A Matter of Metals: Copper but Not Cadmium Affects the Microbial Alpha-Diversity of Soils and Sediments - a Meta-analysis
Language English Country United States Media print-electronic
Document type Meta-Analysis, Journal Article
Grant support
TN200V
Libera Università di Bolzano
PubMed
36180621
PubMed Central
PMC10335967
DOI
10.1007/s00248-022-02115-4
PII: 10.1007/s00248-022-02115-4
Knihovny.cz E-resources
- Keywords
- Alpha-diversity, Bacterial communities, Heavy metals, Meta-analysis, Rhizosphere, Sediment, Soil,
- MeSH
- Bacteria genetics MeSH
- Cadmium MeSH
- Soil Pollutants * analysis MeSH
- Copper analysis MeSH
- Soil MeSH
- Soil Microbiology MeSH
- Metals, Heavy * analysis MeSH
- Publication type
- Journal Article MeSH
- Meta-Analysis MeSH
- Names of Substances
- Cadmium MeSH
- Soil Pollutants * MeSH
- Copper MeSH
- Soil MeSH
- Metals, Heavy * MeSH
Heavy metal (HM) accumulation in soil affects plants and soil fauna, yet the effect on microbial alpha-diversity remains unclear, mainly due to the absence of dedicated research synthesis (e.g. meta-analysis). Here, we report the first meta-analysis of the response of soil microbial alpha-diversity to the experimental addition of cadmium (Cd) and copper (Cu). We considered studies conducted between 2013 and 2022 using DNA metabarcoding of bacterial and fungal communities to overcome limitations of other cultivation- and electrophoresis-based techniques. Fungi were discarded due to the limited study number (i.e. 6 studies). Bacterial studies resulted in 66 independent experiments reported in 32 primary papers from four continents. We found a negative dose-dependent response for Cu but not for Cd for bacterial alpha-diversity in the environments, only for Cu additions exceeding 29.6 mg kg-1 (first loss of - 0.06% at 30 mg kg-1). The maximal loss of bacterial alpha-diversity registered was 13.89% at 3837 mg kg-1. Our results first highlight that bacterial communities behave differently to soil pollution depending on the metal. Secondly, our study suggests that even extreme doses of Cu do not cause a dramatic loss in alpha-diversity, highlighting how the behaviour of bacterial communities diverges from soil macro-organisms.
Competence Centre for Plant Health Free University of Bolzano Bolzano Italy
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
Faculty of Science and Technology Free University of Bolzano Piazza Università 5 Bolzano Italy
See more in PubMed
Dantas de Miranda M, Pereira HM, Corley MFV, Merckx T. Beta diversity patterns reveal positive effects of farmland abandonment on moth communities. Sci Rep. 2019;9(1):1–9. doi: 10.1038/s41598-018-38200-3. PubMed DOI PMC
Grilli J. Macroecological laws describe variation and diversity in microbial communities. Nat Commun. 2020;11(1):1–11. doi: 10.1038/s41467-020-18529-y. PubMed DOI PMC
Jost L. Partitioning diversity into independent alpha beta concepts. Ecology. 2007;88(10):2427–2439. doi: 10.1890/06-1736.1. PubMed DOI
Prober SM, et al. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett. 2015;18(1):85–95. doi: 10.1111/ele.12381. PubMed DOI
Walters KE, Martiny JBH. Alpha-, beta-, and gamma-diversity of bacteria varies across habitats. PLoS One. 2020;15(9 September):1–17. doi: 10.1371/journal.pone.0233872. PubMed DOI PMC
Edward O. Wilson, The diversity of life. Massachusetts: Belknap Press of Harvard University Press; 1992.
