Soil fertility and plant diversity enhance microbial performance in metal-polluted soils

Science of the Total Environment

Volumn 439, Issue , 2012, Pages 211-219

  Stefanowicz, Anna M ^a   Kapusta, Paweł ^a   Szarek Łukaszewska, Grazyna ^a   Grodzińska, Krystyna ^a   Niklińska, Maria ^b   Vogt, Rolf D ^c  

^a W SZAFER INSTITUTE OF BOTANY   (Poland)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Heavy metals; Plant functional diversity; Plant species richness; Soil microbial communities; Soil physicochemical properties

Indexed keywords

BASAL RESPIRATION; CLAY CONTENT; CULTURABLE; EXPLANATORY VARIABLES; FUNCTIONAL DIVERSITY; HEAVY METAL POLLUTION; HIGH-CONTENT; LEAD MINING; METAL CONTAMINATION; MICROBIAL BIOMASS; MICROBIAL COMMUNITIES; MICROBIAL PARAMETERS; MICROBIAL RESPIRATION; MINING WASTE; MULTIPLE REGRESSION ANALYSIS; NUTRIENT AVAILABILITY; PHOSPHORUS CONTENTS; PHYSICOCHEMICAL PROPERTY; PLANT COMMUNITIES; PLANT DIVERSITY; PLANT SPECIES; SOIL BACTERIUM; SOIL FERTILITY; SOIL MICROBES; SOIL MICROBIAL COMMUNITY; SOIL TYPES; TOXIC EFFECT; TRACE METAL; VEGETATION PARAMETERS;

BACTERIA; FORESTRY; HEAVY METALS; LEAD; PHOSPHORUS; REGRESSION ANALYSIS; SOIL POLLUTION; ZINC;

SOILS;

CADMIUM; CALCIUM; CARBON; LEAD; MAGNESIUM; NITROGEN; ORGANIC CARBON; PHOSPHORUS; POTASSIUM; ZINC;

BIOMASS; HEAVY METAL; MICROBIAL ACTIVITY; MULTIPLE REGRESSION; NUTRIENT AVAILABILITY; PHYSICOCHEMICAL PROPERTY; PLANT; SOIL BIOTA; SOIL FERTILITY; SOIL POLLUTION; SPECIES DIVERSITY; SPECIES RICHNESS;

ARTICLE; CLAY; FUNGUS; LEGUME; MICROBIAL BIOMASS; MICROBIAL COMMUNITY; MICROBIAL RESPIRATION; MINING; NONHUMAN; PHYSICAL CHEMISTRY; PLANT COMMUNITY; POACEAE; POLAND; PRIORITY JOURNAL; SAND; SOIL FERTILITY; SOIL MICROFLORA; SOIL POLLUTION; SOIL RESPIRATION; SPECIES DIVERSITY; SPECIES RICHNESS; VEGETATION;

BIODIVERSITY; CADMIUM; FERTILITY; LEAD; METALS, HEAVY; MINING; PLANT DEVELOPMENT; PLANTS; POLAND; SOIL; SOIL MICROBIOLOGY; SOIL POLLUTANTS; SPECIES SPECIFICITY; ZINC;

FUNGI;

EID: 84867325682     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2012.09.030     Document Type: Article

References (73)

