Abstract
Events of soil contamination by heavy metals are mostly related to human activities that release these metals into the environment as emissions or effluents. Among the industrial activities related to heavy metal pollution, cement production plants are considered one of the most common sources. In this work we applied the High-throughput sequencing approach called 16 S rDNA metabarcoding to perform the taxonomic characterization of the prokaryotic communities of the soil surrounding three cement plants as well as two areas outside the influence of the cement plants that represented agricultural production environments free of heavy metal contamination (control areas). We applied the environmental genomics approaches known as “structural community metrics” (α- and β-diversity metrics) and “functional community metrics” (PICRUSt2 approach) to verify whether or not the effects of heavy metal contamination in the study area generated impacts on soil bacterial communities. We found that the impact related to the elevation of heavy metal concentration due to the operation of cement plants in the surrounding soil can be considered smooth according to globally recognized indices such as Igeo. However, we identified that both the taxonomic and functional structures of the communities surrounding cement plants were different from those found in the control areas. We consider that our findings contribute significantly to the general understanding of the effects of heavy metals on the soil ecosystem by showing that light contamination can disturb the dynamics of ecosystem services provided by soil, specifically those associated with microbial metabolism.
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Data availability
All sequencing data generated in this study can be accessed from GenBank Database at Bioproject PRJNA732183.
References
Abdu N, Abdullahi AA, Abdulkadir A (2017) Heavy metals and soil microbes. Environ Chem Lett 15:65–84. https://doi.org/10.1007/s10311-016-0587-x
Alvarez A, Saez JM, Costa JSD et al. (2017) Actinobacteria: current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere 166:41–62. https://doi.org/10.1016/j.chemosphere.2016.09.070
Baldrian P (2019) The known and the unknown in soil microbial ecology. FEMS Microbiol Ecol 95:fiz005. https://doi.org/10.1093/femsec/fiz005
Barka EA, Vatsa P, Sanchez L et al. (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43. https://doi.org/10.1128/MMBR.00019-15
Bermudez GM, Moreno M, Invernizzi R, Plá R, Pignata ML (2010) Heavy metal pollution in topsoils near a cement plant: the role of organic matter and distance to the source to predict total and HCl-extracted heavy metal concentrations. Chemosphere 78:375–381. https://doi.org/10.1016/j.chemosphere.2009.11.012
Beslin LG (2020) Significance of Environmental Genomics Research. J Biomed Res Environ Sci 23:103–104. https://doi.org/10.37871/jels1126
Bolyen E, Rideout JR, Dillon MR et al. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6:e04691. https://doi.org/10.1016/j.heliyon.2020.e04691
Brussaard L (1998) Soil fauna, guilds, functional groups and ecosystem processes. Appl Soil Ecol 9:123–135. https://doi.org/10.1016/S0929-1393(98)00066-3
Brussaard L (2012) Ecosystem services providedby the soil biota. In: Wall DH, Bardgett RD, Behan-Pelletier V, Herrick JE, Jones H, Ritz K, Six J, Strong DR, van der Putten WH (eds) Soil ecology and ecosystem services. Oxford University Press, Oxford, UK, pp 45–58
Bünemann EK, Bongiorno G, Bai Z et al. (2018) Soil quality–A critical review. Soil Biol Biochem 120:105–125. https://doi.org/10.1016/j.soilbio.2018.01.030