Hagerty SL, Hutchison KE, Lowry CA, Bryan AD. An empirically derived method for measuring human gut microbiome alpha diversity: demonstrated utility in predicting healthrelated outcomes among a human clinical sample. PLoS ONE. 2020;15(3):1–21. doi: 10.1371/journal.pone.0229204. PubMed DOI PMC
T. H. M. P. Consortium Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214. doi: 10.1038/nature11234. PubMed DOI PMC
Whittaker RH. Evolution and measurement of species diversity. Taxon. 1972;21(2/3):213–251. doi: 10.2307/1218190. DOI
Fierer N, Jackson RB. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A. 2006;103(3):626–631. doi: 10.1073/pnas.0507535103. PubMed DOI PMC
Kaarlejärvi E, Salemaa M, Tonteri T, Merilä P, Laine AL. Temporal biodiversity change following disturbance varies along an environmental gradient. Glob Ecol Biogeogr. 2021;30(2):476–489. doi: 10.1111/geb.13233. DOI
Kondratyeva A, et al. Urbanization effects on biodiversity revealed by a two-scale analysis of species functional uniqueness vs. redundancy. Front Ecol Evol. 2020;8(March):1–16. doi: 10.3389/fevo.2020.00073. DOI
Willig MR, Presley SJ (2017) Biodiversity and disturbance, vol. 1–5. Elsevier Inc. 10.1016/B978-0-12-809665-9.09813-X
Johnson CN, et al. Biodiversity losses and conservation responses in the Anthropocene. Science (80) 2017;356(6335):270–275. doi: 10.1126/science.aam9317. PubMed DOI
Seddon N, et al. Biodiversity in the anthropocene: prospects and policy. Proc R Soc B Biol Sci. 2016;283(1844):1–9. doi: 10.1098/rspb.2016.2094. PubMed DOI PMC
Krinner G, et al. Long-term climate change: projections, commitments and irreversibility. Clim Chang 2013 Phys Sci Basis Work Gr I Contrib Fifth Assess Rep Intergov Panel Clim Chang. 2013;9781107057:1029–1136. doi: 10.1017/CBO9781107415324.024. DOI
Monchanin C, Devaud JM, Barron AB, Lihoreau M. Current permissible levels of metal pollutants harm terrestrial invertebrates. Sci Total Environ. 2021;779:146398. doi: 10.1016/j.scitotenv.2021.146398. PubMed DOI
Sánchez-Bayo F, Wyckhuys KAG. Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv. 2019;232(September 2018):8–27. doi: 10.1016/j.biocon.2019.01.020. DOI
Alloway BJ. Heavy Met Soils. 2013 doi: 10.1007/978-94-007-4470-7. DOI
Genova G et al (2021) Copper and zinc as a window to past agricultural land-use. J Hazard Mater (March): 126631. 10.1016/j.jhazmat.2021.126631 PubMed
Tovar-Sánchez E, Hernández-Plata I, Martínez MS, Valencia-Cuevas L, Galante PM. Heavy metal pollution as a biodiversity threat. Heavy Met. 2018 doi: 10.5772/intechopen.74052. DOI
Hu C, Shui B, Yang X, Wang L, Dong J, Zhang X. Trophic transfer of heavy metals through aquatic food web in a seagrass ecosystem of Swan Lagoon, China. Sci Total Environ. 2021;762:143139. doi: 10.1016/j.scitotenv.2020.143139. PubMed DOI
Michelutti N, et al. Trophic position influences the efficacy of seabirds as metal biovectors. Proc Natl Acad Sci U S A. 2010;107(23):10543–10548. doi: 10.1073/pnas.1001333107. PubMed DOI PMC
Heikens A, Peijnenburg WJGM, Hendriks AJ. Bioaccumulation of heavy metals in terrestrial invertebrates. Environ Pollut. 2001;113(3):385–393. doi: 10.1016/S0269-7491(00)00179-2. PubMed DOI
Moyson S, Town RM, Vissenberg K, Blust R. The effect of metal mixture composition on toxicity to C. elegans at individual and population levels. PLoS One. 2018;14(6):1–23. doi: 10.1371/journal.pone.0218929. PubMed DOI PMC