1. Anderson J.P.E., Domsch K.H. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 1978, 10:215-221.
2. Avidano L., Gamalero E., Cossa G.P., Carraro E. Characterization of soil health in an Italian polluted site by using microorganisms as bioindicators. Appl Soil Ecol 2005, 30:21-33.
3. Bååth E. Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Pollut 1989, 47:335-379.
4. 2 uptake in dry grasslands. Soil Biol Biochem 2011, 43:1006-1013.
5. Batty L.C., Hallberg K.B. Ecology of industrial pollution 2010, Cambridge University Press, Cambridge.
6. Boivin M.-E.Y., Greve G.D., García-Meza J.V., Massieux B., Sprenger W., Kraak M.H.S., et al. Algal-bacterial interactions in metal contaminated floodplain sediments. Environ Pollut 2007, 145:884-894.
7. Brookes P. The soil microbial biomass: concept, measurement and applications in soil ecosystem research. Microbes Environ 2001, 16:131-140.
8. Buyer J.S., Roberts D.P., Millner P., Russek-Cohen E. Analysis of fungal communities by sole carbon source utilization profiles. J Microbiol Methods 2001, 45:53-60.
9. Cabala J., Teper L. Metalliferous constituents of rhizosphere soils contaminated by Zn-Pb mining in southern Poland. Water Air Soil Pollut 2007, 178:351-362.
10. Cabala J., Krupa P., Misz-Kennan M. Heavy metals in mycorrhizal rhizospheres contaminated by Zn-Pb mining and smelting around Olkusz in southern Poland. Water Air Soil Pollut 2009, 199:139-149.
11. Chodak M., Niklińska M. Effect of texture and tree species on microbial properties of mine soils. Appl Soil Ecol 2010, 46:268-275.
12. Commission of the European Communities Council Directive of 12 June 1986 on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Off J Eur Commun 1986, No L181(86/278/EEC):6-12.
13. De Deyn G.B., Quirk H., Bardgett R.D. Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility. Biol Lett 2011, 7:75-78.
14. Dobranic J.K., Zak J.C. A microtiter plate procedure for evaluating fungal functional diversity. Mycologia 1999, 91:756-765.
15. Eisenhauer N., Beβler H., Engels C., Gleixner G., Habekost M., Milcu A., et al. Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 2010, 91:485-496.
16. Eisenhauer N., Yee K., Johnson E.A., Maraun M., Parkinson D., Straube D., et al. Positive relationship between herbaceous layer diversity and the performance of soil biota in a temperate forest. Soil Biol Biochem 2011, 43:462-465.
17. Farrell M., Griffith G.W., Hobbs P.J., Perkins W.T., Jones D.L. Microbial diversity and activity are increased by compost amendment of metal-contaminated soil. FEMS Microbiol Ecol 2010, 71:94-105.
18. Garbeva P., van Elsas J., van Veen J. Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 2008, 302:19-32.
19. García-Palacios P., Bowker M.A., Chapman S.J., Maestre F.T., Soliveres S., Gallardo A., et al. Early-successional vegetation changes after roadside prairie restoration modify processes related with soil functioning by changing microbial functional diversity. Soil Biol Biochem 2011, 43:1245-1253.
20. Garland J.L., Mills A.L. Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 1991, 57:2351-2359.
21. Giller K.E., Witter E., McGrath S.P. Heavy metals and soil microbes. Soil Biol Biochem 2009, 41:2031-2037.
22. Gobran G.R., Clegg S. A conceptual model for nutrient availability in the mineral soil-root system. Can J Soil Sci 1996, 76:125-131.
23. Grayston S.J., Vaughan D., Jones D. Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 1997, 5:29-56.
24. Hinsinger P., Plassard C., Jaillard B. Rhizosphere: a new frontier for soil biogeochemistry. J Geochem Explor 2006, 88:210-213.
25. Hooper D.U., Bignell D.E., Brown V.K., Brussaard L., Dangerfield J.M., Wall D.H., et al. Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience 2000, 50:1049-1061.
26. Hooper D.U., Chapin F.S., Ewel J.J., Hector A., Inchausti P., Lavorel S., et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 2005, 75:3-35.
