Environmental factors influencing the structural dynamics of soil microbial communities during assisted phytostabilization of acid-generating mine tailings: A mesocosm experiment

Science of the Total Environment

Volumn 500-501, Issue , 2014, Pages 314-324

  Valentín Vargas, Alexis ^a   Root, Robert A ^a   Neilson, Julia W ^a   Chorover, Jon ^a   Maier, Raina M ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Acidification; Mesocosms; Metal(loid)s; Microbial community structure; Mine tailings; Phytostabilization

Indexed keywords

ACIDIFICATION; BACTERIA; COBALT; DETOXIFICATION; DYNAMICS; ECOSYSTEMS; EXPERIMENTS; FUNGI; REVEGETATION; SOCIAL SCIENCES; SOIL CONSERVATION; STRUCTURAL DYNAMICS; SUSTAINABLE DEVELOPMENT; TAILINGS; WATER;

ENVIRONMENTAL CONDITIONS; MESOCOSMS; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY DYNAMICS; MICROBIAL COMMUNITY STRUCTURES; MINE TAILINGS; PHYTOSTABILIZATION; SOIL MICROBIAL COMMUNITY;

COMPOSTING;

COBALT; WATER; SOIL; SOIL POLLUTANT;

ACID MINE DRAINAGE; COMMUNITY STRUCTURE; ENVIRONMENTAL FACTOR; MESOCOSM; MICROBIAL COMMUNITY; SOIL MICROORGANISM; SOIL STABILIZATION; TAILINGS;

ARTICLE; BIOREMEDIATION; COMMUNITY DYNAMICS; COMMUNITY STRUCTURE; COMPOST; CONTROLLED STUDY; DETOXIFICATION; DNA FINGERPRINTING; ENVIRONMENTAL FACTOR; FUNGAL COMMUNITY; GERMINATION; MESOCOSM; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MINE TAILINGS; MULTIVARIATE ANALYSIS; NONHUMAN; PHYTOSTABILIZATION; REVEGETATION; RNA GENE; SOIL ACIDIFICATION; SOIL ACIDITY; SOIL AMENDMENT; SOIL MICROFLORA; WATER ANALYSIS; ANALYSIS; CHEMISTRY; MICROBIOLOGY; MINING; PLANT; PLANT DEVELOPMENT; PLANT ROOT; SOIL; SOIL POLLUTANT;

BIODEGRADATION, ENVIRONMENTAL; MINING; PLANT DEVELOPMENT; PLANT ROOTS; PLANTS; SOIL; SOIL MICROBIOLOGY; SOIL POLLUTANTS;

EID: 84907662196     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2014.08.107     Document Type: Article

References (102)

