Microbial indicators of soil health as tools for ecological risk assessment of a metal contaminated site in Brazil

Applied Soil Ecology

Volumn 59, Issue , 2012, Pages 96-105

  Niemeyer, Júlia Carina ^a,b   Lolata, Giovana Bortoti ^c   Carvalho, Gabriel Martins de ^d   Da Silva, Eduardo Mendes ^b   Sousa, José Paulo ^a   Nogueira, Marco Antonio ^c,e  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^c STATE UNIVERSITY OF LONDRINA   (Brazil)

^d DEPARTAMENTO DE CIÊNCIAS BIOLÓGICAS   (Brazil)

^e EMBRAPA CERRADOS   (Brazil)

Author keywords

Metals; Microbial activity; Microbial biomass; Soil enzymes; Soil quality

Indexed keywords

EID: 84860639295     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2012.03.019     Document Type: Article

References (78)

1. Alkorta I., Aizpurua A., Riga P., Albizu I., Amezaga I., Garbisu C. Soil enzyme activities as biological indicators of soil health. Rev. Environ. Health 2003, 18:65-73.
2. 2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol. Biochem. 1993, 25:393-395.
3. Anderson J.M., Ingram J.S.I. Tropical Soil Biology and Fertility: A Handbook of Methods 1993, CAB International, Wallingford.
4. Anjos, J.S.A., 2003. Avaliação da eficiência de uma zona alagadiça (wetland) no 536 controle da poluição por metais pesados: o caso da Plumbum em Santo Amaro da 537 Purificação/BA. Thesis. University of São Paulo, Brazil.
5. Araújo A.S.F., Monteiro R.T.R., Abarkeli R.B. Effect of glyphosate on the microbial activity of two Brazilian soils. Chemosphere 2003, 52:799-804.
6. Balota E.L., Kanashiro M., Colozzi Filho A., Andrade D.S., Dick R.P. Soil enzyme activities under long-term tillage and crop rotation systems in subtropical agro-ecosystems. Braz. J. Microbiol. 2004, 35:300-306.
7. Bastida F., Moreno J.L., Hernández T., García C. Microbiological activity in a soil 15 years after its devegetation. Soil Biol. Biochem. 2006, 38:2503-2507.
8. Bardgett R.D., Saggar S. Effects of heavy metal contamination on the short-term decomposition of labeled [14C] glucose in a pasture soil. Soil Biol. Biochem. 1994, 26:727-733.
9. Begonia M.T., Begonia G.B., Miler G., Giliard D., Young C. Phosphatase activity and populations of microorganisms from cadmium- and lead-contaminated soils. Bull. Environ. Contam. Toxicol. 2004, 73:1025-1032.
10. Brookes P.C., Landman A., Pruden G., Jenkinson D.S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 1985, 17:837-842.
11. Broos K., Mertens J., Smolders E. Toxicity of heavy metals in soil assessed with various soil microbial and plant growth assays: a comparative study. Environ. Toxicol. Chem. 2005, 24:634-640.
12. Casida L.E., Klein D.A., Santoro T. Soil dehydrogenase activity. Soil Sci. 1964, 98:371-376.
13. Castaldi S., Rutigliano F.A., Virzo S.A. Suitability of soil microbial parameters as indicators of heavy metal pollution. Water Air Soil Pollut. 2004, 158:21-35.
14. Chen G., Zhu H., Zhang Y. Soil microbial activities and carbon and nitrogen fixation. Res. Microbiol. 2003, 154:393-398.
15. Carvalho F.M., Neto A.M.S., Tavares T.M., Costa A.C.A., Chaves C.R., Nascimento L.D., Reis M.A. Chumbo no sangue de crianças e passivo ambiental de uma fundição de chumbo no Brasil. Pan. Am. J. Public Health 2003, 13:19-23.
16. Chapman H.D., Pratt P.F. Methods of Analysis for Soils, Plants and Waters 1978, University of California, Division of Agricultural Science.
17. Clemente R., de la Fuente C., Moral R., Bernal M.P. Changes in microbial biomass parameters of a heavy metal-contaminated calcareous soil during a field remediation experiment. J. Environ. Qual. 2007, 36:1137-1144.
18. Costa, A.C.A., 2001. Avaliação de alguns efeitos do passivo ambiental de uma metalurgia de chumbo em Santo Amaro da Purificação, Bahia. Dissertation. Federal University of Bahia.
19. Delorme T.A., Gagliardi J.V., Angle J.S., Chaney R.L. Influence of the zinc hyperaccumulator Thlaspi caerulescens J. & C. Presl. and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can. J. Microbiol. 2001, 47:773-776.
