonas putida in the presence of surfactant. J Hazard Mater 96:15–27. https://doi.org/10.1016/s0304-3894(02)00167-x
Douglas GM, Maffei VJ, Zaneveld JR et al (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688. https://doi.org/10.1038/s41587-020-0548-6
El Baz S, Baz M, Barakate M, Hassani L, El Gharmali A, Imziln B (2015) Resistance to and accumulation of heavy metals by actinobacteria isolated from abandoned mining areas. Sci World J 2015:761834. https://doi.org/10.1155/2015/761834
Fanning DS, Fanning MCB (1989) Soil morphology, genesis, and classification. John Wiley and Sons Inc.
Fierer N, Ladau J (2012) Predicting microbial distributions in space and time. Nat Methods 9:549–551. https://doi.org/10.1038/nmeth.2041
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks CA
Gil-Martínez M, López-García Á, Domínguez MT, Kjøller R, Navarro-Fernández CM, Rosendahl S, Marañón T (2021) Soil fungal diversity and functionality are driven by plant species used in phytoremediation. Soil Biol Biochem 153:108102. https://doi.org/10.1016/j.soilbio.2020.108102
Glöckner FO, Yilmaz P, Quast C, Gerken J, Beccati A, Ciuprina A, Bruns G, Yarza P, Peplies J, Westram R, Ludwig W (2017) 25 years of serving the community with ribosomal RNA gene reference databases and tools. J Biotechnol 261:169–176. https://doi.org/10.1016/j.jbiotec.2017.06.1198
Gomez E, Garland J, Conti M (2004) Reproducibility in the response of soil bacterial community-level physiological profiles from a land use intensification gradient. Appl Soil Ecol 26:21–30. https://doi.org/10.1016/j.apsoil.2003.10.007
Gómez-Sagasti MT, Alkorta I, Becerril JM et al (2012) Microbial monitoring of the recovery of soil quality during heavy metal phytoremediation. Water Air Soil Pollut 223:3249–3262. https://doi.org/10.1007/s11270-012-1106-8
Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129. https://doi.org/10.1111/j.1574-6976.2012.00343.x
Guebert MD, Gardner TW (2001) Macropore flow on a reclaimed surface mine: infiltration and hillslope hydrology. Geomorphology 39:151–169. https://doi.org/10.1016/S0169-555X(00)00107-0
Guerra CA, Heintz-Buschart A, Sikorski J, Chatzinotas A et al (2020) Blind spots in global soil biodiversity and ecosystem function research. Nat Commun 11:3870. https://doi.org/10.1038/s41467-020-17688-2
Guerra CA, Bardgett RD, Caon L, Crowther TW et al (2021) Tracking, targeting, and conserving soil biodiversity. Science 371:239–241. https://doi.org/10.1126/science.abd7926
Gundlapally SR, Garcia-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol 52:345–357. https://doi.org/10.1007/s00248-006-9011-6
Guo Y, Chen J, Tsolmon B, He A, Guo J, Yang J, Bao Y (2020) Effects of subsidence and transplanted trees on soil arbuscular mycorrhizal fungal diversity in a coal mining area of the Loess Plateau. Glob Ecol Conserv 24:e01308. https://doi.org/10.1016/j.gecco.2020.e01308
Hall EK, Bernhardt ES, Bier RL, Bradford MA et al (2018) Understanding how microbiomes influence the systems they inhabit. Nat Microbiol 3:977–982. https://doi.org/10.1038/s41564-018-0201-z
He ZL, Deng Y, Van Nostrand JD, Tu QC et al (2010) GeoChip 3.0 as a high throughput tool for analyzing microbial community composition, structure and functional activity. ISME J 4:1167–1179. https://doi.org/10.1038/ismej.2010.46
Holguin G (2011) Contexto minero en el departamento del Cesar. Estado actual y proyecciones, Bogotá, p 10
Instituto Colombiano de Normas Técnicas y Certificación – ICONTEC (2007) Norma técnica colombiana NTC 5526. Calidad de suelo. Determinación de micronutrientes disponibles: cobre, zinc, hierro y manganeso. Bogotá. 8
Instituto Colombiano de Normas Técnicas y Certificación - ICONTEC (2008) Norma técnica colombiana NTC 5596. Calidad de suelo. Determinación de la conductividad electrica. Bogotá. 10
Instituto Colombiano de Normas Técnicas y Certificación – ICONTEC (2020) Norma técnica colombiana NTC 5350: Calidad del suelo determinación de fósforo disponible. Segunda actualización. Bogotá. 18
Instituto Colombiano de Normas Técnicas y Certificación - ICONTEC (2016) Norma técnica colombiana NTC 5349. Calidad de suelo. Determinación de las bases cambiables: Método del acetato amonio 1M y pH 7,0. Segunda actualización. Bogotá. 9 p.
