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Microbial Activities Response to Contamination in Soil and Sediments Rich in As Surrounding an Industrial Gold Mine

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Abstract

Gold mines are widely recognized as important sources of arsenic (As) pollution and this work proposes the use of in situ microbial community enzymatic response to assess the risk of As in soil and sediments surrounding “Morro do Ouro,” the largest industrial gold mine in Brazil. Bacterial community exposed to high metals concentrations deviates energy from growth to cell maintenance modifying enzymatic activity response. Even if the number of bacterial cells presented in soil and sediment samples was in the same order of 107 cell cm−3, it declines in sediment samples closer to a mining area. Dehydrogenase activity (DHA) showed the same trend, suggesting inhibition by toxic effect of metals, while esterase activities (EST) behaved in the opposite way, representative of increasing energy demand by the community under environmental stress. The Quality Ratio (QR) index for environmental risk assessment was applied to integrate geochemical (grain size, total organic carbon contents, and metals as indicators of complex contamination) and microbial parameters (DHA—energy production into cell and EST—hydrolase organic matter outside the cell membrane). QR indicated that the risk associated with soil and sediment is driven by As levels and decreases from the mine facilities.

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References

  • Allison, S. D., & Martiny, J. B. H. (2008). Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences, 105, 11512–11519. https://doi.org/10.1073/pnas.0801925105.

    Article  Google Scholar 

  • ATSDR - Agency for Toxic Substances and Disease Registry - US. (2007) Agency for toxic substances and disease registry. Toxicological profile for arsenic. Atlanta

  • Babich, H., & Stotzky, G. (1985). Heavy metal toxicity to microbe-mediated ecologic processes: a review and potential application to regulatory policies. Environmental Research, 36, 111–137.

    Article  CAS  Google Scholar 

  • Bidone, E. D., Castilhos, Z. C., Bertolino, L. C., Santos, M. C. B., Silva, R. S. V., & Cesar, R. G. (2014). Arsenic in soils and sediments from Paracatu, Brazil. In M. I. Litter, H. B. Nicolli, J. M. Meichtry, N. Quici, J. Bundschuh, P. Bhattacharya, & R. Naidu (Eds.), V international congress of arsenic in the environment – As2014 (pp. 113–115). Proceedings: Buenos Aires, Argenina, CRC Press-Taylor and Francis Group.

    Google Scholar 

  • Bidone, E. D., Castilhos, Z. C., Cesar, R. G., Santos, M. C., Sierpe, R., & Ferreira, M. (2016). Hydrogeochemistry of arsenic pollution in watersheds influenced by gold mining activities in Paracatu (Minas Gerais State, Brazil). Environmental Science and Pollution Research, 23(9), 8546–8555. https://doi.org/10.1007/s11356-016-6089-3.

    Article  CAS  Google Scholar 

  • Bidone, E. D., Cesar, R. G., Santos, M. C., Sierpe, R., Silva-Filho, E. V., Kutter, V., et al. (2018). Mass balance of arsenic fluxes in rivers impacted by gold mining activities in Paracatu (Minas Gerais State, Brazil). Environmental Science and Pollution Research, 25, 9085–9100. https://doi.org/10.1007/s11356-018-1215-z.

    Article  CAS  Google Scholar 

  • Bowell, R. J., Alpers, C. H., Jamieson, H. E., Nordstrom, D. K., & Majzlan, J. (2014). The environmental geochemistry of arsenic—an overview. Reviews in Mineralogy & Geochemistry, 79, 1–16.

    Article  Google Scholar 

  • Busch, J., Nascimento, J. R., Magalhães, A. C. R., Dutilh, B. E., & Dinsdale, E. (2015). Copper tolerance and distribution of epibiotic bacteria associated with giant kelp Macrocystis pyrifera in southern California. Ecotoxicology, 24, 1131–1140. https://doi.org/10.1007/s10646-015-1460-6.

    Article  CAS  Google Scholar 

  • Caruso, G., La Ferla, R., Azzaro, M., et al. (2016). Microbial assemblages for environmental quality assessment: knowledge, gaps and usefulness in the European marine strategy framework directive. Critical Reviews in Microbiology, 42(6), 883–904. https://doi.org/10.3109/1040841X.2015.1087380.