20. Dias-Junior H.E., Moreira F.M.S., Siqueira J.O., Silva R. Metais pesados, densidade e atividade microbiana em solo contaminado por rejeitos de indústria de zinco. Rev. Bras. Cienc. Solo 1998, 22:631-640.
21. Edwards C.A. Assessing the effects of environmental pollutants on soil organisms, communities, processes and ecosystems. Eur. J. Soil Biol. 2002, 38:225-231.
22. Epelde L., Hernández-allica J., Becerril J.M., Garbisu C. Assessment of the efficiency of a metal phytoremediation process with biological indicators of soil health. Difpolmine Conference 2006.
23. Epelde L., Becerril J.M., Kowalchuk G.A., Deng Y., Zhou J., Garbisu C. Impact of metal pollution and Thlaspi caerulescens growth on soil microbial communities. Appl. Environ. Microbiol. 2010, 76:7843-7853.
24. Fliessbach A., Martens A., Reber H.H. Soil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage-sludge. Soil Biol. Biochem. 1994, 26:1201-1205.
25. Frankenberger W.T., Tabatabai M.A. Asparaginase activity of soils. Biol. Fert. Soils 1991, 11:6-12.
26. Giller K.E., Witter E., McGrath S.P. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol. Biochem. 1998, 30:1389-1414.
27. Giller K.E., Witter E., McGrath S.P. Heavy metals and soil microbes. Soil Biol. Biochem. 2009, 41:2031-2037.
28. Gregorich E.G., Carter M.R., Angers D.A., Monreal C.M., Ellert B.H. Towards a minimum data set to assess soil organic matter quality in agricultural soils. Can. J. Soil Sci. 1994, 74:367-385.
29. Gülser F., Erdogan E. The effects of heavy metal pollution on enzyme activities and basal soil respiration of roadside soils. Environ. Monit. Assess. 2008, 145:127-133.
30. Hernández-Allica J., Becerril J.M., Zárate O., Garbisu C. Assessment of the efficiency of a metal phytoextraction process with biological indicators of soil health. Plant Soil 2006, 281:147-158.
31. Houba V.J.G., Lexmond T.M., Novozamsky J.J., Van Der Lee J. State of the art and future developments in soil analysis for bioavailability assessment. Sci. Total Environ. 1996, 178:21-28.
32. ISO, 1994. Soil quality, Determination of pH. International Organization for Standardization, Guideline no. 10390. Geneva, Switzerland.
33. ISO, 1994. Soil quality, Determination of effective cation exchange capacity and base saturation level using barium chloride solution. International Organization for Standardization, Guideline no. 11260. Geneva, Switzerland.
34. ISO, 1998. Soil quality, Determination of the water-retention characteristic - Laboratory methods. International Organization for Standardization, Guideline no. 11274. Geneva, Switzerland.
35. Janssens T.K., Lopéz R., Mariën J., Timmermans M.J., Montagne-Wajer K., van Straalen N.M., Roelofs D. Comparative population analysis of metallothionein promoter alleles suggests stress-induced microevolution in the field. Environ. Sci. Technol. 2008, 42:3873-3878.
36. Jiang J., Wu L., Li N., Luo Y., Liu L., Zhao Q., Zhang L., Christie P. Effects of multiple heavy metal contamination and repeated phytoextraction by Sedum plumbizincicola on soil microbial properties. Eur. J. Soil Biol. 2010, 46:18-26.
37. Kaschuk K., Alberton O., Hungria M. Three decades of soil microbial biomass studies in Brazilian ecosystems: lessons learned about soil quality and indications for improving sustainability. Soil Biol. Biochem. 2010, 42:1-13.
38. Kelly J.J., Haggblom M.M., Tate R.L. Effects of heavy metal contamination and remediation of soil microbial communities in the vicinity of a zinc smelter as indicated by analysis of microbial community phospholipid fatty acid profiles. Biol. Fert. Soils 2003, 38:65-71.
39. Khan K., Joergensen R. Decomposition of heavy metal contaminated nettles (Urtica dioica L.) in soils subjected to heavy metal pollution by river sediments. Chemosphere 2006, 65:981-987.
