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RESEARCH ARTICLE

Microbiological indicators as sensitive indicators in the assessment of areas contaminated by heavy metals

Eliane Guimarães Pereira Melloni https://orcid.org/0000-0001-7183-7404 A , Rogério Melloni https://orcid.org/0000-0002-2724-2603 A * , Rocío Pastor-Jáuregui https://orcid.org/0000-0002-1806-6986 B , Antonio Aguilar-Garrido https://orcid.org/0000-0001-7292-9511 C and Francisco José Martín-Peinado https://orcid.org/0000-0002-1389-5531 C
+ Author Affiliations
- Author Affiliations

A Instituto de Recursos Naturais, Universidade Federal de Itajubá, Campus Itajubá, MG, Brazil.

B Departamento de Recursos Hídricos, Universidad Nacional Agraria La Molina, Lima, Peru.

C Departamento de Edafología y Química Agrícola, Universidad de Granada, Granada, Spain.

* Correspondence to: rmelloni@unifei.edu.br

Handling Editor: Nathan Basiliko

Soil Research 61(7) 663-673 https://doi.org/10.1071/SR23012
Submitted: 19 January 2023  Accepted: 26 May 2023   Published: 13 June 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: As one of the world’s largest mining spills, the Aznalcóllar pyrite mine accident in Spain in 1998 resulted in ~45 km2 of agricultural soils polluted by arsenic and heavy metals. The Guadiamar Green Corridor (GGC) helped with soil remediation but residual pollution is still detected 20 years later.

Aims: Several methodologies based on chemical indicators have been used to assess the recovery of these areas. However, simple microbiological indicators (e.g. microbial activity and biomass, and metabolic quotient (qCO2)) are yet to be uesed. The aim of this study was to evaluate areas contaminated by arsenic and heavy metals using microbiological indicators of soil quality.

Methods: We used a systematic random sampling design to collect soil samples from two soil groups with different recovery trajectories. We analysed the total and water-soluble concentrations of arsenic (As), lead (Pb), copper (Cu), and zinc (Zn), the main soil properties, and bioassays including microbial activity and biomass, and metabolic quotient or microbial stress (qCO2).

Key results: Twenty years after the accident, soils with As and Pb concentrations that consistently exceeded regulatory levels had altered soil microbial biomass and functioning. Although overall rates of microbial respiration were not significantly different between polluted soils, microbial biomass was lower and qCO2 was higher in the more polluted than in less polluted soils.

Conclusions: The metabolic quotient and microbial biomass are sensitive indicators in the monitoring over time of soil polluted by arsenic and heavy metals.

Implications: Microbial indicators must be considered in the assessment of potential ecotoxicity and in the evaluation of soil biological properties influencing soil recovery in the long term.

Keywords: Aznalcóllar, microbial biomass, microbiological indicators, metabolic quotient, pyrite mine, soil microbiology, soil recovery, tailings.


References

Adamcová D, Vaverková MD, Bartoň S, Havlíček Z, Břoušková E (2016) Soil contamination in landfills: a case study of a landfill in Czech Republic. Solid Earth 7, 239–247.
Soil contamination in landfills: a case study of a landfill in Czech Republic.Crossref | GoogleScholarGoogle Scholar |

Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122, 121–142.
Role of assisted natural remediation in environmental cleanup.Crossref | GoogleScholarGoogle Scholar |

Aguilar J, Dorronsoro C, Fernández E, Fernández J, García I, Martín F, Simón M (2004) Soil pollution by a pyrite mine spill in Spain: evolution in time. Environmental Pollution 132, 395–401.
Soil pollution by a pyrite mine spill in Spain: evolution in time.Crossref | GoogleScholarGoogle Scholar |

Akmal M, Jianming X (2009) Microbial biomass and bacterial community changes by Pb contamination in acidic soil. Journal of Agricultural and Biological Sciences 1, 30–37.