Iram S, Ahmad I, Stuben D (2009) Analysis of mines and contaminated agricultural soil samples for fungal diversity and tolerance to heavy metals. Pak J Bot 41:885–895
Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil Acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453. https://doi.org/10.1038/ismej.2008.127
Kampf N, Schneider P, Giasson E (1997) Properties: pedogenesis and classification of constructed soils in coal mining areas of the Baixo Jacuí region in Southern Brazil. Braz J Soil Sci 21:9–88
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462. https://doi.org/10.1093/nar/gkv1070
Kishimoto N, Kosako Y, Tano T (1991) Acidobacterium capsulatum gen. nov., sp. nov.: an acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment. Curr Microbiol 22:1–7. https://doi.org/10.1007/BF02106205
Kneller T, Harris RJ, Bateman A, Muñoz-Rojas M (2018) Native-plant amendments and topsoil addition enhance soil function in post-mining arid grasslands. Sci Total Environ 621:744–752. https://doi.org/10.1016/j.scitotenv.2017.11.219
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. https://doi.org/10.1128/AEM.00335-09
Li Y, Chen L, Wen H, Zhou T, Zhang T, Gao X (2014) 454 Pyrosequencing analysis of bacterial diversity revealed by a comparative study of soils from mining subsidence and reclamation areas. J Microbiol Biotech 24:313–323. https://doi.org/10.4014/jmb.1309.09001
Lladó S, Žifčáková L, Větrovský T, Eichlerová I, Baldrian P (2016) Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biol Fertil Soils 52:251–260. https://doi.org/10.1007/s00374-015-1072-6
Louca S, Doebeli M, Parfrey LW (2018) Correcting for 16S rRNA gene copy numbers in microbiome surveys remains an unsolved problem. Microbiome 6:41. https://doi.org/10.1186/s40168-018-0420-9
Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585. https://doi.org/10.1128/AEM.01996-06
Lu ZM, Deng Y, van Nostrand JD et al (2012) Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume. ISME J 6:451–460. https://doi.org/10.1038/ismej.2011.91
Madej G, Barczyk G, Gdawiec M (2011) Evaluation of soil biological quality index (QBS-ar): its sensitivity and usefulness in the post-mining chronosequence - preliminary research. Pol J Environ Stud 20(5):1367–1372
Maiti SK (2013). Introduction. In: Ecorestoration of the coalmine degraded lands. Springer, India. https://doi.org/10.1007/978-81-322-0851-8_1
Marín C, Kohout P (2021) Response of soil fungal ecological guilds to global changes. New Phytol 229:656–658. https://doi.org/10.1111/nph.17054
McGuire KL, Treseder KK (2010) Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem 42:529–535. https://doi.org/10.1016/j.soilbio.2009.11.016
McMurdie PJ, Holmes S (2012) Phyloseq: a bioconductor package for handling and analysis of high-throughput phylogenetic sequence data. In Biocomputing 2012 (235–246). https://doi.org/10.1142/9789814366496_0023
Mishra A, Nautiyal CS (2009) Functional diversity of the microbial community in the rhizosphere of chickpea grown in diesel fuel-spiked soil amended with Trichoderma ressei using sole-carbon-source utilization profiles. World J Microbiol Biotechnol 25:1175–1180. https://doi.org/10.1007/s11274-009-9998-1
Moquin SA, Garcia JR, Brantley SL, Takacs-Vesbach CD, Shepherd UL (2012) Bacterial diversity of bryophyte-dominant biological soil crusts and associated mites. J Arid Environ 87:110–117. https://doi.org/10.1016/j.jaridenv.2012.05.004
Mota EA, Felestrino ÉB, Leão VA, Guerra-Sá R (2020) Manganese (II) removal from aqueous solutions by Cladosporium halotolerans and Hypocrea jecorina. Biotechn Rep 25:e00431. https://doi.org/10.1016/j.btre.2020.e00431
Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. p. 539–579. In: Page AL et al (eds) Methods of soil analysis: Part 2. Chemical and microbiological properties. ASA Monograph Number 9. https://doi.org/10.2134/agronmonogr9.2.2ed.c29
Nilsson RH, Larsson K-H, Taylor AFS, Bengtsson-Palme J et al (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264. https://doi.org/10.1093/nar/gky1022
Oksanen J, Blanchet FG, Kindt R, Legendre P et al (2010) Vegan: community ecology package. R package version 1.17–4. http://cran. r-project.org
Ouanphanivanh N, Illyes Z, Merenyi Z, Orczan AK, Szigeti Z, Bratek Z (2013) Mycorrhizal fungi and endophytes of orchids living in three Hungarian abandoned mines. Sydowia 65:245–266
Peng M, Zi X, Wang Q (2015) Bacterial community diversity of oil contaminated soils assessed by high throughput sequencing of 16S rRNA genes. Int J Environ Res Public Health 12:12002–12015. https://doi.org/10.3390/ijerph121012002
Radeva G, Kenarova A, Bachvarova V, Flemming K, Popov I, Vassilev D, Selenska-Pobell S (2013) Bacterial diversity at abandoned uranium mining and milling sites in Bulgaria as revealed by 16S rRNA genetic diversity study. Water Air Soil Pollut 224:1–14. https://doi.org/10.1007/s11270-013-1748-1
Ranjard L, Lejon DPH, Mougel C, Schehrer L, Merdinoglu D, Chaussod R (2003) Sampling strategy in molecular microbial ecology: influence of soil sample size on DNA fingerprinting analysis of fungal and bacterial communities. Environ Microbiol 5:1111–1120. https://doi.org/10.1046/j.1462-2920.2003.00521.x
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
RStudio Team (2021) RStudio: integrated development environment for R. RStudio, PBC, Boston. URL: http://www.rstudio.com/. Accessed 2021
Rutgers M, Wouterse M, Drost SM, Breure AM, Mulder C, Stone D et al (2016) Monitoring soil bacteria with community-level physiological profiles using BiologTM ECO-plates in the Netherlands and Europe. Appl Soil Ecol 97:23–35. https://doi.org/10.1016/j.apsoil.2015.06.007
Sait M, Davis KE, Janssen PH (2006) Effect of pH on isolation and distribution of members of subdivision 1 of the phylum Acidobacteria occurring in soil. Appl Environ Microbiol 72:1852–1857. https://doi.org/10.1128/AEM.72.3.1852-1857.2006
Sevigny JL, Rothenheber D, Diaz KS, Zhang Y, Agustsson K, Bergeron RD, Thomas WK (2019) Marker genes as predictors of shared genomic function. BMC Genomics 20:268. https://doi.org/10.1186/s12864-019-5641-1
Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H et al (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:1–19. https://doi.org/10.3389/fmicb.2012.00417
Shao Z, Sun F (2007) Intracellular sequestration of manganese and phosphorus in a metal-resistant fungus Cladosporium cladosporioides from deep-sea sediment. Extremophiles 11:435–443. https://doi.org/10.1007/s00792-006-0051-0
Singh AN, Singh JS (2006) Experiments on ecological restoration of coal mine spoil using native trees in a dry tropical environment, India: a synthesis. New for 31:25–39. https://doi.org/10.1007/s11056-004-6795-4
Talbot NJ, Coddington A, Roberts IN, Oliver RP (1988) Diploid construction by protoplast fusion in Fulvia fulva (syn. Cladosporium fulvum): genetic analysis of an imperfect fungal plant pathogen. Curr Genet 14:567–572. https://doi.org/10.1007/BF00434082
Taleski V, Dimkić I, Boev B, Boev I, Živković S, Stanković S (2020) Bacterial and fungal diversity in the lorandite (TlAsS2) mine Allcharin the Republic of North Macedonia. FEMS Microbiol Ecol 96(9):fiaa155. https://doi.org/10.1093/femsec/fiaa155
Tardy V, Mathieu O, Lévêque J, Terrat S, Chabbi A, Lemanceau P, Ranjard L, Maron PA (2014) Stability of soil microbial structure and activity depends on microbial diversity. Environ Microbiol Rep 6:173–183. https://doi.org/10.1111/1758-2229.12126