40. Krave A.S., van Straalen N.M., van Verseveld H.W. Potential nitrification and factors influencing nitrification in pine forest and agricultural soils in Central Java, Indonesia. Pedobiologia 2002, 46:573-594.
41. Kuperman R.G., Carreiro M.M. Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem. Soil Biol. Biochem. 1997, 29:179-190.
42. Lejon D.P.H., Pascault N., Ranjard L. Differential copper impact on density, diversity and resistance of adapted culturable bacterial populations according to soil organic status. Eur. J. Soil Biol. 2010, 46:168-174.
43. LNEC Solos - Análise granulométrica por peneiração húmida. LNEC-E 239 1970, Laboratório Nacional de Engenharia Civil, Lisboa, Portugal.
44. Machado S.L., Ribeiro L.D., Kiperstok A., Botelho M.A.B., Carvalho M.F. Diagnóstico da contaminação por metais pesados em Santo Amaro-BA. Eng. Sanit. Ambient. 2004, 9:140-155.
45. Machado, S.L., Carvalho, M.F., Motta, A.R.P., Delgado, C.W.C., Anjos, J.A.S.A., Ribeiro, L.D., First, A.K., Sánchez, L., 2002. Relatório final do projeto Purifica - Proposta para remediação de áreas degradadas pela atividade extrativa de chumbo em Santo Amaro da Purificação-BA.
46. McGrath S.P. Bioavailability of metals to soil microbes. Bioavailability of Metals in Terrestrial Ecosystems: Importance of Partitioning for Bioavailability to Invertebrates, Microbes, and Plants 2002, 69-87. SETAC Press, Pensacola, FL. H.E. Allen (Ed.).
47. Mertens J., Springael D., De Troyer I., Cheyns K., Wattiau P., Smolders E. Long-term exposure to elevated zinc concentrations induced structural changes and zinc tolerance of the nitrifying community in soil. Environ. Microbiol. 2006, 8:2170-2178.
48. Monokrousos N., Papatheodoru E.M., Diamantopoulos J.D., Stamou G.P. Soil quality variables in organically and conventionally cultivated field sites. Soil Biol. Biochem. 2006, 38:1282-1289.
49. Moreno J.L., Bastida F., Ros M., Hernández T., García C. Soil organic carbon buffers heavy metal contamination on semiarid soils: effects of different metal threshold levels on soil microbial activity. Eur. J. Soil Biol. 2009, 45:220-228.
50. Nayak D.R., Babu Y.J., Adhya T.K. Long-term application of compost influences microbial biomass and enzyme activities in a tropical Aeric Endoaquept planted to rice under flooded condition. Soil Biol. Biochem. 2007, 39:1897-1906.
51. Niemeyer J.C., Moreira-Santos M., Nogueira M.A., Carvalho G.M., Ribeiro R., Da Silva E.M., Sousa J.P. Environmental risk assessment of a metal-contaminated area in the Tropics. Tier I: screening phase. J. Soils Sediments 2010, 10:1557-1571.
52. Niemeyer, J.C., Nogueira, M.A., Carvalho, G.M., Cohin-de-Pinho, S.J., Outeiro, U.S., Rodrigues, G.G., Da Silva. E.M., Sousa, J.P. Functional and structural parameters to assess the ecological status of a metal contaminated area in the tropics. Ecol. Paramet., submitted.
53. Nogueira M.A., Albino U.B., Brandão-Júnior O., Braun G., Cruz M.F., Dias B.A., Duarte R.T.D., Gioppo N.M.R., Menna P., Orlandi J.M., Raiman M.P., Rampazo L.G.L., Santos M.A., Silva M.E.Z., Vieira F.P., Torezan J.M.D., Hungria M., Andrade G. Promising indicators for assessment of agro ecosystems alteration among natural, reforested and agricultural land use in southern Brazil. Agric. Ecosyst. Environ. 2006, 115:237-247.
54. Rajapaksha R.M.C.P., Tobor-Kaplon M.A., Baath E. Metal toxicity affects fungal and bacterial activities in soil differently. Appl. Environ. Microbiol. 2004, 70:2966-2973.
55. Renella G., Chaudri A.M., Brookes P.C. Fresh additions of heavy metals do not model long-term effects on microbial biomass and activity. Soil Biol. Biochem. 2002, 34:121-124.
56. Rost U., Joergensen R.G., Chander K. Effects of Zn enriched sewage sludge on microbial activities and biomass in soil. Soil Biol. Biochem. 2001, 33:633-638.
57. Rutgers, M., Tuinstra, J., Spijker, J., Mesman, M., Wintersen, A., Posthuma, L., 2008. Ecological risks of soil contamination in the second step of the remediation criterion. Report 711701072. RIVM, Bilthoven, The Netherlands (in Dutch with English summary).