Anderson JPE (1982) Soil respiration. In ‘Methods of soil analysis: chemical and microbiological properties’. (Eds AL Page, RH Miller, DR Keeney) pp. 831–871. (Soil Science Society of America/American Society of Agronomy: Madison)

Anderson T-H, Domsch KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as ph, on the microbial biomass of forest soils. Soil Biology and Biochemistry 25, 393–395.
The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as ph, on the microbial biomass of forest soils.Crossref | GoogleScholarGoogle Scholar |

Andrade SAL, Silveira APD (2004) Biomassa e atividade microbianas do solo sob influência de chumbo e da rizosfera da soja micorrizada. Pesquisa Agropecuária Brasileira 39, 1191–1198.
Biomassa e atividade microbianas do solo sob influência de chumbo e da rizosfera da soja micorrizada.Crossref | GoogleScholarGoogle Scholar |

Anza M, Garbisu C, Salazar O, Epelde L, Alkorta I, Martínez-Santos M (2021) Acidification alters the functionality of metal polluted soils. Applied Soil Ecology 163, 103920
Acidification alters the functionality of metal polluted soils.Crossref | GoogleScholarGoogle Scholar |

Bi D, Yuan G, Wei J, Xiao L, Feng L, Meng F, Wang J (2019) A Soluble humic substance for the simultaneous removal of cadmium and arsenic from contaminated soils. International Journal of Environmental Research and Public Health 16, 4999
A Soluble humic substance for the simultaneous removal of cadmium and arsenic from contaminated soils.Crossref | GoogleScholarGoogle Scholar |

BOJA – Boletín Oficial de la Junta de Andalucía (2015) Decreto 18/2015, de 27 de enero, por el que se aprueba el reglamento que regula el régimen aplicable a los suelos contaminados. Consejería de Medio Ambiente y Ordenación del Territorio. Junta de Andalucía, Spain.

Chander K, Joergensen RG (2001) Decomposition of 14C glucose in two soils with different amounts of heavy metal contamination. Soil Biology and Biochemistry 33, 1811–1816.
Decomposition of 14C glucose in two soils with different amounts of heavy metal contamination.Crossref | GoogleScholarGoogle Scholar |

CMA – Consejería de Medio Ambiente (2003) Ciencia y Restauración del Río Guadiamar. PICOVER 1998–2002. Consejería de Medio Ambiente, Junta de Andalucía, Sevilla.

Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387, 253–260.
The value of the world’s ecosystem services and natural capital.Crossref | GoogleScholarGoogle Scholar |

Dias-Júnior HE, Moreira FMS, Siqueira JO, Silva R (1998) Metais pesados, densidade e atividade microbiana em solo contaminado por rejeitos de indústria de zinco. Revista Brasileira de Ciência do Solo 22, 631–640.
Metais pesados, densidade e atividade microbiana em solo contaminado por rejeitos de indústria de zinco.Crossref | GoogleScholarGoogle Scholar |

Domínguez MT, Alegre JM, Madejón P, Madejón E, Burgos P, Cabrera F, Marañón T, Murillo JM (2016) River banks and channels as hotspots of soil pollution after large-scale remediation of a river basin. Geoderma 261, 133–140.
River banks and channels as hotspots of soil pollution after large-scale remediation of a river basin.Crossref | GoogleScholarGoogle Scholar |

Doran JW, Parkin TB (1994) Defining and assessing soil quality. In ‘Defining soil quality for a sustainable environment’. (Eds JW Doran, DC Coleman, DF Bezdicek, BA Stewart). pp. 1–21. (SSSA Special Publication Number: Madison)

Doran JW, Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Applied Soil Ecology 15, 3–11.
Soil health and sustainability: managing the biotic component of soil quality.Crossref | GoogleScholarGoogle Scholar |

Epelde L, Becerril JM, Mijangos I, Garbisu C (2009) Evaluation of the efficiency of a phytostabilization process with biological indicators of soil health. Journal of Environmental Quality 38, 2041–2049.
Evaluation of the efficiency of a phytostabilization process with biological indicators of soil health.Crossref | GoogleScholarGoogle Scholar |

Epelde L, Lanzén A, Blanco F, Urich T, Garbisu C (2015) Adaptation of soil microbial community structure and function to chronic metal contamination at an abandoned Pb-Zn mine. FEMS Microbiology Ecology 91, 1–11.
Adaptation of soil microbial community structure and function to chronic metal contamination at an abandoned Pb-Zn mine.Crossref | GoogleScholarGoogle Scholar |

Ferreira AS, Camargo FAO, Vidor C (1999) Utilização de microondas na avaliação da biomassa microbiana do solo. Revista Brasileira de Ciência do Solo 23, 991–996.
Utilização de microondas na avaliação da biomassa microbiana do solo.Crossref | GoogleScholarGoogle Scholar |

Fidelis RR, Santos Alexandrino CM, Silva DB, Alves Sugai MA, Silva RR (2016) Indicadores biológicos de qualidade do solo em culturas intercalares ao pinhão manso. Brazilian Journal of Applied Technology for Agricultural Science 9, 87–95.

