Contrasting soil fungal communities at different habitats in a revegetated copper mine wasteland
Jie-liang Liang, Jun Liu, Tao-tao Yang, Pan-deng Wang, Sheng-chang Zhang, Pu Jia, Bin Liao, Wen-sheng Shu, Jin-tian Li
Contrasting soil fungal communities at different habitats in a revegetated copper mine wasteland
Little is known about the responses of soil fungal communities to revegetation of mine wastelands, representing a major gap in the knowledge needed to improve the performances of revegetation schemes for mine wastelands. To shed some light on this matter, we re-established 4000 m2 of vegetation on an extremely acidic (pH 2.5) copper mine tailings pond and collected soil samples from three different types of habitats: amended layer of the reclaimed tailings (ALRT), unamended layer of the reclaimed tailings (ULRT), and unreclaimed tailings (UT). Soil fungal communities in the 120 samples collected in two consecutive years were characterized via high-throughput sequencing. The fungal diversities at ALRT and ULRT were found to be significantly higher than those at UT. Ascomycota whose relative abundance ranged from 74.5% to 98.4% was the most predominant phylum across all habitats, exhibiting the lowest predominance at ALRT. Two acidophilic fungal genera, Acidomyces and Acidiella, dominated UT with relative abundances being as high as 37.8% and 15.2%, respectively. In contrast, three genera with plant growth-promoting species (Talaromyces, Trichoderma and Penicillium) were abundant at ULRT and ALRT. Remarkably, their relative abundances at ULRT could be up to 29.0%, 26.9% and 9.7%, respectively. The three types of habitats differed considerably in the overall soil fungal community composition at species level, which became more pronounced as time progressed. The abovementioned differences between habitats in soil fungal community features were related to the reduced availability of soil copper and zinc. These results improved our understanding of fungal ecology of mine wastelands.
Extremely acidic / Fungal community structure / Mine soil / Next generation sequencing / Phytostabilization / Restoration
[1] |
Aguilera, A., Manrubia, S.C., Gómez, F., Rodríguez, N., Amils, R., 2006. Eukaryotic community distribution and its relationship to water physicochemical parameters in an extreme acidic environment, Rio Tinto (southwestern Spain). Applied and Environmental Microbiology 72, 5325–5330
CrossRef
Pubmed
Google scholar
|
[2] |
Ascher, J., Ceccherini, M.T., Landi, L., Mench, M., Pietramellara, G., Nannipieri, P., Renella, G., 2009. Composition, biomass and activity of microflora, and leaf yields and foliar elemental concentrations of lettuce, after in situ stabilization of an arsenic-contaminated soil. Applied Soil Ecology 41, 351–359
CrossRef
Google scholar
|
[3] |
Baker, B.J., Lutz, M.A., Dawson, S.C., Bond, P.L., Banfield, J.F., 2004. Metabolically active eukaryotic communities in extremely acidic mine drainage. Applied and Environmental Microbiology 70, 6264–6271
CrossRef
Pubmed
Google scholar
|
[4] |
Bendfeldt, E.S., Burger, J.A., Daniels, W.L., 2001. Quality of amended mine soils after sixteen years. Soil Science Society of America Journal 65, 1736–1744
CrossRef
Google scholar
|
[5] |
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. Microbial Ecology 71, 711–724
CrossRef
Pubmed
Google scholar
|
[6] |
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Turnbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336
CrossRef
Pubmed
Google scholar
|
[7] |
Clarke, K.R., Ainsworth, M., 1993. A method of linking multivariate community structure to environmental variables. Marine Ecology Progress Series 92, 205–219
CrossRef
Google scholar
|
[8] |
Cuadros-Orellana, S., Leite, L. R., Smith, A., Medeiros, J. D., Badotti, F., Fonseca, P. L., Vaz1, A. B. M., Oliveira, G., Góes-Neto, A., 2013. Assessment of fungal diversity in the environment using metagenomics: a decade in review. Fungal Genomics & Biology 3, 1–13.
