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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

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2018 Impact Factor: 3.883

Front Envir Sci Eng    2012, Vol. 6 Issue (2) : 213-223    https://doi.org/10.1007/s11783-011-0345-z
RESEARCH ARTICLE
Plant diversity reduces the effect of multiple heavy metal pollution on soil enzyme activities and microbial community structure
Yang GAO1,4(), Chiyuan MIAO2(), Jun XIA1, Liang MAO4, Yafeng WANG3, Pei ZHOU4
1. Key Laboratory of Water Cycle and Related Land Surface Processes, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China; 2. State Key Laboratory of Earth Surface Processes and Resource Ecology, College of Global Change and Earth System Science, Beijing Normal University, Beijing 100875, China; 3. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; 4. School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
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Abstract

It is unclear whether certain plant species and plant diversity could reduce the impacts of multiple heavy metal pollution on soil microbial structure and soil enzyme activities. Random amplified polymorphic DNA (RAPD) was used to analyze the genetic diversity and microbial similarity in planted and unplanted soil under combined cadmium (Cd) and lead (Pb) pollution. A metal hyperaccumulator, Brassica juncea, and a common plant, Festuca arundinacea Schreb, were used in this research. The results showed that microorganism quantity in planted soil significantly increased, compared with that in unplanted soil with Cd and Pb pollution. The order of microbial community sensitivity in response to Cd and Pb stress was as follows: actinomycetes>bacteria>fungi. Respiration, phosphatase, urease and dehydrogenase activity were significantly inhibited due to Cd and Pb stress. Compared with unplanted soil, planted soils have frequently been reported to have higher rates of microbial activity due to the presence of additional surfaces for microbial colonization and organic compounds released by the plant roots. Two coexisting plants could increase microbe population and the activity of phosphatases, dehydrogenases and, in particular, ureases. Soil enzyme activity was higher in B. juncea phytoremediated soil than in F. arundinacea planted soil in this study. Heavy metal pollution decreased the richness of the soil microbial community, but plant diversity increased DNA sequence diversity and maintained DNA sequence diversity at high levels. The genetic polymorphism under heavy metal stress was higher in B. juncea phytoremediated soil than in F. arundinacea planted soil.

Keywords enzyme activity      soil DNA      microbial population      plant diversity      heavy metal     
Corresponding Author(s): GAO Yang,Email:gaoyang@igsnrr.ac.cn, gaoyang@163.com; MIAO Chiyuan,Email:miaocy@vip.sina.com   
Issue Date: 01 April 2012
 Cite this article:   
Yang GAO,Jun XIA,Liang MAO, et al. Plant diversity reduces the effect of multiple heavy metal pollution on soil enzyme activities and microbial community structure[J]. Front Envir Sci Eng, 2012, 6(2): 213-223.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-011-0345-z
https://academic.hep.com.cn/fese/EN/Y2012/V6/I2/213
sample No.factors
Cd10Cd25Pb200Pb500B. junceaF. arundinacea
A100001
B000101
C011001
D010010
E001010
F010110
G010011
H000111
I010111
J010000
K001000
L010100
M000010
N000001
O000011
P000000
Tab.1  Experimental design for 6 factors and 2 levels
No. of primerssequences of primerspercentage of GC
S1GTTTCGCTCC60