    Article  Google Scholar 

  • CETEM - Centro de Tecnologia Mineral (2018) Relatório Final- Ambiental “Avaliação da Contaminação Ambiental por Arsenio em Paracatu-MG”. Available at: <https://www.cetem.gov.br/images/gestao/relatorio_paracatu_ambiental_2018_cetem.pdf>. Accessed June 2020.

  • CONAMA - Conselho Nacional de Meio Ambiente (2009) Resolução 420. Available at: <http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=506>. Accessed September 2019.

  • CONAMA - Conselho Nacional do Meio Ambiente (2012) Resolução 454. Available at: <http://www2.mma.gov.br/port/conama/legiabre. cfm?codlegi=693>. Accessed September 2019.

  • Cornall, A., Rose, A., Streten, C., McGuinness, K., Parry, D., & Gibb, K. (2016). Molecular screening of microbial communities for candidate indicators of multiple metal impacts in marine sediments from northern Australia. Environmental Toxicology and Chemistry, 35, 468–484. https://doi.org/10.1002/etc.3205.

    Article  CAS  Google Scholar 

  • Craw, D., & Bowell, R. J. (2014). The characterization of arsenic in mine waste. Reviews in Mineralogy & Geochemistry, 79, 473–505.

    Article  Google Scholar 

  • Decho, A. W. (2000). Microbial biofilms in intertidal systems: an overview. Continental Shelf Research, 20, 1257–1273.

    Article  Google Scholar 

  • Demaison, G. J., & Moore, G. T. (1980). Anoxic environment and oil source bed genesis. Organic Geochemistry, 2, 9–31.

    Article  CAS  Google Scholar 

  • EMBRAPA - EMPRESA BRASILEIRA DE PESQUISA AGROPECUÁRIA (1997). Manual de métodos de análises de solo. Rio de Janeiro, RJ, p 212.

  • Fabiano, M., Danovaro, R., Magi, E., & Mazzucotelli, A. (1994). Effects of heavy metals on benthic bacteria in coastal marine sediments: a field result. Marine Pollution Bulletin, 28, 18–23. https://doi.org/10.1016/0025-326X(94)90181-3.

    Article  CAS  Google Scholar 

  • Fiori, C. S. F., Rodrigues, A. P. C., Santelli, R. E., et al. (2013). Ecological risk index for aquatic pollution control: a case study of coastal water bodies from the Rio de Janeiro state, southeastern Brazil. Geochimica Brasiliensis, 2, 24–36. https://doi.org/10.5327/Z0102-9800201300010003.

    Article  CAS  Google Scholar 

  • Flemming, H. C. (2016). EPS—Then and now. Microorganisms, 4, 41. https://doi.org/10.3390/microorganisms4040041.

    Article  CAS  Google Scholar 

  • Flemming, H. C., & Wingender, J. (2010). The biofilm matrix. Nature Reviews Microbiology, 19, 139–150. https://doi.org/10.1038/nrmicro2415.

    Article  CAS  Google Scholar 

  • Guo, W., Liu, X., Liu, Z., & Li, G. (2010). Pollution and potential ecological risk evaluation of heavy metals in the sediments around Dongjiang Harbor, Tianjin. Procedia Environmental Sciences, 2, 729–736. https://doi.org/10.1016/j.proenv.2010.10.084.

    Article  Google Scholar 

  • Hakanson, L. (1980). An ecological risk index for aquatic pollution control. A sedimentological approach. Water Research, 14, 975–1001. https://doi.org/10.1016/0043-1354(80)90143-8.

    Article  Google Scholar 

  • Harrison, J. J., Ceri, H., & Turner, R. J. (2007). Multimetal resistance and tolerance in microbial biofilms. Nature Reviews Microbiology, 5, 928–938. https://doi.org/10.1038/nrmicro1774.

    Article  CAS  Google Scholar 

  • Henderson, R. D. (2006). Paracatu mine technical report. Kinross Gold Corporation, Technical Report.