Insam H, Hutchinson TC, Reber HH (1996) Effects of heavy metal stress on the metabolic quotient of the soil microflora. Soil Biology and Biochemistry 28, 691–694.
Effects of heavy metal stress on the metabolic quotient of the soil microflora.Crossref | GoogleScholarGoogle Scholar |

IUSS (International Union of Soil Sciences) Working Group WRB (2015) World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No 106. FAO, Rome, Italy.

Jia J, Bai J, Xiao R, Tian S, Wang D, Wang W, Zhang G, Cui H, Zhao Q (2022) Fractionation, source, and ecological risk assessment of heavy metals in cropland soils across a 100-year reclamation chronosequence in an estuary, South China. Science of The Total Environment 807, 151725
Fractionation, source, and ecological risk assessment of heavy metals in cropland soils across a 100-year reclamation chronosequence in an estuary, South China.Crossref | GoogleScholarGoogle Scholar |

Kaschuk G, Alberton O, Hungria M (2010) Three decades of soil microbial biomass studies in Brazilian ecosystems: lessons learned about soil quality and indications for improving sustainability. Soil Biology and Biochemistry 42, 1–13.
Three decades of soil microbial biomass studies in Brazilian ecosystems: lessons learned about soil quality and indications for improving sustainability.Crossref | GoogleScholarGoogle Scholar |

MAPA (1994) Métodos Oficiales de Análisis. Tomo III Secretaría General Técnica del Ministerio de Agricultura, Pesca y Alimentación (MAPA), Madrid, Spain.

Martín Peinado FJ, Romero-Freire A, García Fernández I, Sierra Aragón M, Ortiz-Bernad I, Simón Torres M (2015) Long-term contamination in a recovered area affected by a mining spill. Science of The Total Environment 514, 219–223.
Long-term contamination in a recovered area affected by a mining spill.Crossref | GoogleScholarGoogle Scholar |

Nakamaru YM, Martín Peinado FJ (2017) Effect of soil organic matter on antimony bioavailability after the remediation process. Environmental Pollution 228, 425–432.
Effect of soil organic matter on antimony bioavailability after the remediation process.Crossref | GoogleScholarGoogle Scholar |

Nielsen MN, Winding A (2002) Microorganisms as indicators of soil health. National Environmental Research Institute, Denmark. Technical Report 388.

Nikolic N, Kostic L, Djordjevic A, Nikolic M (2011) Phosphorus deficiency is the major limiting factor for wheat on alluvium polluted by the copper mine pyrite tailings: a black box approach. Plant and Soil 339, 485–498.
Phosphorus deficiency is the major limiting factor for wheat on alluvium polluted by the copper mine pyrite tailings: a black box approach.Crossref | GoogleScholarGoogle Scholar |

OECD – Organization for Economic Cooperation and Development (2004) ‘Environmental performance reviews: Spain 2004.’ (OECD Publications: Cedex 16, France)

Ohya H, Fujiwara S, Komai Y, Yamaguchi M (1988) Microbial biomass and activity in urban soils contaminated with Zn and Pb. Biology and Fertility of Soils 6, 9–13.
Microbial biomass and activity in urban soils contaminated with Zn and Pb.Crossref | GoogleScholarGoogle Scholar |

Oijagbe IJ, Abubakar BY, Edogbanya PRO, Suleiman MO, Olorunmola JB (2019) Effects of heavy metals on soil microbial biomass carbon. MOJ Biology and Medicine 4, 30–32.
Effects of heavy metals on soil microbial biomass carbon.Crossref | GoogleScholarGoogle Scholar |

O’Neill P (1995) Arsenic. In ‘Heavy metals in soils’. (Ed. BJ Alloway) pp. 105–121. (Blackie Academic & Professional: London)

Pardo T, Clemente R, Epelde L, Garbisu C, Bernal MP (2014) Evaluation of the phytostabilisation efficiency in a trace elements contaminated soil using soil health indicators. Journal of Hazardous Materials 268, 68–76.
Evaluation of the phytostabilisation efficiency in a trace elements contaminated soil using soil health indicators.Crossref | GoogleScholarGoogle Scholar |

Park JH, Lamb D, Paneerselvam P, Choppala G, Bolan N, Chung J-W (2011) Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. Journal of Hazardous Materials 185, 549–574.
Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils.Crossref | GoogleScholarGoogle Scholar |