27. Kapusta P., Szarek-Łukaszewska G., Stefanowicz A.M. Direct and indirect effects of metal contamination on soil biota in a Zn-Pb post-mining and smelting area (S Poland). Environ Pollut 2011, 159:1516-1522.
28. Kowalchuk G.A., Buma D.S., de Boer W., Klinkhamer P.G.L., van Veen J.A. Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Anton Leeuw Int J G 2002, 81:509-520.
29. Kraus G.F., Druzhinina I., Gams W., Bissett J., Zafari D., Szakacs G., et al. Trichoderma brevicompactum sp. nov. Mycologia 2004, 96:1059-1073.
30. Lalande R., Gagnon B., Royer I. Impact of natural or industrial liming materials on soil properties and microbial activity. Can J Soil Sci 2009, 89:209-222.
31. Lamb E., Kennedy N., Siciliano S. Effects of plant species richness and evenness on soil microbial community diversity and function. Plant Soil 2011, 338:483-495.
32. 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.
33. Lepš J., Šmilauer P. Multivariate analysis of ecological data using CANOCO 2003, Cambridge University Press, Cambridge.
34. Liu Z., Fu B., Zheng X., Liu G. Plant biomass, soil water content and soil N:P ratio regulating soil microbial functional diversity in a temperate steppe: a regional scale study. Soil Biol Biochem 2010, 42:445-450.
35. Loranger-Merciris G., Barthes L., Gastine A., Leadley P. Rapid effects of plant species diversity and identity on soil microbial communities in experimental grassland ecosystems. Soil Biol Biochem 2006, 38:2336-2343.
36. Mahieu S., Frérot H., Vidal C., Galiana A., Heulin K., Maure L., et al. Anthyllis vulneraria/Mesorhizobium metallidurans, an efficient symbiotic nitrogen fixing association able to grow in mine tailings highly contaminated by Zn, Pb and Cd. Plant Soil 2011, 342:405-417.
37. Marquard E., Weigelt A., Temperton V.M., Roscher C., Schumacher J., Buchmann N., et al. Plant species richness and functional composition drive overyielding in a six-year grassland experiment. Ecology 2009, 90:3290-3302.
38. Marschner P., Crowley D., Yang C.H. Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 2004, 261:199-208.
39. McGrath S.P., Chaudri A.M., Giller K.E. Long-term effects of metals in sewage sludge on soils, microorganisms and plants. J Ind Microbiol Biotechnol 1995, 14:94-104.
40. Milcu A., Partsch S., Scherber C., Weisser W.W., Scheu S. Earthworms and legumes control litter decomposition in a plant diversity gradient. Ecology 2008, 89:1872-1882.
41. Mirek Z., Piekoś-Mirkowa H., Zajac A., Zajac M. Flowering plants and pteridophytes of Poland - a checklist 2002, W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków.
42. Mulder C.P.H., Jumpponen A., Högberg P., Huss-Danell K. How plant diversity and legumes affect nitrogen dynamics in experimental grassland communities. Oecologia 2002, 133:412-421.
43. Naeem S., Li S. Biodiversity enhances ecosystem reliability. Nature 1997, 390:507-509.
44. Naeem S., Loreau M., Inchausti P. Biodiversity and ecosystem functioning: the emergence of a synthetic ecological framework. Biodiversity and ecosystem functioning 2002, 3-11. Oxford University Press, Oxford. S. Naeem, M. Loreau, P. Inchausti (Eds.).
45. Niklińska M., Chodak M., Laskowski R. Characterization of the forest humus microbial community in a heavy metal polluted area. Soil Biol Biochem 2005, 37:2185-2194.
46. Olko A., Abratowska A., Zyłkowska J., Wierzbicka M., Tukiendorf A. Armeria maritima from a calamine heap - initial studies on physiologic-metabolic adaptations to metal-enriched soil. Ecotoxicol Environ Saf 2008, 69:209-218.
47. Rajapaksha R.M.C.P., Tobor-Kapłon M.A., Bååth E. Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 2004, 70:2966-2973.
48. Ramsey P.W., Rillig M.C., Feris K.P., Gordon N.S., Moore J.N., Holben W.E., et al. Relationship between communities and processes; new insights from a field study of a contaminated ecosystem. Ecol Lett 2005, 8:1201-1210.
49. Rodríguez-Loinaz G., Onaindia M., Amezaga I., Mijangos I., Garbisu C. Relationship between vegetation diversity and soil functional diversity in native mixed-oak forests. Soil Biol Biochem 2008, 40:49-60.