Tu Q, Yu H, He Z, Deng Y, Wu L, Van Nostrand JD, Zhou A, Voordeckers J, Lee Y-J, Qin Y et al (2014) GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis. Mol Ecol Resour 14:914–928. https://doi.org/10.1111/1755-0998.12239
Ugland KI, Gray JS, Ellingsen KE (2003) The species–accumulation curve and estimation of species richness. J of Anim Ecol 72(5):888–897. https://doi.org/10.1046/j.1365-2656.2003.00748.x
Unidad de Planeación Minero-Energética - UPME (2016) Boletín Estadístico de Minas y energía 2012 – 2016. Ministerio de Minas y Energía. Available via http://www1.upme.gov.co/simco/Documents/Boletin_Estadistico_2012_2016.pdf. Accessed December 2016
Vahter T, Bueno CG, Davison J, Herodes K, Hiiesalu I, Kasari-Toussaint L et al (2020) Co-introduction of native mycorrhizal fungi and plant seeds accelerates restoration of post-mining landscapes. J of Appl Ecol 57(9):1741–1751. https://doi.org/10.1111/1365-2664.13663
Vargas C (2011) Caracterización florística y fitogeográfica del sector sur de la serranía de Perijá y áreas adyacentes de la cordillera oriental colombiana. Tesis de Maestría. Universidad Nacional de Colombia. Available via http://www.bdigital.unal.edu.co/5239/1/carlosalbertovargasrincon.2011.pdf. Accessed January 2017
Vazquez S, Nogales B, Ruberto L, Mestre C, Christie-Oleza J, Ferrero M et al (2013) Characterization of bacterial consortia from diesel-contaminated Antarctic soils: towards the design of tailored formulas for bioaugmentation. Int Biodeterior & Biodegrad 77:22–30. https://doi.org/10.1016/j.ibiod.2012.11.002
Wei SHI, Xue-na ZHANG, Hai-bin JIA, Sheng-dong FENG, Zhi-xin YANG, Ou-ya ZHAO, Yu-ling LI (2017) Effective remediation of aged HMW-PAHs polluted agricultural soil by the combination of Fusarium sp. and smooth bromegrass (Bromus inermis Leyss.). J of Integr Agric 16.1:199–209 ISSN 2095–3119. https://doi.org/10.1016/S2095-3119(16)61373-4.
Wrighton KC, Thomas BC, Sharon I, Miller CS et al (2012) Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337:1661–1665. https://doi.org/10.1126/science.1224041
Xu X, Wang N, Lipson D, Sinsabaugh R, Schimel J, He L et al (2020) Microbial macroecology: in search of mechanisms governing microbial biogeographic patterns. Global Ecol Biogeogr 29:1870–1886. https://doi.org/10.1111/geb.13162
Zhang X, Lin L, Chen M, Zhu Z, Yang W, Chen B et al (2012) A nonpathogenic Fusarium oxysporum strain enhances phytoextraction of heavy metals by the hyperaccumulator Sedum alfredii Hance. J of Hazard Mater 229:361–370. https://doi.org/10.1016/j.jhazmat.2012.06.013
Zhao OY, Zhang XN, Feng SD, Zhang LX, Shi W, Yang ZX et al (2017) Starch-enhanced degradation of HMW PAHs by Fusarium sp. in an aged, polluted soil from a coal mining area. Chemosphere 174:774–780. https://doi.org/10.1016/j.chemosphere.2016.12.026
Acknowledgements
We thank Luciano Levin, Luciano Merini, Elka Arzuza, Rafael Arango, and Pablo Patiño, and coal mine employees who prefer to be anonymous for their administrative and logistics support during the development of this study.
Funding
This work was possible due to the financial aid for research of “Fondo Regional de Tecnologia Agropecuaria FONTAGRO FTG-5021/16” that supported the work of T. A. C. M. was supported by “Convocatoria Nacional Subvención a Instalación Academia Convocatoria Año 2021 + Folio SA77210019 (ANID—Chile).”
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Arcila-Galvis, J.E., Marín, C., Ortega-Cuadros, M. et al. A Metagenomic Assessment of Soil Microbial Communities in a Coal Mine Spoil Dump Under Reclaimed Vegetation in La Guajira, Colombia. J Soil Sci Plant Nutr 22, 4377–4390 (2022). https://doi.org/10.1007/s42729-022-01036-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-022-01036-y