S2CTGCTGGGAC70
S3TCTCCCTCAG60
S4TCCGCAACCA60
S5CACTTCCGCT60
S6GGTTACTGCC60
S7CTCCCCAGAC70
S8TTGCAGGCAG60
S9GTAAGCCCCT60
S10GTAAGCCCGT60
Tab.2  Sequences of ten primers used in this experiment
Fig.1  Microbial diversity of different treatments
Fig.2  Changes of (a) soil respiration, (b) phosphatase, (c) urease, (d) dehydrogenase at 14, 35 and 70 days in different treatments
No.ABCDEFGHIJKLMNOP
ababababababababababababababab
S10221100211212311011102010111219
S21123322221222331221221112223418
S312022221132211322222211122232410
S42221111122210031231213113113326
S52121122222132112212212211331238
S60112201301211232240101022113237
S712211222222322123211121133311210
S82111121111002202132121211010218
S91112212122212313111203121212129
S102211121213132112300212022322127
total1215141513141417141816171618171818191116101891317181719202182
a + b272927313233343537272822353641
P/%32.935.432.937.839.040.241.542.745.132.934.126.842.743.950.0
Tab.3  Changes of total bands, polymorphic bands, and varied bands under different treatments
Fig.3  The RAPD fingerprints of primer S4 from sample A to P
No.ABCDEFGHIJKLMNO
B0.63
C0.540.58
D0.480.440.50
E0.460.490.520.65
F0.450.530.470.680.64
G0.560.620.610.580.540.63
H0.480.570.590.610.540.580.66
I0.490.530.560.620.580.660.700.65
J0.370.320.360.400.360.410.380.400.42
K0.330.310.370.390.420.430.360.380.410.71
L0.350.390.440.420.390.450.390.400.390.740.78
M0.670.650.680.720.740.760.680.740.760.530.560.52
N0.620.570.680.770.730.790.690.720.730.490.540.540.82
O0.580.670.590.720.740.690.650.710.670.450.510.480.780.83
P0.560.610.620.650.670.630.710.640.690.520.490.420.740.790.81
Tab.4  Coefficients of microbial community DNA sequence similarity of different soil samples
Fig.4  Interactions among microorganisms and macro-organisms in soils
1 Viketoft M, Palmborg C, Sohlenius B, Huss-Danell K, Bengtsson J. Plant species effects on soil nematode communities in experimental grasslands. Applied Soil Ecology , 2005, 30(2): 90-103
doi: 10.1016/j.apsoil.2005.02.007
2 Chen X, Tang J J, Fang Z G, Shimizu K. Effects of weed communities with various species numbers on soil features in a subtropical orchard ecosystem. Agriculture Ecosystems & Environment , 2004, 102(3): 377-388
doi: 10.1016/j.agee.2003.08.006
3 Gao Y, Miao C Y, Mao L, Zhou P, Jin Z G, Shi W J. Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. Journal of Hazardous Materials , 2010, 181(1-3): 771-777
doi: 10.1016/j.jhazmat.2010.05.080 pmid:20566243
4 Nguyen C. Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie , 2003, 23(5-6): 375-396
doi: 10.1051/agro:2003011
5 Broughton L C, Gross K L. Patterns of diversity in plant and soil microbial communities along a productivity gradient in a Michigan old field. Oecologia , 2000, 125(3): 420-427
doi: 10.1007/s004420000456
6 Stephan A, Meyer A H, Schmid B. Plant diversity affects culturable soil bacteria in experimental grassland communities. Journal of Ecology , 2000, 88(6): 988-998
doi: 10.1046/j.1365-2745.2000.00510.x
7 Martens D A, Johanson J B, Frankerberger W T Jr. Production and persistence of soil enzymes with repeated addition of organic residues. Soil Science , 1992, 153(1): 53-61
doi: 10.1097/00010694-199201000-00008
8 Quartacci M F, Argilla A, Baker A J M, Navari-Izzo F. Phytoextraction of metals from a multiply contaminated soil by Indian mustard. Chemosphere , 2006, 63(6): 918-925
doi: 10.1016/j.chemosphere.2005.09.051 pmid:16307777
9 Dick R P. Soil enzyme activities as integrative indicators of soil health. In: Pankhurst C E, Doube B M, Gupta V V S R, eds. Biological Indicators of Soil Health . Wallingford: CAB International, 1997, 121-156