1. Akcil A., Koldas S. Acid Mine Drainage (AMD): causes, treatment and case studies. J Clean Prod 2006, 14:1139-1145.
2. Alvarenga P., Gonçalves A.P., Fernandes R.M., de Varennes A., Vallini G., Duarte E., et al. Evaluation of composts and liming materials in the phytostabilization of a mine soil using perennial ryegrass. Sci Total Environ 2008, 406:43-56.
3. Bardgett R.D., Mawdsley J.L., Edwards S., Hobbs P.J., Rodwell J.S., Davies W.J. Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 1999, 13:650-660.
4. Bittman S., Forge T.A., Kowalenko C.G. Responses of the bacterial and fungal biomass in a grassland soil to multiyear applications of dairy manure slurry and fertilizer. Soil Biol Biochem 2005, 37:613-623.
5. Bolan N.S., Duraisamy V.P. Role of inorganic and organic soil amendments on immobilisation and phytoavailability of heavy metals: a review involving specific case studies. J Soil Res 2003, 41:533-555.
6. Bradl H.B. Adsorption of heavy metal ions on soils and soils constituents. J Colloid Interface Sci 2004, 277:1-18.
7. Brodie M.J., Broughton L.M., Robertson A.M. A conceptual rock classification system for waste management and a laboratory method for ARD prediction from rock piles. Conference proceedings-Second International Conference on the Abatement of Acidic Drainage (Montreal, Quebec, Canada) 1991, 119-135. Quebec Mining Association, Ottawa. MEND Program (Ed.).
8. Buée M., De Boer W., Martin F., Van Overbeek L. The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 2009, 321:189-212.
9. Buyer J.S., Roberts D.P., Russek-Cohen E. Soil and plant effects on microbial community structure. Can J Microbiol 2002, 48:955-964.
10. Casamayor E.O., Schäfer H., Bañeras L., Pedrós-Alió C., Muyzer G. Identification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis. Appl Environ Microbiol 2000, 66:499-508.
11. Casamayor E.O., Massana R., Benlloch S., Ovreas L., Diez B., Goddard V.J., et al. Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol 2002, 4:338-348.
12. Chuan M.C., Shu G.Y., Liu J.C. Solubility of heavy metals in a contaminated soil: effects of redox potential and pH. Water Air Soil Pollut 1996, 90:543-556.
13. Colores G.M., Macur R.E., Ward D.M., Inskeep W.P. Molecular analysis of surfactant-driven microbial population shifts in hydrocarbon-contaminated soil. Appl Environ Microbiol 2000, 66:2959-2964.
14. Cravotta-Iii C.A., Trahan M.K. Limestone drains to increase pH and remove dissolved metals from acidic mine drainage. Appl Geochem 1999, 14:581-606.
15. de Boer W., Folman L.B., Summerbell R.C., Boddy L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 2005, 29:795-811.
16. Dybowska A., Farago M., Valsami-Jones E., Thornton I. Remediation strategies for historical mining and smelting sites. Sci Prog 2006, 89:71-138.
17. EA-EST (EA Engineering, Science, Technology Inc.) Remedial investigation report: Iron King Mine-Humboldt Smelter Superfund Site, Dewey-Humboldt, Yavapai County, Arizona Available from:, [Accessed on April 4, 2013]. http://yosemite.epa.gov/r9/sfund/r9sfdocw.nsf/3dc283e6c5d6056f88257426007417a2/9ff58681f889089c882576fd0075ea2f!OpenDocument.
18. Ehrlich H.L. Microbes and metals. Appl Microbiol Biotechnol 1997, 48:687-692.
19. Ekstrom E.B., Morel F.M. Cobalt limitation of growth and mercury methylation in sulfate-reducing bacteria. Environ Sci Technol 2008, 42:93-99.
20. Erguder T.H., Boon N., Wittebolle L., Marzorati M., Verstraete W. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 2009, 33:855-869.
21. Ferris M.J., Muyzer G., Ward D.M. Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 1996, 62:340-346.
22. Fierer N., Jackson R.B. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 2006, 103:626-631.
23. Fierer N., Strickland M.S., Liptzin D., Bradford M.A., Cleveland C.C. Global patterns in belowground communities. Ecol Lett 2009, 12:1238-1249.
24. Frey S.D., Knorr M., Parrent J.L., Simpson R.T. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 2004, 196:159-171.
25. Gadd G.M. Microbial influence on metal mobility and application for bioremediation. Geoderma 2004, 122:109-119.
26. Gadd G.M. Metals, minerals and microbes: geomicrobiology and bioremediation. Annu Rev Microbiol 2010, 156:609-643.