|
[9] |
Davey, M.L., Heegaard, E., Halvorsen, R., Ohlson, M., Kauserud, H., 2012. Seasonal trends in the biomass and structure of bryophyte-associated fungal communities explored by 454 pyrosequencing. New Phytologist 195, 844–856
CrossRef
Pubmed
Google scholar
|
[10] |
de Goes, K.C.G.P., da Silva, J.J., Lovato, G.M., Iamanaka, B.T., Massi, F.P., Andrade, D.S., 2017. Talaromyces sayulitensis, Acidiella bohemica and Penicillium citrinum in Brazilian oil shale by-products. Antonie van Leeuwenhoek 110, 1637–1646
CrossRef
Pubmed
Google scholar
|
[11] |
Dos Santos, J.V., de Melo Rangel, W., Azarias Guimarães, A., Duque Jaramillo, P.M., Rufini, M., Marra, L.M., Varón López, M., Pereira da Silva, M.A., Fonsêca Sousa Soares, C.R., de Souza Moreira, F.M., 2013. Soil biological attributes in arsenic-contaminated gold mining sites after revegetation. Ecotoxicology (London, England) 22, 1526–1537
CrossRef
Pubmed
Google scholar
|
[12] |
Dudka, S., Adriano, D.C., 1997. Environmental impacts of metal ore mining and processing: a review. Journal of Environmental Quality 26, 590–602
CrossRef
Google scholar
|
[13] |
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 2194–2200
CrossRef
Pubmed
Google scholar
|
[14] |
Gastauer, M., Vera, M.P.O., de Souza, K.P., Pires, E.S., Alves, R., Caldeira, C.F., Ramos, S.J., Oliveira, G., 2019. A metagenomic survey of soil microbial communities along a rehabilitation chronosequence after iron ore mining. Scientific Data 6, 190008
CrossRef
Pubmed
Google scholar
|
[15] |
Goodwin, S., McPherson, J.D., McCombie, W.R., 2016. Coming of age: ten years of next-generation sequencing technologies. Nature Reviews. Genetics 17, 333–351
CrossRef
Pubmed
Google scholar
|
[16] |
Gordon, R.B., 2002. Production residues in copper technological cycles. Resources, Conservation and Recycling 36, 87–106
CrossRef
Google scholar
|
[17] |
Harman, G.E., Howell, C.R., Viterbo, A., Chet, I., Lorito, M., 2004. Trichoderma species--opportunistic, avirulent plant symbionts. Nature Reviews. Microbiology 2, 43–56
CrossRef
Pubmed
Google scholar
|
[18] |
Huang, L., Baumgartl, T., Mulligan, D., 2012. Is rhizosphere remediation sufficient for sustainable revegetation of mine tailings? Annals of Botany 110, 223–238
CrossRef
Pubmed
Google scholar
|
[19] |
Hujslová, M., Kubátová, A., Bukovská, P., Chudíčková, M., Kolařík, M., 2017. Extremely acidic soils are dominated by species-poor and highly specific fungal communities. Microbial Ecology 73, 321–337
CrossRef
Pubmed
Google scholar
|
[20] |
Hujslová, M., Kubátová, A., Kostovčík, M., Kolařík, M., 2013. Acidiella bohemica gen. et sp. nov. and Acidomyces spp. (Teratosphaeriaceae), the indigenous inhabitants of extremely acidic soils in Europe. Fungal Diversity 58, 33–45
CrossRef
Google scholar
|
[21] |
Jiujiang Statistical Bureau, 2018. Statistical Yearbook of Jiujiang – 2017. Jiujiang, China: Jiujiang Statistical Bureau.
|
[22] |
Johnson, D.B., 2003. Chemical and microbiological characteristics of mineral spoils and drainage waters at abandoned coal and metal mines. Water, Air, and Soil Pollution 3, 47–66
CrossRef
Google scholar
|
[23] |
Kardol, P., Wardle, D.A., 2010. How understanding aboveground-belowground linkages can assist restoration ecology. Trends in Ecology & Evolution 25, 670–679
CrossRef
Pubmed
Google scholar
|
[24] |
Kirk, J.L., Beaudette, L.A., Hart, M., Moutoglis, P., Klironomos, J.N., Lee, H., Trevors, J.T., 2004. Methods of studying soil microbial diversity. Journal of Microbiological Methods 58, 169–188
CrossRef
Pubmed
Google scholar
|
[25] |
Kohler, J., Caravaca, F., Azcón, R., Díaz, G., Roldán, A., 2016. Suitability of the microbial community composition and function in a semiarid mine soil for assessing phytomanagement practices based on mycorrhizal inoculation and amendment addition. Journal of Environmental Management 169, 236–246
CrossRef
Pubmed
Google scholar
|
[26] |
Kõljalg, U., Nilsson, R.H., Abarenkov, K., Tedersoo, L., Taylor, A.F., Bahram, M., Bates, S.T., Bruns, T.D., Bengtsson-Palme, J., Callaghan, T.M., Douglas, B., Drenkhan, T., Eberhardt, U., Dueñas, M., Grebenc, T., Griffith, G.W., Hartmann, M., Kirk, P.M., Kohout, P., Larsson, E., Lindahl, B.D., Lücking, R., Martín, M.P., Matheny, P.B., Nguyen, N.H., Niskanen, T., Oja, J., Peay, K.G., Peintner, U., Peterson, M., Põldmaa, K., Saag, L., Saar, I., Schüßler, A., Scott, J.A., Senés, C., Smith, M.E., Suija, A., Taylor, D.L., Telleria, M.T., Weiss, M., Larsson, K.H., 2013. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22, 5271–5277
