The exposition of a calcareous Mediterranean soil to toxic concentrations of Cr, Cd and Pb produces changes in the microbiota mainly related to differential metal bioavailability

Chemosphere

Volumn 89, Issue 5, 2012, Pages 494-504

  Caliz, Joan ^a   Montserrat, Genoveva ^a   Martí, Esther ^b   Sierra, Jordi ^b   Cruañas, Robert ^b   Antonia Garau, M ^b   Triadó Margarit, Xavier ^a   Vila, Xavier ^a  

^a UNIVERSITY OF GIRONA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Arthrobacter; Bacillus; Heavy metals; PCR DGGE; Respirometry; Stenotrophomonas maltophilia

Indexed keywords

BACILLI; BACTERIA; BACTERIOLOGY; BIOCHEMISTRY; BIOREMEDIATION; CADMIUM COMPOUNDS; HEAVY METALS; LEAD COMPOUNDS; POLYMERASE CHAIN REACTION; SOIL POLLUTION; SOILS;

ARTHROBACTER; BACTERIAL COMMUNITY; BACTERIAL COMPOSITION; CONTROLLED LABORATORIES; METAL BIOAVAILABILITY; PCR-DGGE; RESPIROMETRY; STENOTROPHOMONAS MALTOPHILIA;

CHROMIUM COMPOUNDS;

CADMIUM; CHROMIUM; LEAD;

AGRICULTURAL SOIL; BACTERIUM; BIOAVAILABILITY; BIOREMEDIATION; CADMIUM; CALCAREOUS SOIL; CHROMIUM; COMMUNITY COMPOSITION; COMMUNITY DYNAMICS; CONCENTRATION (COMPOSITION); ECOTOXICOLOGY; LEAD; MICROBIAL COMMUNITY; MICROCOSM; POLLUTION EFFECT; POLLUTION EXPOSURE; POLYMERASE CHAIN REACTION; SOIL POLLUTION; SOIL RESPIRATION;

ARTHROBACTER; ARTICLE; BIOAVAILABILITY; BIOREMEDIATION; MEDITERRANEAN SEA; MICROBIAL COMMUNITY; MICROCOSM; MICROFLORA; NONHUMAN; POLYMERASE CHAIN REACTION; RESPIROMETRY; SOIL ANALYSIS; SOIL POLLUTION; STENOTROPHOMONAS MALTOPHILIA; TOXICITY;

ARTHROBACTER; ARTHROBACTER CRYSTALLOPOIETES; BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); STENOTROPHOMONAS MALTOPHILIA;

EID: 84864519645     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2012.05.002     Document Type: Article

References (76)