58. Sarathchandra S.V. Nitrification activities and the changes in the population of nitrifying bacteria in soil perfused with two different H-ion concentrations. Plant Soil 1978, 50:99-111.
59. Sauvé S., Dumestre A., McBride M., Gillett J.W., Berthelin J., Hendershot W. Nitrification potential in field-collected soils contaminated with Pb or Cu. Appl. Soil Ecol. 1999, 12:29-39.
60. Schmidt E.L., Belser L.W. Autotrophic nitrifying bacteria. Methods of Soil Analysis. Part 2: Microbiological and Biochemical Properties 1994, 159-177. Soil Sci. Soc. Am. J. R.W. Weaver, S. Angle, P. Bottomley, D. Bezdicek, S. Smith, A. Tabatabai, A. Wollum (Eds.).
61. Schuster E., Schroder D. Side effects of sequentially-applied pesticides on target soil microorganisms: field experiments. Soil Biol. Biochem. 1990, 22:67-373.
62. Smejkalova M., Mikanova O., Boruvka L. Effects of heavy metal concentrations on biological activity of soil micro-organisms. Plant Soil Environ. 2003, 49:321-326.
63. Sobolev D., Begonia M.F.T. Effects of heavy metal contamination upon soil microbes: lead-induced changes in general and denitrifying microbial communities as evidenced by molecular markers. Int. J. Environ. Res. Public Health 2008, 5:450-456.
64. Tabatabai M.A., Bremner J.M. Use of ρ-nitrofenil phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1969, 1:301-307.
65. Timmermans M.J.T.N., Ellers J., Van Straalen N.M. Allelic diversity of metallothionein in Orchesella cincta (L.): traces of natural selection by environmental pollution. Heredity 2007, 98:311-319.
66. Tordoff G.M., Baker A.J.M., Willis A.J. Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 2000, 41:219-228.
67. Tu C., Ristaino J.B., Hu S. Soil microbial biomass and activity in organic tomato farming systems: effects of organic inputs and straw mulching. Soil Biol. Biochem. 2006, 38:247-255.
68. USEPA, 2004. Framework for inorganic metals risk assessment. United States Environmental Protection Agency, Draft EPA/630/P-04/068B, Washington, DC.
69. Valsecchi G., Gigliotti C., Farini A. Microbial biomass, activity, and organic matter accumulation in soils contaminated with heavy metals. Biol. Fert. Soils 1995, 20:253-259.
70. Vance E.D., Brookes P.C., Jenkinson D.S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 1987, 19:703-707.
71. Veiga M.D., Wildner L.D.P. Manual para la instalación y conducción de experimentos de perdida de suelos 1993, EPAGRI/FAO, Santiago.
72. Vig K., Megharaj M., Sethunathan N., Naidu R. Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv. Environ. Res. 2003, 8:121-135.
73. Widianarko B., Verweij R., Van Gestel C., Van Straalen N.M. Spatial distribution of trace metals in sediments from urban streams of Semarang Central Java, Indonesia. Ecotoxicol. Environ. Saf. 2000, 46:96-100.
74. Woomer P.L. Most probable number counts. Methods of Soil Analysis, Part 2: Microbiological and Biochemical Properties 1994, 59-79. Soil Sci. Soc. Am. J. Madison. R.W. Weaver, S. Angle, P. Bottomley, D. Bezdicek, S. Smith, A. Tabatabai, A. Wollum (Eds.).
75. Yuangen Y., Congqiang L., Lei X., Pan W., Guoping Z. Effects of heavy metal contamination on microbial biomass and community structure in soils. Chin. J. Geochem. 2004, 23:319-328.
76. Zeng L.S., Liao M., Chen C.L., Huang C.Y. Effects of lead contamination on soil enzymatic activities, microbial biomass, and rice physiological indices in soil-lead-rice (Oryza sativa L.) system. Ecotoxicol. Environ. Saf. 2007, 67:67-74.
77. Zhang Y., Zhang H., Su Z., Zhang C. Soil microbial characteristics under long-term heavy metal stress: a case study in Zhangshi wastewater irrigation area, Shenyang. Pedosphere 2008, 18:1-10.
78. Zimakowska-Gnoinska D., Bech J., Tobias F.J. Assessment of the heavy metal pollution effects on the soil respiration in the Baix Llobregat (Catalonia, NE Spain). Environ. Monit. Assess. 2000, 61:301-313.