Nahmani J, Lavelle P. Effects of heavy metal pollution on soil macrofauna in a grassland of Northern France. Eur J Soil Biol. 2002;38(3–4):297–300. doi: 10.1016/S1164-5563(02)01169-X. DOI
Spurgeon DJ, Hopkin SP. Seasonal variation in the abundance, biomass and biodiversity of earthworms in soils contaminated with metal emissions from a primary smelting works. J Appl Ecol. 1999;36(1):173–183. doi: 10.1046/j.1365-2664.1999.00389.x. DOI
Manu M, Honciuc V, Neagoe A, Băncilă RI, Iordache V, Onete M. Soil mite communities (Acari: Mesostigmata, Oribatida) as bioindicators for environmental conditions from polluted soils. Sci Rep. 2019;9(1):1–13. doi: 10.1038/s41598-019-56700-8. PubMed DOI PMC
Gutiérrez C, et al. Effect of soil properties, heavy metals and emerging contaminants in the soil nematodes diversity. Environ Pollut. 2016;213:184–194. doi: 10.1016/j.envpol.2016.02.012. PubMed DOI
Chauvin C, et al. Soil nematodes as indicators of heavy metal pollution: a meta-analysis. Open J Soil Sci. 2020;10(12):579–601. doi: 10.4236/ojss.2020.1012028. DOI
Pouyat RV, et al. Multi-scale assessment of metal contamination in residential soil and soil fauna: a case study in the Baltimore-Washington metropolitan region, USA. Landsc Urban Plan. 2015;142:7–17. doi: 10.1016/j.landurbplan.2015.05.001. DOI
Dance A. The search for microbial dark matter. Nature. 2020;582(7811):301–303. doi: 10.1038/d41586-020-01684-z. PubMed DOI
Thaler DS (2021) Is global microbial biodiversity increasing, decreasing, or staying the same? Front Ecol Evol 9(April). 10.3389/fevo.2021.565649
FAO (2020) State of knowledge of soil biodiversity - status, challenges and potentialities. 10.4060/cb1928en
Raynaud X, Nunan N (2014) Spatial ecology of bacteria at the microscale in soil. PLoS One 9(1). 10.1371/journal.pone.0087217. PubMed PMC
Roesch LFW, et al. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 2007;1(4):283–290. doi: 10.1038/ismej.2007.53. PubMed DOI PMC
Torsvik V, Goksoyr J, Daae FL. High diversity in DNA of soil bacteria. Appl Environ Microbiol. 1990;56(3):782–787. doi: 10.1128/aem.56.3.782-787.1990. PubMed DOI PMC
Trevors JT. One gram of soil: a microbial biochemical gene library, Antonie van Leeuwenhoek. Int J Gen Mol Microbiol. 2010;97(2):99–106. doi: 10.1007/s10482-009-9397-5. PubMed DOI
Almela P, Velázquez D, Rico E, Justel A, Quesada A. Carbon pathways through the food web of a microbial mat from byers peninsula, antarctica. Front Microbiol. 2019;10(MAR):1–11. doi: 10.3389/fmicb.2019.00628. PubMed DOI PMC
Antunes PM, Koyama A (2017) Mycorrhizas as nutrient and energy pumps of soil food webs: multitrophic interactions and feedbacks, no. November. Elsevier Inc. 10.1016/B978-0-12-804312-7.00009-7
Heijboer A, de Ruiter PC, Bodelier PLE, Kowalchuk GA. Modulation of litter decomposition by the soil microbial food web under influence of land use change. Front Microbiol. 2018;9(NOV):1–11. doi: 10.3389/fmicb.2018.02860. PubMed DOI PMC
Holtkamp R, Kardol P, van der Wal A, Dekker SC, van der Putten WH, de Ruiter PC. Soil food web structure during ecosystem development after land abandonment. Appl Soil Ecol. 2008;39(1):23–34. doi: 10.1016/j.apsoil.2007.11.002. DOI