Changey F, Blaud A, Pando A, Herrmann AM, Lerch TZ (2021) Monitoring soil microbial communities using molecular tools: DNA extraction methods may offset long‐term management effects. Eur J Soil Sci 72:1026–1041. https://doi.org/10.1111/ejss.13026
Chase JM, McGill BJ, Thompson PL et al. (2019) Species richness change across spatial scales. Oikos 128:1079–1091. https://doi.org/10.1111/oik.05968
Cheaib B, Boulch ML, Mercier PL, Derome N (2018) Taxon-function decoupling as an adaptive signature of Lake Microbial metacommunities under a chronic polymetallic pollution gradient. Front Microbiol 9:869. https://doi.org/10.3389/fmicb.2018.00869
Chen J, He F, Zhang X, Sun X, Zheng J, Zheng J (2014) Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiol Ecol 87:164–181. https://doi.org/10.1111/1574-6941.12212
Choi K, Khan R, Lee SW (2021) Dissection of plant microbiota and plant-microbiome interactions. J Microbiol 59:281–291. https://doi.org/10.1007/s12275-021-0619-5
Cordier T, Alonso‐Sáez LApothéloz‐Perret‐Gentil L et al. (2020) Ecosystems monitoringpowered by environmental genomics: a review of current strategies with animplementation roadmap Mol Ecol. 1–22. https://doi.org/10.1111/mec.15472
Cristescu ME (2019) Can environmental RNA revolutionize biodiversity science? Trends Ecol Evol 34:694–697. https://doi.org/10.1016/j.tree.2019.05.003
Daims H (2014) 59 The Family Nitrospiraceae. In The Prokaryotes. Other Major Lineages of Bacteria and The Archaea. Springer
De Silva S, Ball AS, Indrapala DV, Reichman SM (2020) Review of the interactions between vehicular emitted potentially toxic elements, roadside soils, and associated biota. Chemosphere 128135. https://doi.org/10.1016/j.chemosphere.2020.128135
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
Diquattro S, Garau G, Mangia NP, Drigo B, Lombi E, Vasileiadis S, Castaldi P (2020) Mobility and potential bioavailability of antimony in contaminated soils: Short-term impact on microbial community and soil biochemical functioning. Ecotoxicol Environ Saf 196:110576. https://doi.org/10.1016/j.ecoenv.2020.110576
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
Durazzi F, Sala C, Castellani G et al. (2021) Comparison between 16S rRNA and shotgun sequencing data for the taxonomic characterization of the gut microbiota. Sci Rep 11:1–10. https://doi.org/10.1038/s41598-021-82726-y
Elangovan R, Philip L, Chandraraj K (2010) Hexavalent chromium reduction by free and immobilized cell-free extract of Arthrobacter rhombi-RE. Appl Biochem Biotechnol 160:81–97. https://doi.org/10.1007/s12010-008-8515-6
Ellis RJ, Neish B, Trett MW et al. (2001) Comparison of microbial and meiofaunal community analyses for determining impact of heavy metal contamination. J Microbiol Methods 45:171–185. https://doi.org/10.1016/S0167-7012(01)00245-7
Fajardo C, Costa G, Nande M, Botías P, García-Cantalejo J, Martín M (2019) Pb, Cd, and Zn soil contamination: monitoring functional and structural impacts on the microbiome. Appl Soil Ecol 135:56–64. https://doi.org/10.1016/j.apsoil.2018.10.022
Gilbert JA, Jansson JK, Knight R (2014) The Earth Microbiome project: successes and aspirations. BMC Biol 12:1–4. https://doi.org/10.1186/s12915-014-0069-1
Giller KE, Witter E, McGrath SP (2009) Heavy metals and soil microbes. Soil Biol Biochem 41:2031–2037. https://doi.org/10.1016/j.soilbio.2009.04.026
Gmach MR, Cherubin MR, Kaiser K, Cerri CEP (2020) Processes that influence dissolved organic matter in the soil: a review. Sci Agric 77:e20180164. https://doi.org/10.1590/1678-992x-2018-0164
Gong WJ, Niu ZF, Wang XR, Zhao HP (2021) How the soil microbial communities and activities respond to long-term heavy metal contamination in electroplating contaminated site. Microorganisms 9:362. https://doi.org/10.3390/microorganisms9020362