1. Abou-Shanab R.A.I., Angle J.S., van Berkum P. Chromate-tolerant bacteria for enhanced metal uptake by Eichhornia crassipes (MART.). Int. J. Phytoremediat. 2007, 9:91-105.
2. Alonso A., Sanchez P., Martinez J.L. Stenotrophomonas maltophilia D457R contains a cluster of genes from gram-positive bacteria involved in antibiotic and heavy metal resistance. Antimicrob. Agents Chemother. 2000, 44:1778-1782.
3. American-Public-Health-Association, 1998. Metals, part 3000. In: Clesceri, L.S., Greenberg, A.E., Eaton, A.D. (Ed.). Standard Methods for the Determination of Water and Wastewater. American Public Health Association, Washington, DC, pp. 65-68.
4. Antonioli P., Lampis S., Chesini I., Vallini G., Rinalducci S., Zolla L., Righetti P.G. Stenotrophomonas maltophilia SeITE02, a new bacterial strain suitable for bioremediation of selenite-contaminated environmental matrices. Appl. Environ. Microbiol. 2007, 73:6854-6863.
5. Baker G.C., Smith J.J., Cowan D.A. Review and re-analysis of domain-specific 16S primers. J. Microbiol. Methods 2003, 55:541-555.
6. Bataillard P., Cambier P., Picot C. Short-term transformations of lead and cadmium compounds in soil after contamination. Eur. J. Soil Sci. 2003, 54:365-376.
7. Becker J., Parkin T., Nakatsu C., Wilbur J., Konopka A. Bacterial activity, community structure, and centimeter-scale spatial heterogeneity in contaminated soil. Microb. Ecol. 2006, 51:220-231.
8. Bernard L., Maron P.A., Mougel C., Nowak V., Leveque J., Marol C., Balesdent J., Gibiat F., Ranjard L. Contamination of soil by copper affects the dynamics, diversity, and activity of soil bacterial communities involved in wheat decomposition and carbon storage. Appl. Environ. Microbiol. 2009, 75:7565-7569.
9. Blaser P., Zimmermann S., Luster J., Shotyk W. Critical examination of trace element enrichments and depletions in soils: As, Cr, Cu, Ni, Pb, and Zn in Swiss forest soils. Sci. Total Environ. 2000, 249:257-280.
10. Branco R., Chung A., Veríssimo A., Morais P. Impact of chromium-contaminated wastewaters on the microbial community of a river. FEMS Microbiol. Ecol. 2005, 54:35-46.
11. Broos K., Warne M.S.J., Heemsbergen D.A., Stevens D., Barnes M.B., Correll R.L., MCLaughlin M.J. Soil factors controlling the toxicity of copper and zinc to microbial processes in Australian soils. Environ. Toxicol. Chem. 2007, 26:583-590.
12. Cáliz, J., Montserrat, G., Sierra, J., Martí, E., Sánchez, M., Cruañas, R., Garau, M.A., Vila, X., 2008. Chromium-resistant bacteria and TCP/PCP-resistant bacteria from a calcareous clayey soil: detection, identification, isolation and characterization of their behaviour at high pollutant concentrations. In: F&U confirm, L. (Ed.), 10th International Conference on Contaminated Soil (ConSoil 2008), Milan (Italy) (ISBN: 978-3-00-024598-5).
13. Cáliz J., Vila X., Martí E., Sierra J., Cruañas R., Garau M.A., Montserrat G. Impact of chlorophenols on microbiota of an unpolluted acidic soil: microbial resistance and biodegradation. FEMS Microbiol. Ecol. 2011, 78:150-164.
14. Cáliz J., Vila X., Martí E., Sierra J., Nordgren J., Lindgren P.E., Bañeras L., Montserrat G. The microbiota of an unpolluted calcareous soil faces up chlorophenols: evidences of resistant strains with potential for bioremediation. Chemosphere 2011, 83:104-116.
15. Camargo F.A., Bento F.M., Okeke B.C., Frankenberger W.T. Hexavalent chromium reduction by an actinomycete, Arthrobacter crystallopoietes ES 32. Biol. Trace Elem. Res. 2004, 97:183-194.
16. 2+. Appl. Microbiol. Biotechnol. 2003, V62:569.
17. Camargo F.A.O., Okeke B.C., Bento F.M., Frankenberger W.T. Diversity of chromium-resistant bacteria isolated from soils contaminated with dichromate. Appl. Soil Ecol. 2005, 29:193.