27. Gao Y., Zhou P., Mao L., Zhi Y., Zhang C., Shi W. Effects of plant species coexistence on soil enzyme activities and soil microbial community structure under Cd and Pb combined pollution. J Environ Sci (China) 2010, 22:1040-1048.
28. Garbeva P., van Veen J.A., van Elsas J.D. Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 2004, 42:243-270.
29. García-Sánchez A., Alastuey A., Querol X. Heavy metal adsorption by different minerals: application to the remediation of polluted soils. Sci Total Environ 1999, 242:179-188.
30. Gebel T.W. Arsenic methylation is a process of detoxification through accelerated excretion. Int J Hyg Environ Health 2002, 205:505-508.
31. Görres C.M., Conrad R., Petersen S.O. Effect of soil properties and hydrology on Archaeal community composition in three temperate grasslands on peat. FEMS Microbiol Ecol 2013, 85:227-240.
32. Grandlic C.J., Mendez M.O., Chorover J., Machado B., Maier R.M. Plant growth-promoting bacteria for phytostabilization of mine tailings. Environ Sci Technol 2008, 42:2079-2084.
33. Grantz D.A., Vaughn D.L., Farber R.J., Kim B., Ashbaugh L., VanCuren T., et al. Wind barriers suppress fugitive dust and soil-derived airborne particles in arid regions. J Environ Qual 1998, 27:946-952.
34. Gremion F., Chatzinotas A., Kaufmann K., Sigler Von W., Harms H. Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS Microbiol Ecol 2004, 48:273-283.
35. Guo G., Zhou Q., Ma L.Q. Availability and assessment of fixing additives for the in situ remediation of heavy metal contaminated soils: a review. Environ Monit Assess 2006, 116:513-528.
36. Gyssels G., Poesen J., Bochet E., Li Y. Impact of plant roots on the resistance of soils to erosion by water: a review. Prog Phys Geogr 2005, 29:189-217.
37. Hammer Ø., Harper D., Ryan P.D. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 2001, 4:1-9.
38. Hayden H.L., Mele P.M., Bougoure D.S., Allan C.Y., Norng S., Piceno Y.M., et al. Changes in the microbial community structure of bacteria, archaea and fungi in response to elevated CO(2) and warming in an Australian native grassland soil. Environ Microbiol 2012, 14:3081-3096.
39. Högberg M.N., Högberg P., Myrold D.D. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three?. Oecologia 2007, 150:590-601.
40. Hutchinson I.P.G., Ellison R.D. Mine waste management 1992, Lewis Publishers, Michigan.
41. Johnson D.B., Hallberg K.B. Acid mine drainage remediation options: a review. Sci Total Environ 2005, 338:3-14.
42. Kabas S., Acosta J.A., Zornoza R., Faz-Cano A., Carmona D.M., Martinez-Martinez S. Integration of landscape reclamation and design in a mine tailing in Cartagena-La Unión, SE Spain. Int J Energy Environ 2011, 2:301-308.
43. Khan S., Hesham A.E.-L., Qiao M., Rehman S., He Z.J. Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res Int 2010, 17:288-296.
44. Kim S.D., Kilbane J.J., Cha D.K. Prevention of acid mine drainage by sulfate reducing bacteria: organic substrate addition to mine waste piles. Environ Eng Sci 1999, 16:139-145.
45. Kobayashi M., Shimizu S. Cobalt proteins. Eur J Biochem 1999, 261:1-9.
46. Kondrat'eva T.F., Pivovarova T.A., Tsaplina I.A., Fomchenko N.V., Zhuravleva A.E., Murav'ev M.I., et al. Diversity of the communities of acidophilic chemolithotrophic microorganisms in natural and technogenic ecosystems. Microbiology 2012, 81:1-24.
47. Kort J., Collins M., Ditsch D. A review of soil erosion potential associated with biomass crops. Biomass Bioenergy 1998, 14:351-359.
48. Kumpiene J., Lagerkvist A., Maurice C. Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments-a review. Waste Manag 2008, 28:215-225.
49. Lauber C.L., Strickland M.S., Bradford M.A., Fierer N. The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 2008, 40:2407-2415.
50. Lauber C.L., Hamady M., Knight R., Fierer N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 2009, 75:5111-5120.
51. Lehtovirta L.E., Prosser J.I., Nicol G.W. Soil pH regulates the abundance and diversity of Group 1.1c Crenarchaeota. FEMS Microbiol Ecol 2009, 70:367-376.
52. Lepš J., Šmilauer P. Multivariate analysis of ecological data using CANOCO 2003, Cambridge University Press, New York. 1st ed.
53. Li J., Zheng Y., Yan J., Li H., Wang X., He J., et al. Effects of different regeneration scenarios and fertilizer treatments on soil microbial ecology in reclaimed opencast mining areas on the loess plateau, China. PLoS One 2013, 8:e63275.