CrossRef
Pubmed
Google scholar
|
[27] |
Li, X., Huang, L., 2015. Toward a new paradigm for tailings phytostabilization—nature of the substrates, amendment options, and anthropogenic pedogenesis. Critical Reviews in Environmental Science and Technology 45, 813–839
CrossRef
Google scholar
|
[28] |
Liu, J., Sui, Y., Yu, Z., Shi, Y., Chu, H., Jin, J., Liu, X., Wang, G., 2015. Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Biology & Biochemistry 83, 29–39
CrossRef
Google scholar
|
[29] |
Lundell, T.K., Mäkelä, M.R., Hildén, K., 2010. Lignin-modifying enzymes in filamentous basidiomycetes--ecological, functional and phylogenetic review. Journal of Basic Microbiology 50, 5–20
CrossRef
Pubmed
Google scholar
|
[30] |
Marschner, P., 2007. Soil microbial community structure and function assessed by FAME, PLFA and DGGE—advantages and limitations. In: Varma, A., Oelmüller, R., eds. Advanced Techniques in Soil Microbiology. Vol 11. Berlin: Springer, 181–200
|
[31] |
Mendez, M.O., Maier, R.M., 2008. Phytostabilization of mine tailings in arid and semiarid environments--an emerging remediation technology. Environmental Health Perspectives 116, 278–283
CrossRef
Pubmed
Google scholar
|
[32] |
Mulligan, D.R., Gillespie, M.J., Gravina, A.J., Currey, N.A., 2006. An assessment of the direct revegetation strategy on the tailings storage facility at Kidston gold mine, North Queensland, Australia. In: Fourie, A., Tibbett, M., eds. Proceedings of the First International Seminar on Mine Closure. Perth: Australian Centre for Geomechanics, 371–381
|
[33] |
Nemergut, D.R., Townsend, A.R., Sattin, S.R., Freeman, K.R., Fierer, N., Neff, J.C., Bowman, W.D., Schadt, C.W., Weintraub, M.N., Schmidt, S.K., 2008. The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environmental Microbiology 10, 3093–3105
CrossRef
Pubmed
Google scholar
|
[34] |
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2015. Vegan: Community Ecology Package, R package version 2.3–1
|
[35] |
Pennanen, T., Frostegard, A., Fritze, H., Baath, E., 1996. Phospholipid fatty acid composition and heavy metal tolerance of soil microbial communities along two heavy metal-polluted gradients in coniferous forests. Applied and Environmental Microbiology 62, 420–428
CrossRef
Pubmed
Google scholar
|
[36] |
Pitt, J.I., Samson, R.A., Frisvad, J.C., 2000. List of accepted species and their synonyms in the family Trichocomaceae. In: Samson RA, Pitt JI, eds. Integration of modern taxonomic methods for Penicillium and Aspergillus classification. Amsterdam: Harwood Academic Publishers, 9–79
|
[37] |
Rastogi, G., Sani, R.K., 2011. Molecular techniques to assess microbial community structure, function, and dynamics in the environment. In: Ahmad, I., Ahmad, F., Pichtel, J., eds. Microbes and microbial technology: agricultural and environmental applications. New York: Springer, 29–57
|
[38] |
Renella, G., Landi, L., Ascher, J., Ceccherini, M.T., Pietramellara, G., Mench, M., Nannipieri, P., 2008. Long-term effects of aided phytostabilisation of trace elements on microbial biomass and activity, enzyme activities, and composition of microbial community in the Jales contaminated mine spoils. Environmental Pollution 152, 702–712
CrossRef
Pubmed
Google scholar
|
[39] |
Roseby, S.J., Mulligan, D.R., Menzies, N.W., Ritchie, P.J., Currey, N.A., 1998. Ecosystem development on tailings at Kidston Gold Mine, North Queensland, Australia. In: Fox HR, Moore HM, McIntosh AD, eds. Land reclamation: achieving sustainable benefits. Rotterdam: A. A. Balkema, 137–142
|
[40] |
Rousk, J., Bååth, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal 4, 1340–1351
CrossRef
Pubmed
Google scholar
|
[41] |
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J., Weber, C.F., 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541
CrossRef
Pubmed
Google scholar
|
[42] |
Shokralla, S., Spall, J.L., Gibson, J.F., Hajibabaei, M., 2012. Next-generation sequencing technologies for environmental DNA research. Molecular Ecology 21, 1794–1805
CrossRef
Pubmed
Google scholar
|
[43] |