50. Rooney D., Clipson N. Phosphate addition and plant species alters microbial community structure in acidic upland grassland soil. Microb Ecol 2009, 57:4-13.
51. Rosenvald K., Kuznetsova T., Ostonen I., Truu M., Truu J., Uri V., et al. Rhizosphere effect and fine-root morphological adaptations in a chronosequence of silver birch stands on reclaimed oil shale post-mining areas. Ecol Eng 2011, 37:1027-1034.
52. Rousk J., Demoling L.A., Bahr A., Bååth E. Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol Ecol 2008, 63:350-358.
53. Rousk J., Brookes P.C., Bååth E. Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil. Soil Biol Biochem 2010, 42:926-934.
54. Sanaullah M., Blagodatskaya E., Chabbi A., Rumpel C., Kuzyakov Y. Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition. Appl Soil Ecol 2011, 48:38-44.
55. Schipper L.A., Lee W.G. Microbial biomass, respiration and diversity in ultramafic soils of West Dome, New Zealand. Plant Soil 2004, 262:151-158.
56. Shukurov N., Pen-Mouratov S., Steinberger Y. The impact of the Almalyk Industrial Complex on soil chemical and biological properties. Environ Pollut 2005, 136:331-340.
57. Spehn E.M., Joshi J., Schmid B., Alphei J., Körner C. Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 2000, 224:217-230.
58. Spehn E.M., Scherer-Lorenzen M., Schmid B., Hector A., Caldeira M.C., Dimitrakopoulos P.G., et al. The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen. Oikos 2002, 98:205-218.
59. Spehn E.M., Hector A., Joshi J., Scherer-Lorenzen M., Schmid B., Bazeley-White E., et al. Ecosystem effects of biodiversity manipulations in European grasslands. Ecol Monogr 2005, 75:37-63.
60. Stefanowicz A.M., Niklińska M., Laskowski R. Metals affect soil bacterial and fungal functional diversity differently. Environ Toxicol Chem 2008, 27:591-598.
61. Stefanowicz A.M., Niklińska M., Kapusta P., Szarek-Łukaszewska G. Pine forest and grassland differently influence the response of soil microbial communities to metal contamination. Sci Total Environ 2010, 408:6134-6141.
62. Stephan A., Meyer A.H., Schmid B. Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 2000, 88:988-998.
63. Teklay T., Shi Z., Attaeian B., Chang S.X. Temperature and substrate effects on C & N mineralization and microbial community function of soils from a hybrid poplar chronosequence. Appl Soil Ecol 2010, 46:413-421.
64. Temperton V., Mwangi P., Scherer-Lorenzen M., Schmid B., Buchmann N. Positive interactions between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment. Oecologia 2007, 151:190-205.
65. ter Braak C.J.F., Šmilauer P. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5) 2002, Microcomputer Power, Ithaca.
66. 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.
67. Walker B.H. Biodiversity and ecological redundancy. Conserv Biol 1992, 6:18-23.
68. Wardle D.A., Bardgett R.D., Klironomos J.N., Setälä H., van der Putten W.H., Wall D.H. Ecological linkages between aboveground and belowground biota. Science 2004, 304:1629-1633.
69. Wierzbicka M., Panufnik D. The adaptation of Silene vulgaris to growth on a calamine waste heap (S. Poland). Environ Pollut 1998, 101:415-426.
70. Wierzbicka M., Pielichowska M. Adaptation of Biscutella laevigata L, a metal hyperaccumulator, to growth on a zinc-lead waste heap in southern Poland. I: differences between waste-heap and mountain populations. Chemosphere 2004, 54:1663-1674.
71. Zak D.R., Holmes W.E., White D.C., Peacock A.D., Tilman D. Plant diversity, soil microbial communities, and ecosystem function: are there any links?. Ecology 2003, 84:2042-2050.
72. Załecka R., Wierzbicka M. The adaptation of Dianthus carthusianorum L. (Caryophyllaceae) to growth on a zinc-lead heap in southern Poland. Plant Soil 2002, 246:249-257.
73. Zhang Y., Zhang H.-W., Su Z.-C., Zhang C.-G. Soil microbial characteristics under long-term heavy metal stress: a case study in Zhangshi wastewater irrigation area, Shenyang. Pedosphere 2008, 18:1-10.