Potapov AM, et al. Size compartmentalization of energy channeling in terrestrial belowground food webs. Ecology. 2021;102(8):1–14. doi: 10.1002/ecy.3421. PubMed DOI
Borruso L, Zerbe S, Brusetti L. Bacterial community structures as a diagnostic tool for watershed quality assessment. Res Microbiol. 2015;166(1):38–44. doi: 10.1016/j.resmic.2014.11.004. PubMed DOI
Hoshino T, et al. Global diversity of microbial communities in marine sediment. Proc Natl Acad Sci U S A. 2020;117(44):27587–27597. doi: 10.1073/pnas.1919139117. PubMed DOI PMC
Varliero G, Bienhold C, Schmid F, Boetius A, Molari M. Microbial diversity and connectivity in deep-sea sediments of the South Atlantic Polar Front. Front Microbiol. 2019;10(APR):1–18. doi: 10.3389/fmicb.2019.00665. PubMed DOI PMC
Cavicchioli R, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17(9):569–586. doi: 10.1038/s41579-019-0222-5. PubMed DOI PMC
Danovaro R, Corinaldesi C, Rastelli E, Dell’Anno A. Towards a better quantitative assessment of the relevance of deep-sea viruses, bacteria and archaea in the functioning of the ocean seafloor. Aquat Microb Ecol. 2015;75(1):81–90. doi: 10.3354/ame01747. DOI
Flemming HC, Wuertz S. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol. 2019;17(4):247–260. doi: 10.1038/s41579-019-0158-9. PubMed DOI
Wang Y, et al. Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl Environ Microbiol. 2012;78(23):8264–8271. doi: 10.1128/AEM.01821-12. PubMed DOI PMC
Haferburg G, Kothe E. Microbes and metals: interactions in the environment. J Basic Microbiol. 2007;47(6):453–467. doi: 10.1002/jobm.200700275. PubMed DOI
Gadd GM, Griffiths AJ. Microorganisms and heavy metal toxicity. Microb Ecol. 1978;4(4):303–317. doi: 10.1007/BF02013274. PubMed DOI
Yi J, Lo LSH, Liu H, Qian P-Y, Cheng J. Study of heavy metals and microbial communities in contaminated sediments along an urban estuary. Front Mar Sci. 2021;8(November):1–17. doi: 10.3389/fmars.2021.741912. PubMed DOI
Frossard A, Hartmann M, Frey B. Tolerance of the forest soil microbiome to increasing mercury concentrations. Soil Biol Biochem. 2017;105:162–176. doi: 10.1016/j.soilbio.2016.11.016. DOI
Rajapaksha RMCP, Tobor-Kapłon MA, Bååth E. Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol. 2004;70(5):2966–2973. doi: 10.1128/AEM.70.5.2966-2973.2004. PubMed DOI PMC
Gerwien F, Skrahina V, Kasper L, Hube B, Brunke S. Metals in fungal virulence. FEMS Microbiol Rev. 2018;42(1):1–21. doi: 10.1093/femsre/fux050. PubMed DOI PMC
Solioz M (2019) Copper disposition in bacteria. Elsevier Inc. 10.1016/b978-0-12-810532-0.00011-2
Vest KE, Zhu X, Cobine PA (2019) Copper disposition in yeast, in Clinical and Translational Perspectives on WILSON DISEASE, Elsevier Inc, pp. 115–126. 10.1016/b978-0-12-810532-0.00012-4
Hao X, et al. Recent advances in exploring the heavy metal(loid) resistant microbiome. Comput Struct Biotechnol J. 2021;19:94–109. doi: 10.1016/j.csbj.2020.12.006. PubMed DOI PMC
Xie Y, et al. Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation. Front Plant Sci. 2016;7(MAY2016):1–12. doi: 10.3389/fpls.2016.00755. PubMed DOI PMC
Chen Y, et al. Long-term and high-concentration heavy-metal contamination strongly influences the microbiome and functional genes in Yellow River sediments. Sci Total Environ. 2018;637–638:1400–1412. doi: 10.1016/j.scitotenv.2018.05.109. PubMed DOI