54. Liao M., Xie X.M. Effect of heavy metals on substrate utilization pattern, biomass, and activity of microbial communities in a reclaimed mining wasteland of red soil area. Ecotoxicol Environ Saf 2007, 66:217-223.
55. Lonsdale D., Pautasso M., Holdenrieder O. Wood-decaying fungi in the forest: conservation needs and management options. Eur J For Res 2008, 127:1-22.
56. Ma Y., Prasad M.N., Rajkumar M., Freitas H. Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 2011, 29:24-58.
57. Madejón E., Pérez-de-Mora A., Felipe E., Burgos P., Cabrera F. Soil amendments reduce trace element solubility in a contaminated soil and allow regrowth of natural vegetation. Environ Pollut 2006, 139:40-52.
58. Martens J.H., Barg H., Warren M., Jahn D. Microbial production of vitamin B12. Appl Microbiol Biotechnol 2002, 58:275-285.
59. Mason R.P. The methylation of metals and metalloids in aquatic systems. Methylation - from DNA, RNA and histones to diseases and treatment 2012, 271-302. InTech, Croatia. A. Dricu (Ed.).
60. May L.A., Smiley B., Schmidt M.G. Comparative denaturing gradient gel electrophoresis analysis of fungal communities associated with whole plant corn silage. Can J Microbiol 2001, 47:829-841.
61. Mendez M.O., Maier R.M. Phytostabilization of mine tailings in arid and semiarid environments-an emerging remediation technology. Environ Health Perspect 2008, 116:278-283.
62. Mendez M.O., Maier R.M. Phytoremediation of mine tailings in temperate and arid environments. Rev Environ Sci Biotechnol 2008, 7:47-59.
63. Mendez M.O., Glenn E.P., Maier R.M. Phytostabilization potential of quailbush for mine tailings: growth, metal accumulation and microbial community changes. J Environ Qual 2007, 36:245-253.
64. Mendez M.O., Neilson J.W., Maier R.M. Characterization of a bacterial community in an abandoned semiarid lead-zinc mine tailing site. Appl Environ Microbiol 2008, 74:3899-3907.
65. Meyer J., Michalke K., Kouril T., Hensel R. Volatilisation of metals and metalloids: an inherent feature of methanoarchaea?. Syst Appl Microbiol 2008, 31:81-87.
66. Meza-Figueroa D., Maier R.M., de la O-Villanueva M., Gómez-Alvarez A., Moreno-Zazueta A., Rivera J., et al. The impact of unconfined mine tailings in residential areas from a mining town in a semi-arid environment: Nacozari, Sonora, Mexico. Chemosphere 2009, 77:140-147.
67. Mummey D.L., Stahl P.D., Buyer J.S. Microbial biomarkers as an indicator of ecosystem recovery following surface mine reclamation. Appl Soil Ecol 2002, 21:251-259.
68. Navarrete A.A., Cannavan F.S., Taketani R.G., Tsai S.M. A molecular survey of the diversity of microbial communities in different Amazonian agricultural model systems. Diversity 2010, 2:787-809.
69. Nicol G.W., Leininger S., Schleper C., Prosser J.I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 2008, 10:2966-2978.
70. Nies D.H. Microbial heavy-metal resistance. Appl Microbiol Biotechnol 1999, 51:730-750.
71. Okamoto S., Eltis L.D. The biological occurrence and trafficking of cobalt. Metallomics 2011, 3:963-970.
72. Park J.H., Lamb D., Paneerselvam P., Choppala G., Bolan N., Chung J.W. Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. J Hazard Mater 2011, 185:549-574.
73. Pereira-e-Silva M.C., Dias A.C., van Elsas J.D., Salles J.F. Spatial and temporal variation of archaeal, bacterial and fungal communities in agricultural soils. PLoS One 2012, 7:e51554.
74. Pérez-de-Mora A., Ortega-Calvo J.J., Cabrera F., Madejón E. Changes in enzyme activities and microbial biomass after "in situ" remediation of a heavy metal-contaminated soil. Appl Soil Ecol 2005, 28:125-137.
75. Pérez-de-Mora A., Burgos P., Madejón E., Cabrera F., Jaeckel P., Schloter M. Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biol Biochem 2006, 38:327-341.
76. Ram M.S., Singh L., Suryanarayana M., Alam S.I. Effect of iron, nickel and cobalt on bacterial activity and dynamics during anaerobic oxidation of organic matter. Water Air Soil Pollut 2000, 117:305-312.
77. Ranquet C., Ollagnier-de-Choudens S., Loiseau L., Barras F., Fontecave M. Cobalt stress in Escherichia coli: the effect on the iron-sulfur proteins. J Biol Chem 2007, 282:30442-30451.
78. Reed H.E., Martiny J.B. Testing the functional significance of microbial composition in natural communities. FEMS Microbiol Ecol 2007, 62:161-170.