Gueuning M, Ganser D, Blaser S, Albrecht M, Knop E, Praz C, Frey JE (2019) Evaluating next‐generation sequencing (NGS) methods for routine monitoring of wild bees: Metabarcoding, mitogenomics or NGS barcoding. Mol Ecol Resour 19:847–862. https://doi.org/10.1111/1755-0998.13013
Gujre N, Mitra S, Soni A, Agnihotri R, Rangan L, Rene ER, Sharma MP (2021) Speciation, contamination, ecological and human health risks assessment of heavy metals in soils dumped with municipal solid wastes. Chemosphere 262:128013. https://doi.org/10.1016/j.chemosphere.2020.128013
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 27:1281–1291. https://doi.org/10.1007/s10646-018-1981-x
Hong C, Si Y, Xing Y, Li Y (2015) Illumina MiSeq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environ. Sci. & Pollut 22:10788–10799. https://doi.org/10.1007/s11356-015-4186-3
Jiang B, Adebayo A, Jia J et al. (2019) Impacts of heavy metals and soil properties at a Nigerian e-waste site on soil microbial community. J Hazard Mater 362:187–195. https://doi.org/10.1016/j.jhazmat.2018.08.060
Jafari A, Ghaderpoori M, Kamarehi B, Abdipour H (2019) Soil pollution evaluation and health risk assessment of heavy metals around Douroud cement factory, Iran. Environ Earth Sci 78:1–9. https://doi.org/10.1007/s12665-019-8220-5
Kandeler F, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Biol Fertil Soils 23:299–306. https://doi.org/10.1007/BF00335958
Kandeler E, Tscherko D, Bruce KD, Stemmer M, Hobbs PJ, Bardgett RD, Amelung W (2000) Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biol Fertil Soils 32:390–400. https://doi.org/10.1007/s003740000268
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27
Kasemodel MC, Sakamoto IK, Varesche MBA, Rodrigues VGS (2019) Potentially toxic metal contamination and microbial community analysis in an abandoned Pb and Zn mining waste deposit. Sci Total Environ 675:367–379. https://doi.org/10.1016/j.scitotenv.2019.04.223
Khachatryan L, de Leeuw RH, Kraakman ME et al. (2020) Taxonomic classification and abundance estimation using 16S and WGS—A comparison using controlled reference samples. Forensic Sci. Int. Genet. 46:102257. https://doi.org/10.1016/j.fsigen.2020.102257
Langille MGI, Zaneveld J, Caporaso JG et al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Lanzén A, Lekang K, Jonassen I, Thompson EM, Troedsson C (2017) DNA extraction replicates improve diversity and compositional dissimilarity in metabarcoding of eukaryotes in marine sediments. PLOS ONE 13:e0192337. https://doi.org/10.1371/journal.pone.0192337
Lazzaro A, Widmer F, Sperisen C, Frey B (2008) Identification of dominant bacterial phylotypes in a cadmium-treated forest soil. FEMS Microbiol Ecol 63:143–155. https://doi.org/10.1111/j.1574-6941.2007.00417.x
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
Lin Y, Ye Y, Hu Y, Shi H (2019) The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotoxicol Environ Saf 180:557–564. https://doi.org/10.1016/j.ecoenv.2019.05.057
Ling N, Sun Y, Ma J et al. (2014) Response of the bacterial diversity and soil enzyme activity in particle-size fractions of Mollisol after different fertilization in a long-term experiment. Biol Fertil Soils 50:901–911. https://doi.org/10.1007/s00374-014-0911-1
Liu C, Jin Y, Hu Y et al. (2019) Drivers of soil bacterial community structure and diversity in tropical agroforestry systems. Agric Ecosyst Environ 278:24–34. https://doi.org/10.1016/j.agee.2019.03.015
Mangold S, Potrykus J, Björn E, Lövgren L, Dopson M (2013) Extreme zinc tolerance in acidophilic microorganisms from the bacterial and archaeal domains. Extremophiles 17:75–85. https://doi.org/10.1007/s00792-012-0495-3
Meyer-Dombard DAR, Bogner JE, Malas J (2020) A Review of Landfill Microbiology and Ecology: A Call for Modernization With ‘Next Generation’Technology. Front Microbiol 11:1127. https://doi.org/10.3389/fmicb.2020.01127