18. Coombs J.M., Barkay T. Molecular evidence for the evolution of metal homeostasis genes by lateral gene transfer in bacteria from the deep terrestrial subsurface. Appl. Environ. Microbiol. 2004, 70:1698-1707.
19. Covelo E.F., Vega F.A., Andrade M.L. Simultaneous sorption and desorption of Cd, Cr, Cu, Ni, Pb, and Zn in acid soils: I. Selectivity sequences. J. Hazard. Mater. 2007, 147:852-861.
20. Chien C.C., Hung C.W., Han C.T. Removal of cadmium ions during stationary growth phase by an extremely cadmium resistant strain of Stenotrophomonas sp. Environ. Toxicol. Chem. 2007, 26:664-668.
21. Díaz-Raviña M., Bååth E. Development of metal tolerance in soil bacterial communities exposed to experimentally increased metal levels. Appl. Environ. Microbiol. 1996, 62:2970-2977.
22. DIN, 1984. German Standard Determination of the Leachability by Water (S4). Deutsche Norm, Teil 4 Okt., pp. 464-475.
23. Echeverría J.C., Morera M.T., Mazkiarán C., Garrido J.J. Competitive sorption of heavy metal by soils. Isotherms and fractional factorial experiments. Environ. Pollut. 1998, 101:275-284.
24. Ellis R.J., Morgan P., Weightman A.J., Fry J.C. Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl. Environ. Microbiol. 2003, 69:3223-3230.
25. FAO-UNESCO (Ed.), 1998. FAO-UNESCO. World Reference Base for Soil Resources. FAO-UNESCO, Rome.
26. Fernández-Calviño D., Martín A., Arias-Estévez M., Bååth E., Díaz-Raviña M. Microbial community structure of vineyard soils with different pH and copper content. Appl. Soil Ecol. 2010, 46:276-282.
27. Fernández-Calviño D., Martín A., Arias-Estévez M., Bååth E., Díaz-Raviña M. Bacterial pollution induced community tolerance (PICT) to Cu and interactions with pH in long-term polluted vineyard soils. Soil Biol. Biochem. 2011, 43:2324-2331.
28. Francisco R., Alpoim M.C., Morais P.V. Diversity of chromium-resistant and -reducing bacteria in a chromium-contaminated activated sludge. J. Appl. Microbiol. 2002, 92:837-843.
29. Francisco R., Moreno A., Morais P. Different physiological responses to chromate and dichromate in the chromium resistant and reducing strain Ochrobactrum tritici 5bvl1. BioMetals 2010, 23:713-725.
30. Giller K.E., Witter E., McGrath S.P. Heavy metals and soil microbes. Soil Biol. Biochem. 2009, 41:2031-2037.
31. Ginocchio R., De la Fuente L.M., Sánchez P., Bustamante E., Silva Y., Urrestarazu P., Rodríguez P.H. Soil acidification as a confounding factor on metal phytotoxicity in soils spiked with copper-rich mine wastes. Environ. Toxicol. Chem. 2009, 28:2069-2081.
32. He Z.L., Yang X.E., Stoffella P.J. Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 2005, 19:125-140.
33. Hernandez A., Mellado R.P., Martinez J.L. Metal accumulation and vanadium-induced multidrug resistance by environmental isolates of Escherichia hermannii and Enterobacter cloacae. Appl. Environ. Microbiol. 1998, 64:4317-4320.
34. Hoang T.C., Rogevich E.C., Rand G.M., Gardinali P.R., Frakes R.A., Bargar T.A. Copper desorption in flooded agricultural soils and toxicity to the Florida apple snail (Pomacea paludosa): implications in Everglades restoration. Environ. Pollut. 2008, 154:338-347.
35. Horton R., Apel W., Thompson V., Sheridan P. Low temperature reduction of hexavalent chromium by a microbial enrichment consortium and a novel strain of Arthrobacter aurescens. BMC Microbiol. 2006, 6:5.
36. Huber T., Faulkner G., Hugenholtz P. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 2004, 20:2317-2319.
37. Jackson C.R., Harrison K.G., Dugas S.L. Enumeration and characterization of culturable arsenate resistant bacteria in a large estuary. Syst. Appl. Microbiol. 2005, 28:727-734.