Ding Z, Wu J, You A, Huang B, Cao C. Effects of heavy metals on soil microbial community structure and diversity in the rice (Oryza sativa L. subsp. Japonica, Food Crops Institute of Jiangsu Academy of Agricultural Sciences) rhizosphere. Soil Sci Plant Nutr. 2017;63(1):75–83. doi: 10.1080/00380768.2016.1247385. DOI
Tipayno SC, et al. The bacterial community structure and functional profile in the heavy metal contaminated paddy soils, surrounding a nonferrous smelter in South Korea. Ecol Evol. 2018;8(12):6157–6168. doi: 10.1002/ece3.4170. PubMed DOI PMC
Neaman A, Selles I, Martínez CE, Dovletyarova EA. Analyzing soil metal toxicity: spiked or field-contaminated soils? Environ Toxicol Chem. 2020;39(3):513–514. doi: 10.1002/etc.4654. PubMed DOI
Keiblinger KM, et al. Assessment of Cu applications in two contrasting soils—effects on soil microbial activity and the fungal community structure. Ecotoxicology. 2018;27(2):217–233. doi: 10.1007/s10646-017-1888-y. PubMed DOI PMC
Liu Y, et al. Application of low dosage of copper oxide and zinc oxide nanoparticles boosts bacterial and fungal communities in soil. Sci Total Environ. 2021;757:143807. doi: 10.1016/j.scitotenv.2020.143807. PubMed DOI
Naveed M, et al. Simultaneous loss of soil biodiversity and functions along a copper contamination gradient: when soil goes to sleep. Soil Sci Soc Am J. 2014;78(4):1239–1250. doi: 10.2136/sssaj2014.02.0052. DOI
Karimi B et al (2021) Ecotoxicity of copper input and accumulation for soil biodiversity in vineyards. Environ Chem Lett 0123456789. 10.1007/s10311-020-01155-x
Briffa J, Sinagra E, Blundell R. Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon. 2020;6(9):e04691. doi: 10.1016/j.heliyon.2020.e04691. PubMed DOI PMC
Cesco S, et al. A smart and sustainable future for viticulture is rooted in soil: How to face cu toxicity. Appl Sci. 2021;11(3):1–21. doi: 10.3390/app11030907. DOI
Daehn KE, Cabrera Serrenho A, Allwood JM. How will copper contamination constrain future global steel recycling? Environ Sci Technol. 2017;51(11):6599–6606. doi: 10.1021/acs.est.7b00997. PubMed DOI
Lamichhane JR, Osdaghi E, Behlau F, Köhl J, Jones JB, Aubertot JN (2018) Thirteen decades of antimicrobial copper compounds applied in agriculture. A review. Agron Sustain Dev 38(3). 10.1007/s13593-018-0503-9
Hedges LV, Gurevitch J, Curtis PS. The meta-analysis of response ratios in experimental ecology. Ecology. 1999;80(4):1150. doi: 10.2307/177062. DOI
Gleser L, Olkin I (2009) Stochastically dependent effect sizes. In Cooper H, Hedges LV, Valentine JC (eds) The handbook of research synthesis and meta-analysis. Russell Sage Foundation, pp 357–376
Lajeunesse MJ. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology. 2011;92(11):2049–2055. doi: 10.1890/11-0423.1. PubMed DOI
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor Package. J Stat Softw 36(3). 10.18637/jss.v036.i03
Hengl T et al (2017) SoilGrids250m: global gridded soil information based on machine learning. 12(2). 10.1371/journal.pone.0169748 PubMed PMC
Guerra CA, et al. Blind spots in global soil biodiversity and ecosystem function research. Nat Commun. 2020;11(1):1–13. doi: 10.1038/s41467-020-17688-2. PubMed DOI PMC
Konstantopoulos S. Fixed effects and variance components estimation in three-level meta-analysis. Res Synth Methods. 2011;2(1):61–76. doi: 10.1002/jrsm.35. PubMed DOI