Mishra S, Lin Z, Pang S, Zhang W, Bhatt P, Chen S (2021) Recent advanced technologies for the characterization of xenobiotic-degrading microorganisms and microbial communities. Front Bioeng Biotechnol 9:632059. https://doi.org/10.3389/fbioe.2021.632059
Mohamed N, Abdelmajid H (2017) Diversity of soil microbial communities from an Iron Mining Area (Oued Zem, Morocco). Mat & Geoenviron 64:21–34. https://doi.org/10.1515/rmzmag-2017-0002
Mohammadi AA, Zarei A, Esmaeilzadeh M et al. (2019) Assessment of heavy metal pollution and human health risks assessment in soils around an industrial zone in Neyshabur, Iran. Biol Trace Elem Res 195:343–352. https://doi.org/10.1007/s12011-019-01816-1
Muller G (1969) Index of geoaccumulation in sediments of the Rhine River. Geojournal 2:108–118
Nannipieri P, Ascher-Jenull J, Ceccherini MT, Pietramellara G, Renella G, Schloter M (2020) Beyond microbial diversity for predicting soil functions: A mini review. Pedosphere 30:5–17. https://doi.org/10.1016/S1002-0160(19)60824-6
Nkongolo KK, Narendrula-Kotha R (2020) Advances in monitoring soil microbial community dynamic and function. J Appl Genet 61:249–263. https://doi.org/10.1007/s13353-020-00549-5
Ogunkunle CO, Fatoba PO (2014) Contamination and spatial distribution of heavy metals in topsoil surrounding a mega cement factory. Atmos Pollut Res 5:270–282. https://doi.org/10.5094/APR.2014.033
Okereafor U, Makhatha M, Mekuto L et al. (2020) Toxic metal implications on agricultural soils, plants, animals, aquatic life and human health. Int J Environ Res Public Health 17:2204. https://doi.org/10.3390/ijerph17072204
Pan X, Zhang S, Zhong Q, Gong G, Wang G, Guo X, Xu X (2020) Effects of soil chemical properties and fractions of Pb, Cd, and Zn on bacterial and fungal communities. Sci Total Environ 715:136904. https://doi.org/10.1016/j.scitotenv.2020.136904
Qasemi M, Afsharnia M, Farhang M, Bakhshizadeh A, Allahdadi M, Zarei A (2018) Health risk assessment of nitrate exposure in groundwater of rural areas of Gonabad and Bajestan, Iran. Environ Earth Sci 77:1–9. https://doi.org/10.1007/s12665-018-7732-8
Qin G, Niu Z, Yu J, Li Z, Ma JY, Xiang P (2020) Soil heavy metal pollution and food safety in China: effects, sources and removing technology. Chemosphere, 129205. https://doi.org/10.1016/j.chemosphere.2020.129205
Quast C, Pruesse E, Yilmaz P et al. (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Quince C, Walker AW, Simpson JT, Loman NJ, Segata N (2017) Shotgun metagenomics, from sampling to analysis. Nat Biotechnol 35:833–844. https://doi.org/10.1038/nbt.3935
Sagova-Mareckova M, Boenigk J, Bouchez A et al. (2020) Expanding ecological assessment by integrating microorganisms into routine freshwater biomonitoring. Water Res 116767. https://doi.org/10.1016/j.watres.2020.116767
Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:348. https://doi.org/10.3389/fmicb.2012.00348
Schloter M, Nannipieri P, Sørensen SJ, van Elsas JD (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10. https://doi.org/10.1007/s00374-017-1248-3
Sekhohola‐Dlamini L, Selvarajan R, Ogola HJO, Tekere M (2021) Community diversity metrics, interactions, and metabolic functions of bacteria associated with municipal solid waste landfills at different maturation stages. MicrobiologyOpen 10:e1118. https://doi.org/10.1002/mbo3.1118
Sepulveda AJ, Hoegh A, Gage JA et al. (2021) Integrating environmental DNA results with diverse data sets to improve biosurveillance of river health. Front Ecol Evol 9:620715. https://doi.org/10.3389/fevo.2021.620715
Shade A (2017) Diversity is the question, not the answer. ISME J 11:1–6. https://doi.org/10.1038/ismej.2016.118