38. James B.R., Bartlett R.J. Behavior of chromium in soils. VII. Adsorption and reduction of hexavalent forms. J. Environ. Qual. 1983, 12:177-181.
39. Konopka A., Zakharova T., Bischoff M., Oliver L., Nakatsu C., Turco R.F. Microbial biomass and activity in lead-contaminated soil. Appl. Environ. Microbiol. 1999, 65:2256-2259.
40. Kozdrój J., van Elsas J.D. Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol. Biochem. 2000, 32:1405-1417.
41. Lakzian A., Murphy P., Giller K.E. Transfer and loss of naturally-occurring plasmids among isolates of Rhizobium leguminosarum bv. viciae in heavy metal contaminated soils. Soil Biol. Biochem. 2007, 39:1066-1077.
42. Lane D.J. 16S/23S r RNA sequencing. Nucleic Acid Techniques in Bacterial Systematics 1991, 115-175. John Wiley, Chichester, England. E. Stackebrant, M. Goodfellow (Eds.).
43. Lazzaro A., Hartmann M., Blaser P., Widmer F., Schulin R., Frey B. Bacterial community structure and activity in different Cd-treated forest soils. FEMS Microbiol. Ecol. 2006, 58:278-292.
44. Lazzaro A., Widmer F., Sperisen C., Frey B. Identification of dominant bacterial phylotypes in a cadmium-treated forest soil. FEMS Microbiol. Ecol. 2008, 63:143-155.
45. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, Buchner A., Lai T., Steppi S., Jobb G., Forster W., Brettske I., Gerber S., Ginhart A.W., Gross O., Grumann S., Hermann S., Jost R., Konig A., Liss T., Lussmann R., May M., Nonhoff B., Reichel B., Strehlow R., Stamatakis A., Stuckmann N., Vilbig A., Lenke M., Ludwig T., Bode A., Schleifer K.H. ARB: a software environment for sequence data. Nucleic Acids Res. 2004, 32:1363-1371.
46. Martí E., Cáliz J., Montserrat G., Garau M.A., Cruañas R., Vila X., Sierra J. Air-drying, cooling and freezing for soil sample storage affects the activity and the microbial communities from two mediterranean soils. Geomicrobiol. J. 2012, 29:151-160.
47. Martí E., Sierra J., Cáliz J., Montserrat G., Vila X., Garau M.A., Cruañas R. Soil type-dependent ecotoxicological effects of chlorophenolic compounds. Sci. Total Environ. 2011, 409:2707-2716.
48. Morel M.A., Ubalde M.C., Olivera-Bravo S., Callejas C., Gill P.R., Castro-Sowinski S. Cellular and biochemical response to Cr(VI) in Stenotrophomonas sp. FEMS Microbiol. Lett. 2009, 291:162-168.
49. Muyzer G., de Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59:695-700.
50. Muyzer G., Smalla K. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Anton. Leeuw. Int. J. Gen. mol. Microbiol. 1998, 73:127-141.
51. Muyzer G., Teske A., Wirsen C., Jannasch H. Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch. Microbiol. 1995, 164:165-172.
52. Nakatsu C.H., Carmosini N., Baldwin B., Beasley F., Kourtev P., Konopka A. Soil microbial community responses to additions of organic carbon substrates and heavy metals (Pb and Cr). Appl. Environ. Microbiol. 2005, 71:7679-7689.
53. Pages D., Rose J., Conrod S., Cuine S., Carrier P., Heulin T., Achouak W. Heavy metal tolerance in Stenotrophomonas maltophilia. PLoS One 2008, 3:e1539.
54. Perilli P., Mitchell L.G., Grant C.A., Pisante M. Cadmium concentration in durum wheat grain (Triticum turgidum) as influenced by nitrogen rate, seeding date and soil type. J. Sci. Food Agric. 2009, 90:813-822.
55. Petersen S.O., Klug M.J. Effects of sieving, storage, and incubation temperature on the phospholipid Fatty Acid profile of a soil microbial community. Appl. Environ. Microbiol. 1994, 60:2421-2430.
56. Presley S.M., Abel M.T., Austin G.P., Rainwater T.R., Brown R.W., McDaniel L.N., Marsland E.J., Fornerette A.M., Dillard M.L., Rigdon R.W., Kendall R.J., Cobb G.P. Metal concentrations in schoolyard soils from New Orleans, Louisiana before and after Hurricanes Katrina and Rita. Chemosphere 2010, 80:67-73.