79. Rieuwerts J.S., Thornton I., Farago M.E., Ashmore F.R. Factors influencing metal bioavailability in soils: preliminary investigations for the development of a critical loads approach for metals. Chem Speciat Bioavailab 1998, 10:61-75.
80. Root R.A., Hayes S.M., Schowalter C., Chorovoer J. Coupled arsenic and sulfur speciation in semi-arid tailings. Geochim Cosmochim Acta 2010, 74:A881. [Supplement].
81. Rosario K., Iverson S.L., Henderson D.A., Chartrand S., McKeon C., Glenn E.P., et al. Bacterial community changes during plant establishment at the San Pedro River mine tailings site. J Environ Qual 2007, 36:1249-1259.
82. Rousk J.J., Brookes P.C.P., Bååth E.E. Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 2009, 75:1589-1596.
83. Rousk J., Bååth E., Brookes P.C., Lauber C.L., Lozupone C., Caporaso J.G., et al. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 2010, 4:1340-1351.
84. Schippers A., Breuker A., Blazejak A., Bosecker K., Kock D., Wright T.L. The biogeochemistry and microbiology of sulfidic mine waste and bioleaching dumps and heaps, and novel Fe(II)-oxidizing bacteria. Hydrometallurgy 2010, 104:342-350.
85. Schutter M., Dick R. Shifts in substrate utilization potential and structure of soil microbial communities in response to carbon substrates. Soil Biol Biochem 2001, 33:1481-1491.
86. Sheoran A.S., Sheoran V. Heavy metal removal mechanism of acid mine drainage in wetlands: a critical review. Hydrometallurgy 2006, 19:105-116.
87. Silver S., Phung-le T. A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotechnol 2005, 32:587-605.
88. Solís-Domínguez F.A., Valentín-Vargas A., Chorover J., Maier R.M. Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci Total Environ 2011, 409:1009-1016.
89. Solís-Domínguez F.A., White S.A., Hutter T.B., Amistadi M.K., Root R.A., Chorover J., et al. Response of key soil parameters during compost-assisted phytostabilization in extremely acidic tailings: effect of plant species. Environ Sci Technol 2012, 46:1019-1027.
90. Soppa J. From genomes to function: haloarchaea as model organisms. Annu Rev Microbiol 2006, 152:585-590.
91. Tan G.L., Shu W.S., Hallberg K.B., Li F., Lan C.Y., Zhou W.H., et al. Culturable and molecular phylogenetic diversity of microorganisms in an open-dumped, extremely acidic Pb/Zn mine tailings. Extremophiles 2008, 12:657-664.
92. Taylor G.T., Sullivan C.W. Vitamin B12 and cobalt cycling among diatoms and bacteria in Antarctic sea ice microbial communities. Limnol Oceanogr 2008, 53:5862-5877.
93. ter Braak C.J.F., Šmilauer P. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination. V 4.5 2002, Microcomputer Power, New York.
94. ter Braak C.J.F., Wiertz J. On the statistical analysis of vegetation change: a wetland affected by water extraction and soil acidification. J Veg Sci 1994, 5:361-372.
95. Tordoff G.M., Baker A.J., Willis A.J. Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 2000, 41:219-228.
96. Tuomela M., Vikman M., Hatakka A., Itavaara M. Biodegradation of lignin in a compost environment: a review. Bioresour Technol 2000, 72:169-183.
97. Valentín-Vargas A., Toro-Labrador G., Massol-Deyá A.A. Bacterial community dynamics in full-scale activated sludge bioreactors: operational and ecological factors driving community assembly and performance. PLoS One 2012, 7:e42524.
98. Valentín-Vargas A., Chorover J., Maier R.M. A New Standard-Based Polynomial Interpolation (SBPIn) method to address gel-to-gel variability for the comparison of multiple denaturing gradient gel electrophoresis profile matrices. J Microbiol Methods 2013, 92:173-177.
99. Walker D.J., Clemente R., Bernal M.P. Contrasting effects of manure and compost on soil pH, heavy metal availability and growth of Chenopodium album L. in a soil contaminated by pyritic mine waste. Chemosphere 2004, 57:215-224.
100. Walsh D.A., Papke R.T., Doolittle W.F. Archaeal diversity along a soil salinity gradient prone to disturbance. Environ Microbiol 2005, 7:1655-1666.
101. Warton B., Matthiessen J.N. The crucial role of calcium interacting with soil pH in enhanced biodegradation of metam-sodium. Pest Manag Sci 2005, 61:856-862.
102. Wong M.H. Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 2003, 50:775-780.