Pastor-Jáuregui R, Paniagua-López M, Martínez-Garzón J, Martín-Peinado F, Sierra-Aragón M (2020) Evolution of the residual pollution in soils after bioremediation treatments. Applied Sciences 10, 1006
Evolution of the residual pollution in soils after bioremediation treatments.Crossref | GoogleScholarGoogle Scholar |

Pastor-Jáuregui R, Paniagua-López M, Aguilar-Garrido A, Martín-Peinado F, Sierra-Aragón M (2021) Long-term assessment of remediation treatments applied to an area affected by a mining spill in Spain. Land Degradation & Development 32, 2481–2492.
Long-term assessment of remediation treatments applied to an area affected by a mining spill in Spain.Crossref | GoogleScholarGoogle Scholar |

Paul E (2014) ‘Soil microbiology, ecology and biochemistry.’ (Academic Press, Elsevier)

Romero-Freire A, García Fernández I, Simon Torres M, Martínez Garzón FJ, Martín Peinado FJ (2016) Long-term toxicity assessment of soils in a recovered area affected by a mining spill. Environmental Pollution 208, 553–561.
Long-term toxicity assessment of soils in a recovered area affected by a mining spill.Crossref | GoogleScholarGoogle Scholar |

Sierra Aragón M, Nakamaru YM, García-Carmona M, Martínez Garzón FJ, Martín Peinado FJ (2019) The role of organic amendment in soils affected by residual pollution of potentially harmful elements. Chemosphere 237, 124549
The role of organic amendment in soils affected by residual pollution of potentially harmful elements.Crossref | GoogleScholarGoogle Scholar |

Simón M, Martín F, Ortiz I, García I, Fernández J, Fernández E, Dorronsoro C, Aguilar J (2001) Soil pollution by oxidation of tailings from toxic spill of a pyrite mine. Science of The Total Environment 279, 63–74.
Soil pollution by oxidation of tailings from toxic spill of a pyrite mine.Crossref | GoogleScholarGoogle Scholar |

Simón M, García I, Martín F, Díez M, del Moral F, Sánchez JA (2008) Remediation measures and displacement of pollutants in soils affected by the spill of a pyrite mine. Science of The Total Environment 407, 23–39.
Remediation measures and displacement of pollutants in soils affected by the spill of a pyrite mine.Crossref | GoogleScholarGoogle Scholar |

Sposito G, Lund LJ, Chang AC (1982) Trace metal chemistry in arid-zone field soils amended with sewage sludge: I. Fractionation of Ni, Cu, Zn, Cd, and Pb in solid phases. Soil Science Society of America Journal 46, 260–264.
Trace metal chemistry in arid-zone field soils amended with sewage sludge: I. Fractionation of Ni, Cu, Zn, Cd, and Pb in solid phases.Crossref | GoogleScholarGoogle Scholar |

Stefanowicz AM, Kapusta P, Zubek S, Stanek M, Woch MW (2020) Soil organic matter prevails over heavy metal pollution and vegetation as a factor shaping soil microbial communities at historical Zn–Pb mining sites. Chemosphere 240, 124922
Soil organic matter prevails over heavy metal pollution and vegetation as a factor shaping soil microbial communities at historical Zn–Pb mining sites.Crossref | GoogleScholarGoogle Scholar |

Tai Y, Li Z, Mcbride MB (2016) Natural attenuation of toxic metal phytoavailability in 35-year-old sewage sludge-amended soil. Environmental Monitoring and Assessment 188, 241
Natural attenuation of toxic metal phytoavailability in 35-year-old sewage sludge-amended soil.Crossref | GoogleScholarGoogle Scholar |

US EPA – US Environmental Protection Agency (1998) Field portable x-ray fluorescence spectrometry for the determination of elemental concentrations in soil and sediment. Method 6200. US EPA.

Zhao X, Sun Y, Huang J, Wang H, Tang D (2020) Effects of soil heavy metal pollution on microbial activities and community diversity in different land use types in mining areas. Environmental Science and Pollution Research 27, 20215–20226.
Effects of soil heavy metal pollution on microbial activities and community diversity in different land use types in mining areas.Crossref | GoogleScholarGoogle Scholar |

Zornoza R, Acosta JA, Bastida F, Domínguez SG, Toledo DM, Faz A (2015) Identification of sensitive indicators to assess the interrelationship between soil quality, management practices and human health. Soil 1, 173–185.
Identification of sensitive indicators to assess the interrelationship between soil quality, management practices and human health.Crossref | GoogleScholarGoogle Scholar |