Ishak KJ, Platt RW, Joseph L, Hanley JA, Caro JJ. Meta-analysis of longitudinal studies. Clin Trials. 2007;4(5):525–539. doi: 10.1177/1740774507083567. PubMed DOI
Trikalinos TA, Olkin I. Meta-analysis of effect sizes reported at multiple time points: a multivariate approach. Clin Trials. 2012;9(5):610–620. doi: 10.1177/1740774512453218. PubMed DOI
Jennions MD, Møller AP. Relationships fade with time: a meta-analysis of temporal trends in publication in ecology and evolution. Proc R Soc B Biol Sci. 2002;269(1486):43–48. doi: 10.1098/rspb.2001.1832. PubMed DOI PMC
Nakagawa S, Santos ESA. Methodological issues and advances in biological meta-analysis. Evol Ecol. 2012;26(5):1253–1274. doi: 10.1007/s10682-012-9555-5. DOI
Luo J, Hein C, Mücklich F, Solioz M. Killing of bacteria by copper, cadmium, and silver surfaces reveals relevant physicochemical parameters. Biointerphases. 2017;12(2):020301. doi: 10.1116/1.4980127. PubMed DOI
Moyson S, Vissenberg K, Fransen E, Blust R, Husson SJ. Mixture effects of copper, cadmium, and zinc on mortality and behavior of Caenorhabditis elegans. Environ Toxicol Chem. 2018;37(1):145–159. doi: 10.1002/etc.3937. PubMed DOI
Giachino A, Waldron KJ. Copper tolerance in bacteria requires the activation of multiple accessory pathways. Mol Microbiol. 2020;114(3):377–390. doi: 10.1111/mmi.14522. PubMed DOI
Chen J, Zhang H, Li J, Liu Y, Shi W, Hu H. The toxic factor of copper should be adjusted during the ecological risk assessment for soil bacterial community. Ecol Indic. 2020;111(October 2019):106072. doi: 10.1016/j.ecolind.2020.106072. DOI
Fang F, Imlay JA. Silver ( I ), mercury ( II ), cadmium ( II ), and zinc ( II ) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. Appl Environ Microbiol. 2012;78(10):3614–3621. doi: 10.1128/AEM.07368-11. PubMed DOI PMC
Macomber L, Imlay JA. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci U S A. 2009;106(20):8344–8349. doi: 10.1073/pnas.0812808106. PubMed DOI PMC
Stubbendieck RM, Vargas-bautista C, Straight PD, Romero DF, Beauregard P (2016) Bacterial communities : interactions to scale. 7(August): 1–19. 10.3389/fmicb.2016.01234 PubMed PMC
Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. 104(27). 10.1073/pnas.0611525104 PubMed PMC
Hoshino T, Doi H, Uramoto G, Wörmer L, Adhikari RR, Xiao N (2020) Global diversity of microbial communities in marine sediment. 117(44): 27587–27597. 10.1073/pnas.1919139117 PubMed PMC
Salah I, Parkin IP, Allan E. Copper as an antimicrobial agent: recent advances. RSC Adv. 2021;11(30):18179–18186. doi: 10.1039/d1ra02149d. PubMed DOI PMC
Morey JR, Begg SL, Eijkelkamp BA, Luo Z, Couñago RM, Omara ML, Maher MJ, Ong C-LY, McEwan AG, Kobe B, Paton JC, McDevitt CA. Disregulation of transition metal ion homeostasis is the molecular basis for cadmium toxicity in Streptococcus pneumoniae. Nat Commun. 2014 doi: 10.1038/ncomms7418. PubMed DOI PMC
Ballabio C, et al. Copper distribution in European topsoils: an assessment based on LUCAS soil survey. Sci Total Environ. 2018;636:282–298. doi: 10.1016/j.scitotenv.2018.04.268. PubMed DOI
Jiang HH, Cai LM, Wen HH, Luo J. Characterizing pollution and source identification of heavy metals in soils using geochemical baseline and PMF approach. Sci Rep. 2020;10(1):1–11. doi: 10.1038/s41598-020-63604-5. PubMed DOI PMC