  • IBGE (2010) Censo Demográfico – Características Gerais da População. Resultados da Amostra. IBGE, 2012. Available at: https://censo2010.ibge.gov.br/resultados.html. Accessed September 2019.

  • Meyer-Reil, L. A., & Köster, M. (2000). Eutrophication of marine waters: effects on benthic microbial communities. Marine Pollution Bulletin, 41, 255–263.

    Article  CAS  Google Scholar 

  • Miao, L., Wang, C., Hou, J., Wang, P., Ao, Y., Li, Y., Yao, Y., Lv, B., Yang, Y., You, G., Xu, Y., & Gu, Q. (2017). Response of wastewater biofilm to CuO nanoparticle exposure in terms of extracellular polymeric substances and microbial community structure. Science of the Total Environment, 579, 588–597. https://doi.org/10.1016/j.scitotenv.2016.11.056.

    Article  CAS  Google Scholar 

  • Möller, J. C., Batelochi, M., Akiti, Y., Maxwell, S., & Borges, A. L. (2001). Geologia e caracterização dos recursos minerais de Morro do Ouro, Paracatu, Minas Gerais. In C. P. Pinto & M. A. Martins-Neto (Eds.), Bacia do São Francisco: geologia e recursos naturais (pp. 199–234). SBG: Belo Horizonte.

    Google Scholar 

  • Moreau, J. W., Gionfriddo, C. M., Krabbenhoft, D. P., Ogorek, J. M., DeWild, J. F., Aiken, G. R., & Roden, E. E. (2015). The effect of natural organic matter on mercury methylation by Desulfobulbus propionicus 1pr3. Frontiers in Microbiology, 6. https://doi.org/10.3389/fmicb.2015.01389.

  • Mustapha, M. U., & Halimoon, N. (2015). Microorganisms and biosorption of heavy metals in the environment: a review paper. Journal of Microbial & Biochemical Technology, 7, 253–256. https://doi.org/10.4172/1948-5948.1000219.

    Article  CAS  Google Scholar 

  • Nascimento, J. R (2018). Integração de Indicadores Geoquímicos e Microbiológicos na Avaliação da Disposição Oceânica e Continental de Sedimentos Dragados da Baía de Guanabara – RJ, brasil. PhD. Thesis, Universidade Federal Fluminense.

  • Nascimento, J. R., Silveira, A. E. F., Bidone, E. D., & Sabadini-Santos, E. (2019). Microbial community activity in response to multiple contaminant exposure: a feasible tool for sediment quality assessment. Environmental Monitoring and Assessment, 191, 392. https://doi.org/10.1007/s10661-019-7532-y.

    Article  Google Scholar 

  • Nogales, B., Lanfranconi, M. P., Piña-Villalonga, J. M., & Bosch, R. (2011). Anthropogenic perturbations in marine microbial communities. FEMS Microbiology Reviews, 35, 275–298. https://doi.org/10.1111/j.1574-6976.2010.00248.x.

    Article  CAS  Google Scholar 

  • Obbard, J. P., Sauerbeck, D., & Jones, K. C. (1994). Dehydrogenase activity of the microbial biomass in soils from a field experiment amended with heavy metal contaminated sewage sludges. Science of the Total Environment, 142, 157–162. https://doi.org/10.1016/0048-9697(94)90323-9.

    Article  CAS  Google Scholar 

  • Odum, E. P. (1985). Trends expected in stressed ecosystems. Bioscience, 35, 419–422. https://doi.org/10.2307/1310021.

    Article  Google Scholar 

  • Relexans, J. C., Lin, R. G., Castel, J., et al. (1992). Response of biota to sedimentary organic-matter quality of the west Gironde mud patch, Bay of Biscay (France). Oceanologica Acta, 15, 639–649.

    CAS  Google Scholar 

  • Sabadini-Santos, E., Silva, T. S., Lopes-Rosa, T. D., et al. (2014). Microbial activities and bioavailable concentrations of Cu, Zn, and Pb in sediments from a tropic and eutrothicated bay. Water, Air, and Soil Pollution, 225. 10.1007/s11270-014-1949-2.