57. Pruesse E., Quast C., Knittel K., Fuchs B.M., Ludwig W., Peplies J., Glockner F.O. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35:7188-7196.
58. Rasmussen L.D., Sørensen S.J. The effect of longterm exposure to mercury on the bacterial community in marine sediment. Curr. Microbiol. 1998, 36:291-297.
59. Roane T.M., Josephson K.L., Pepper I.L. Dual-bioaugmentation strategy to enhance remediation of cocontaminated soil. Appl. Environ. Microbiol. 2001, 67:3208-3215.
60. Roane T.M., Pepper I.L. Microbial responses to environmentally toxic cadmium. Microb. Ecol. 1999, 38:358-364.
61. Sandaa R.A., Torsvik V., Enger Ø. Influence of long-term heavy-metal contamination on microbial communities in soil. Soil Biol. Biochem. 2001, 33:287-295.
62. Santos S., Costa C.A.E., Duarte A.C., Scherer H.W., Schneider R.J., Esteves V.I., Santos E.B.H. Influence of different organic amendments on the potential availability of metals from soil: a study on metal fractionation and extraction kinetics by EDTA. Chemosphere 2010, 78:389-396.
63. Shaoping H., Xincai C., Jiyan S., Yingxu C., Qi L. Particle-facilitated lead and arsenic transport in abandoned mine sites soil influenced by simulated acid rain. Chemosphere 2008, 71:2091-2097.
64. Shi W., Bischoff M., Turco R., Konopka A. Long-term effects of chromium and lead upon the activity of soil microbial communities. Appl. Soil Ecol. 2002, 21:169-177.
65. Sillanpää M., Oikari A. Assessing the impact of complexation by EDTA and DTPA on heavy metal toxicity using microtox bioassay. Chemosphere 1996, 32:1485-1497.
66. Stevens C.J., Dise N.B., Gowing D.J. Regional trends in soil acidification and exchangeable metal concentrations in relation to acid deposition rates. Environ. Pollut. 2009, 157:313-319.
67. Sundar K., Mukherjee A., Sadiq M., Chandrasekaran N. Cr (III) bioremoval capacities of indigenous and adapted bacterial strains from Palar river basin. J. Hazard. Mater. 2011, 187:553-561.
68. Tarkpea M., Hansson M., Samuelsson B. Comparison of the microtox test with the 96-hr LC50 test for the harpacticoid Nitocra spinipes. Ecotoxicol. Environ. Safe. 1986, 11:127-143.
69. Turpeinen R., Kairesalo T., Häggblom M.M. Microbial community structure and activity in arsenic-, chromium- and copper-contaminated soils. FEMS Microbiol. Ecol. 2004, 47:39-50.
70. USEPA, 1997. Cleaning up the Nation's Waste Sites: Markets and Technology Trends. Office of Solid Waste and Emergency Response. United States Environmental Protection Agency (USEPA)-542-R-96-005, Washington, DC.
71. Van Zwieten L., Ayres M.R., Morris S.G. Influence of arsenic co-contamination on DDT breakdown and microbial activity. Environ. Pollut. 2003, 124:331-339.
72. Verma T., Garg S.K., Ramteke P.W. Genetic correlation between chromium resistance and reduction in Bacillus brevis isolated from tannery effluent. J. Appl. Microbiol. 2009, 107:1425-1432.
73. Villaescusa I., Martí S., Mates C., Martínez M., Ribó J.M. Chromium (VI) toxicity to luminescent bacteria. Environ. Toxicol. Chem. 1997, 16:871-874.
74. Viti C., Giovannetti L. Characterization of cultivable heterotrophic bacterial communities in Cr-polluted and unpolluted soils using Biolog and ARDRA approaches. Appl. Soil Ecol. 2005, 28:101.
75. Viti C., Mini A., Ranalli G., Lustrato G., Giovannetti L. Response of microbial communities to different doses of chromate in soil microcosms. Appl. Soil Ecol. 2006, 34:125.
76. Wang F., Yao J., Si Y., Chen H., Russel M., Chen K., Qian Y., Zaray G., Bramanti E. Short-time effect of heavy metals upon microbial community activity. J. Hazard. Mater. 2010, 173:510-516.