Mihaileanu RG et al (2019) Assessment of heavy metals (total chromium, lead, and manganese) contamination of residential soil and homegrown vegetables near a former chemical manufacturing facility in Tarnaveni, Romania. Environ Monit Assess 191(1). 10.1007/s10661-018-7142-0 PubMed
Tóth G, Hermann T, Szatmári G, Pásztor L. Maps of heavy metals in the soils of the European Union and proposed priority areas for detailed assessment. Sci Total Environ. 2016;565:1054–1062. doi: 10.1016/j.scitotenv.2016.05.115. PubMed DOI
Chen H, An J, Wei S, Gu J. Spatial patterns and risk assessment of heavy metals in soils in a resource-exhausted city, Northeast China. PLoS One. 2015;10(9):1–12. doi: 10.1371/journal.pone.0137694. PubMed DOI PMC
Lado LR, Hengl T, Reuter HI. Heavy metals in European soils: a geostatistical analysis of the FOREGS Geochemical database. Geoderma. 2008;148(2):189–199. doi: 10.1016/j.geoderma.2008.09.020. DOI
Zhang W, Liu M, Li C. Soil heavy metal contamination assessment in the Hun-Taizi River watershed, China. Sci Rep. 2020;10(1):1–10. doi: 10.1038/s41598-020-65809-0. PubMed DOI PMC
Dumestre A, Sauve S, Mcbride M, Baveye P, Berthelin J (1999) Environmental contamination and toxicology copper speciation and microbial activity in long-term contaminated soils. 131: 124–131. 10.1007/s002449900451 PubMed
Mirlean N, Roisenberg A, Chies JO. Metal contamination of vineyard soils in wet subtropics (southern Brazil) Environ Pollut. 2007;149(1):10–17. doi: 10.1016/j.envpol.2006.12.024. PubMed DOI
Schaider LA, Senn DB, Estes ER, Brabander DJ, Shine JP. Sources and fates of heavy metals in a mining-impacted stream: temporal variability and the role of iron oxides. Sci Total Environ. 2014;490:456–466. doi: 10.1016/j.scitotenv.2014.04.126. PubMed DOI PMC
Senkondo YH, Semu E, Tack FMG. Vertical distribution of copper in copper-contaminated coffee fields in Kilimanjaro, Tanzania. Commun Soil Sci Plant Anal. 2015;46(10):1187–1199. doi: 10.1080/00103624.2015.1019085. DOI
Wei B, Yang L. A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchem J. 2010;94(2):99–107. doi: 10.1016/j.microc.2009.09.014. DOI
Moroń D, et al. Abundance and diversity of wild bees along gradients of heavy metal pollution. J Appl Ecol. 2012;49(1):118–125. doi: 10.1111/j.1365-2664.2011.02079.x. DOI
Mejias Carpio IE, Ansari A, Rodrigues DF. Relationship of biodiversity with heavy metal tolerance and sorption capacity: a meta-analysis approach. Environ Sci Technol. 2018;52(1):184–194. doi: 10.1021/acs.est.7b04131. PubMed DOI
Rillig MC, et al. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science (80) 2019;366(6467):886–890. doi: 10.1126/science.aay2832. PubMed DOI PMC
Rocca JD et al (2019) The Microbiome Stress Project: toward a global meta-analysis of environmental stressors and their effects on microbial communities. Front Microbiol 10(JAN). 10.3389/fmicb.2018.03272. PubMed PMC
Zhou Z, Wang C, Luo Y (2020) Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality. Nat Commun 11(1). 10.1038/s41467-020-16881-7 PubMed PMC
Shade A. Diversity is the question, not the answer. ISME J. 2017;11(1):1–6. doi: 10.1038/ismej.2016.118. PubMed DOI PMC
Chao A. Nonparametric estimation of the number of classes in a population. Scand J Stat. 1984;11(4):265–270.