  • Saxena, G., Marzinelli, E. M., Naing, N. N., He, Z., Liang, Y., Tom, L., Mitra, S., Ping, H., Joshi, U. M., Reuben, S., Mynampati, K. C., Mishra, S., Umashankar, S., Zhou, J., Andersen, G. L., Kjelleberg, S., & Swarup, S. (2015). Ecogenomics reveals metals and land-use pressures on microbial communities in the waterways of a megacity. Environmental Science & Technology, 49, 1462–1471. https://doi.org/10.1021/es504531s.

    Article  CAS  Google Scholar 

  • Silveira, A. E. F., Nascimento, J. R., Sabadini-santos, E., & Bidone, E. D. (2017). Screening-level risk assessment applied to dredging of polluted sediments from. Marine Pollution Bulletin, 118, 368–375. https://doi.org/10.1016/j.marpolbul.2017.03.016.

    Article  CAS  Google Scholar 

  • Sobolev, D., & Begonia, M. F. T. (2008). Effects of heavy metal contamination upon soil microbes: lead-induced changes in general and denitrifying microbial communities as evidenced by molecular markers. International Journal of Environmental Research and Public Health, 5, 450–456. https://doi.org/10.3390/ijerph5050450.

    Article  CAS  Google Scholar 

  • Stubberfield, L. C. E., & Shaw, P. J. A. (1990). A comparison of tetrazolium reduction and FDA\nhydrolysis with other measures of microbial activity. Journal of Microbiological Methods, 12, 151–162.

    Article  CAS  Google Scholar 

  • Trevors, J. T., Mayfield, C. I., & Inniss, W. E. (1982). Measurement of electron transport system (ETS) activity in soil. Microbial Ecology, 8, 163–168. https://doi.org/10.1007/BF02010449.

    Article  CAS  Google Scholar 

  • USEPA (2004). Innovative technology verification report: field measurement technology for mercury in soil and sediment. Ohio Lumex’s RA-915þ/RP-91C mercury analyser. EPA/600/R-03/147. 86.

  • USEPA (2007). Method 3051A: microwave assisted acid digestion of sediments, sludges, soils, and oils. 1–30.

  • Van Beelen, P., & Doelman, P. (1997). Significance and application of microbial toxicity tests in assessing ecotoxicological risks of contaminants in soil and sediment. Chemosphere, 34, 455–499. https://doi.org/10.1016/S0045-6535(96)00388-8.

    Article  Google Scholar 

  • Waite, C. C. D. C., da Silva, G. O. A., Bitencourt, J. A. P., Sabadini-Santos, E., & Crapez, M. A. C. (2016). Copper and lead removal from aqueous solutions by bacterial consortia acting as biosorbents. Marine Pollution Bulletin, 109, 386–392. https://doi.org/10.1016/j.marpolbul.2016.05.044.

    Article  CAS  Google Scholar 

  • Whitman, W. B., Coleman, D. C., & Wiebe, W. J. (1998). Prokaryotes: the unseen majority. Proceedings of the National Academy of Sciences, 95(12), 6578–6583. https://doi.org/10.1073/pnas.95.12.6578.

    Article  CAS  Google Scholar 

  • WHO – World Health Organization (2018) International programme on chemical safety. https://www.who.int/ipcs/en/ Accessed 26 April 2018.

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Acknowledgments

The authors are thankful to Centro de Tecnologia Mineral (CETEM) for the technical and logistic support. The authors also appreciate the scientific discussion with Dr. Mirian Crapez from the Laboratorio de Processos em Ecologia Microbiana, Universidade Federal Fluminense.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.

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Correspondence to Elisamara Sabadini-Santos.

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Sabadini-Santos, E., Castilhos, Z.C. & Bidone, E.D. Microbial Activities Response to Contamination in Soil and Sediments Rich in As Surrounding an Industrial Gold Mine. Water Air Soil Pollut 231, 366 (2020). https://doi.org/10.1007/s11270-020-04734-4

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