Sheik CS, Mitchell TW, Rizvi FZ et al. (2012) Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PloS One 7:e40059. https://doi.org/10.1371/journal.pone.0040059
Song J, Shen Q, Shi J et al. (2021) Changes in microbial community structure due to chronic trace element concentrations in different sizes of soil aggregates. Environ Pollut 268:115933. https://doi.org/10.1016/j.envpol.2020.115933
Spang A, Poehlein A, Offre P et al. (2012) The genome of the ammonia‐oxidizing C andidatus N itrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14:3122–3145. https://doi.org/10.1111/j.1462-2920.2012.02893.x
Srivastava DS, Cadotte MW, Macdonald AAM, Marushia RG, Mirotchnick N (2012) Phylogenetic diversity and the functioning of ecosystems. Ecol Lett 15:637–648. https://doi.org/10.1111/j.1461-0248.2012.01795.x
Sun XY, Zhou YL, Tan YJ, Wu ZX, Lu P, Zhang GH, Yu FX (2018) Restoration with pioneer plants changes soil properties and remodels the diversity and structure of bacterial communities in rhizosphere and bulk soil of copper mine tailings in Jiangxi province, China. Environ. Sci Pollut Res 25:22106–22119. https://doi.org/10.1007/s11356-018-2244-3
Sun Y, Luo C, Jiang L et al. (2020) Land-use changes alter soil bacterial composition and diversity in tropical forest soil in China. Sci Total Environ 712:136526. https://doi.org/10.1016/j.scitotenv.2020.136526
Touceda-González M, Brader G, Antonielli L et al. (2015) Combined amendment of immobilizers and the plant growth-promoting strain Burkholderia phytofirmans PsJN favours plant growth and reduces heavy metal uptake. Soil Biol Biochem 91:140–150. https://doi.org/10.1016/j.soilbio.2015.08.038
Travassos L (2019) Princípios de carstologia e geomorfologia cárstica. Brasília: ICMBio. 246p.
Wang X, He T, Gen S et al. (2020) Soil properties and agricultural practices shape microbial communities in flooded and rainfed croplands. Appl Soil Ecol 147:103449. https://doi.org/10.1016/j.apsoil.2019.103449
Xiao E, Ning Z, Sun W, Jiang S, Fan W, Ma L, Xiao T (2021) Thallium shifts the bacterial and fungal community structures in thallium mine waste rocks. Environ Pollut 268:115834. https://doi.org/10.1016/j.envpol.2020.115834
Xu XH, Zhang Z, Hu SL, Ruan ZP, Jiang JD, Chen C, Shen ZG (2016) Response of soil bacterial communities to lead and zinc pollution revealed by Illumina Miseq sequencing investigation. Environ Sci Pollut Res 24:666–675. https://doi.org/10.1007/s11356-016-7826-3
Yahaya T, Okpuzor J, Ajayi T (2013) The protective efficacy of selected phytonutrients on liver enzymes of albino rats exposed to cement dust. IOSR J Pharm Biol Sci 8:38–44
Zeng XY, Li SW, Leng Y, Kang XH (2020) Structural and functional responses of bacterial and fungal communities to multiple heavy metal exposure in arid loess. Sci Total Environ 723:138081. https://doi.org/10.1016/j.scitotenv.2020.138081
Zhao X, Huang J, Lu J, Sun Y (2019) Study on the influence of soil microbial community on the long-term heavy metal pollution of different land use types and depth layers in mine. Ecotoxicol Environ Saf 170:218–226. https://doi.org/10.1016/j.ecoenv.2018.11.136
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GAL and WSS contributed to conception and design of the experiments. TACS and MPJ performed the experiments. TACS, WSS and GAL analyzed the data. TACS wrote the draft manuscript. All authors contributed to final version of the manuscript.
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da Costa Silva, T.A., de Paula, M., Silva, W.S. et al. Can moderate heavy metal soil contaminations due to cement production influence the surrounding soil bacterial communities?. Ecotoxicology 31, 134–148 (2022). https://doi.org/10.1007/s10646-021-02494-3
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DOI: https://doi.org/10.1007/s10646-021-02494-3