Chao A, Lee SM. Estimating the number of classes via sample coverage. J Am Stat Assoc. 1992;87(417):210–217. doi: 10.1080/01621459.1992.10475194. DOI
Shannon CE, Weaver W (1964) The mathematical theory of communications. Int Bus 131
Simpson EH (1949) Measurment of diversity. Nature 688(1943): 688 [Online]. 10.1038/163688a0
Kurm V, Geisen S, Gera Hol WH. A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa. Environ Microbiol. 2019;21(2):750–758. doi: 10.1111/1462-2920.14492. PubMed DOI PMC
Shade A, et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. MBio. 2014;5(4):1–9. doi: 10.1128/mBio.01371-14. PubMed DOI PMC
Kabata-Pendias A (2011) Trace Elements in Soils and Plants - Fourth Edition 50 Suppl 1
Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15(10):579–590. doi: 10.1038/nrmicro.2017.87. PubMed DOI
Kicińska A, Pomykała R, Izquierdo-Diaz M. Changes in soil pH and mobility of heavy metals in contaminated soils. Eur J Soil Sci. 2022;73(1):1–14. doi: 10.1111/ejss.13203. DOI
Rieuwerts JS, Thornton I, Farago ME, Ashmore MR. Factors influencing metal bioavailability in soils: preliminary investigations for the development of a critical loads approach for metals. Chem Speciat Bioavailab. 1998;10(2):61–75. doi: 10.3184/095422998782775835. DOI
Oorts K (2013) Copper. In: Alloway B (eds) Heavy metals in soils. Environmental Pollution, vol 22. Springer, Dordrecht. 10.1007/978-94-007-4470-7_13
Bravin MN, Tentscher P, Rose J, Hinsinger P. Rhizosphere pH gradient controls copper availability in a strongly acidic soil. Environ Sci Technol. 2009;43(15):5686–5691. doi: 10.1021/es900055k. PubMed DOI
Broos K, et al. Soil factors controlling the toxicity of copper and zinc to microbial processes in Australian soils. Environ Toxicol Chem. 2007;26(4):583–590. doi: 10.1897/06-302R.1. PubMed DOI
Fernández-Calviño D, Bååth E. Interaction between pH and Cu toxicity on fungal and bacterial performance in soil. Soil Biol Biochem. 2016;96:20–29. doi: 10.1016/j.soilbio.2016.01.010. DOI
Fernández-Calviño D, Arias-Estévez M, Díaz-Raviña M, Bååth E. Bacterial pollution induced community tolerance (PICT) to Cu and interactions with pH in long-term polluted vineyard soils. Soil Biol Biochem. 2011;43(11):2324–2331. doi: 10.1016/j.soilbio.2011.08.001. DOI
Chen YT, Wang Y, Yeh KC. Role of root exudates in metal acquisition and tolerance. Curr Opin Plant Biol. 2017;39(Iii):66–72. doi: 10.1016/j.pbi.2017.06.004. PubMed DOI
De Conti L, et al. Iron fertilization to enhance tolerance mechanisms to copper toxicity of ryegrass plants used as cover crop in vineyards. Chemosphere. 2020;243:125298. doi: 10.1016/j.chemosphere.2019.125298. PubMed DOI
Montiel-Rozas MM, Madejón E, Madejón P. Effect of heavy metals and organic matter on root exudates (low molecular weight organic acids) of herbaceous species: an assessment in sand and soil conditions under different levels of contamination. Environ Pollut. 2016;216:273–281. doi: 10.1016/j.envpol.2016.05.080. PubMed DOI
Degryse F, Smolders E, Parker DR. Partitioning of metals (Cd Co, Cu, Ni, Pb, Zn) in soils: concepts, methodologies, prediction and applications - a review. Eur J Soil Sci. 2009;60(4):590–612. doi: 10.1111/j.1365-2389.2009.01142.x. DOI
Liu Y, Xu Z, Hu X, Zhang N, Chen T, Ding Z. Sorption of Pb(II) and Cu(II) on the colloid of black soil, red soil and fine powder kaolinite: effects of pH, ionic strength and organic matter. Environ Pollut Bioavailab. 2019;31(1):85–93. doi: 10.1080/26395940.2019.1578186. DOI
De Boer W, Folman LB, Summerbell RC, Boddy L. Living in a fungal world: Impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29(4):795–811. doi: 10.1016/j.femsre.2004.11.005. PubMed DOI
Emilia Hannula S, Morriën E (2022) Will fungi solve the carbon dilemma? Geoderma 413(February). 10.1016/j.geoderma.2022.115767
FracM, Hannula SE, Belka M, Jȩdryczka M (2018) Fungal biodiversity and their role in soil health. Front Microbiol 9(APR). 10.3389/fmicb.2018.00707 PubMed PMC
Egidi E et al (2019) A few Ascomycota taxa dominate soil fungal communities worldwide. Nat Commun 10(1). 10.1038/s41467-019-10373-z PubMed PMC
Lin Y, Xiao W, Ye Y, Wu C, Hu Y, Shi H. Adaptation of soil fungi to heavy metal contamination in paddy fields—a case study in eastern China. Environ Sci Pollut Res. 2020;27(22):27819–27830. doi: 10.1007/s11356-020-09049-9. PubMed DOI