Shukla, M.K., Lal, R., Ebinger, M.H., 2005. Physical and chemical properties of a minespoil eight years after reclamation in northeastern Ohio. Soil Science Society of America Journal 69, 1288–1297
CrossRef
Google scholar
|
[44] |
Solís-Domínguez, F.A., Valentín-Vargas, A., Chorover, J., Maier, R.M., 2011. Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Science of the Total Environment 409, 1009–1016
CrossRef
Pubmed
Google scholar
|
[45] |
Sun, S., Badgley, B.D., 2019. Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration. Soil Biology & Biochemistry 135, 163–172
CrossRef
Google scholar
|
[46] |
Tedersoo, L., Kõljalg, U., Hallenberg, N., Larsson, K.H., 2003. Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytologist 159, 153–165
CrossRef
Google scholar
|
[47] |
Thavamani, P., Samkumar, R.A., Satheesh, V., Subashchandrabose, S.R., Ramadass, K., Naidu, R., Venkateswarlu, K., Megharaj, M., 2017. Microbes from mined sites: Harnessing their potential for reclamation of derelict mine sites. Environmental Pollution 230, 495–505
CrossRef
Pubmed
Google scholar
|
[48] |
Tilman, D., Wedin, D., Knops, J., 1996. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379, 718–720
CrossRef
Google scholar
|
[49] |
Tordoff, G.M., Baker, A.J.M., Willis, A.J., 2000. Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41, 219–228
CrossRef
Pubmed
Google scholar
|
[50] |
Valentín-Vargas, A., Root, R.A., Neilson, J.W., Chorover, J., Maier, R.M., 2014. Environmental factors influencing the structural dynamics of soil microbial communities during assisted phytostabilization of acid-generating mine tailings: a mesocosm experiment. Science of the Total Environment 500-501, 314–324
CrossRef
Pubmed
Google scholar
|
[51] |
van der Heijden, M.G., Bardgett, R.D., van Straalen, N.M., 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11, 296–310
CrossRef
Pubmed
Google scholar
|
[52] |
Volant, A., Héry, M., Desoeuvre, A., Casiot, C., Morin, G., Bertin, P.N., Bruneel, O., 2016. Spatial distribution of eukaryotic communities using high-throughput sequencing along a pollution gradient in the arsenic-rich creek sediments of Carnoulès mine, France. Microbial Ecology 72, 608–620
CrossRef
Pubmed
Google scholar
|
[53] |
Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73, 5261–5267
CrossRef
Pubmed
Google scholar
|
[54] |
Whitelaw, M.A., 1999. Growth promotion of plants inoculated with phosphate-solubilizing fungi. Advances in Agronomy 69, 99–151
CrossRef
Google scholar
|
[55] |
Whiteway, M., Tebung, W.A., Choudhury, B.I., Rodríguez-Ortiz, R., 2015. Metabolic regulation in model ascomycetes--adjusting similar genomes to different lifestyles. Trends in Genetics 31, 445–453
CrossRef
Pubmed
Google scholar
|
[56] |
Xu, L., Ravnskov, S., Larsen, J., Nilsson, R.H., Nicolaisen, M., 2012. Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Biology & Biochemistry 46, 26–32
CrossRef
Google scholar
|
[57] |
Yang, S.X., Liao, B., Yang, Z.H., Chai, L.Y., Li, J.T., 2016. Revegetation of extremely acid mine soils based on aided phytostabilization: A case study from southern China. Science of the Total Environment 562, 427–434
CrossRef
Pubmed
Google scholar
|
[58] |
Yang, T.T., Liu, J., Chen, W.C., Chen, X., Shu, H.Y., Jia, P., Liao, B., Shu, W.S., Li, J.T., 2017. Changes in microbial community composition following phytostabilization of an extremely acidic Cu mine tailings. Soil Biology & Biochemistry 114, 52–58
CrossRef
Google scholar
|
[59] |
Yao, Q., Liu, J., Yu, Z., Li, Y., Jin, J., Liu, X., Wang, G., 2017. Three years of biochar amendment alters soil physiochemical properties and fungal community composition in a black soil of northeast China. Soil Biology & Biochemistry 110, 56–67
CrossRef
Google scholar
|
[60] |
Yilmaz, N., Visagie, C.M., Houbraken, J., Frisvad, J.C., Samson, R.A., 2014. Polyphasic taxonomy of the genus Talaromyces. Studies in Mycology 78, 175–341
CrossRef
Pubmed
Google scholar
|
[61] |
Yu, L.H., Jia, W.L., Xue, Y.Z., 2009. Survey and analysis of the copper tailing resources in China. Metal Mine 8, 179–181.
|
[62] |
Zornoza, R., Acosta, J.A., Martínez-Martínez, S., Faz, A., Bååth, E., 2015. Main factors controlling microbial community structure and function after reclamation of a tailing pond with aided phytostabilization. Geoderma 245, 1–10
CrossRef
Google scholar
|
/
〈 | 〉 |