10 Bending G D, Turner M K, Rayns F, Marx M C, Wood M. Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes. Soil Biology & Biochemistry , 2004, 36(11): 1785-1792
doi: 10.1016/j.soilbio.2004.04.035
11 Caldwell B A. Enzyme activities as a component of soil biodiversity: a review. Pedobiologia , 2005, 49(6): 637-644
doi: 10.1016/j.pedobi.2005.06.003
12 Gao Y, Zhou P, Mao L, Zhi Y E, Shi W J. Assessment of effects of heavy metals combined pollution on soil enzyme activities and microbial community structure: modified ecological dose-response model and PCR-RAPD. Environment Earth Science , 2010, 60(3): 603-612
doi: 10.1007/s12665-009-0200-8
13 Brookes P. The use of microbial parameters in monitoring soil pollution by heavy metals. Biology and Fertility of Soils , 1995, 19(4): 269-279
doi: 10.1007/BF00336094
14 Muhammad A, Wang H Z, Wu J J, Xu J M, Xu D F. Changes in enzymes activity, substrate utilization pattern and diversity of soil microbial communities under cadmium pollution. Journal of Environmental Sciences (China) , 2005, 17(5): 802-807
pmid:16313007
15 Yang R Y, Tang J J, Chen X, Hu S J. Effects of coexisting plant species on soil microbes and soil enzymes in metal lead contaminated soils. Applied Soil Ecology , 2007, 37(3): 240-246
doi: 10.1016/j.apsoil.2007.07.004
16 Schl?pfer F, Schmid B. Ecosystem effects of biodiversity: a classification of hypotheses and exploration of empirical results. Ecological Applications , 1999, 9(3): 893-912
doi: 10.1890/1051-0761(1999)009[0893:EEOBAC]2.0.CO;2
17 Gao Y, Mao L, Miao C Y, Zhou P, Cao J J, Zhi Y E, Shi W J. Spatial characteristics of soil enzyme activities and microbial community structure under different land uses in Chongming Island, China: geostatistical modelling and PCR-RAPD method. The Science of the Total Environment , 2010, 408(16): 3251-3260
doi: 10.1016/j.scitotenv.2010.04.007 pmid:20435338
18 Atienzar F A, Venier P, Jha A N, Depledge M H. Evaluation of the random amplified polymorphic DNA (RAPD) assay for the detection of DNA damage and mutations. Mutation Research , 2002, 521(1-2): 151-163
pmid:12438012
19 Liu W, Li P J, Qi X M, Zhou Q X, Zheng L, Sun T H, Yang Y S. DNA changes in barley (Hordeum vulgare) seedlings induced by cadmium pollution using RAPD analysis. Chemosphere , 2005, 61(2): 158-167
doi: 10.1016/j.chemosphere.2005.02.078 pmid:16168739
20 Gao Y, Zhou P, Mao L, Zhi Y E, Zhang C, Shi W. Effects of plant species coexistence on soil enzyme activities and soil microbial community structure under Cd and Pb combined pollution. Journal of Environmental Sciences , 2010, 22(7): 1040-1048
doi: 10.1016/S1001-0742(09)60215-1 pmid:21174994(in Chinese)
21 Nair S K, Subba-Rao N S. Microbiology of the root region of coconut and cacao under mixed cropping. Plant and Soil , 1977, 46(3): 511-519
doi: 10.1007/BF00015910
22 Allen O N. Experiments in Soil Bacteriology, 3rd ed. Minneapolis: Burgess Publisher Company, 1959
23 Martin J P. Use of acid, rose bengal and streptomycin in the plate method for estimating soil fungi. Soil Science , 1950, 69(3): 215-232
doi: 10.1097/00010694-195003000-00006
24 Jensen H I. Notes on the biology of Azotobacter. Proceeding of the Society Applied Bacteriology , 1951, 14(1): 89-94
25 Bringmark E, Bringmark L. Standard Respiration, a Method to Test the Influence of Pollution and Environmental Factors on a Large Number of Sample. Stockholm: Swedish Environmental Protection Agency, 1993, 4262
26 Tabatabai M A, Bremner J M. Assay of urease activity in soils. Soil Biology & Biochemistry , 1972, 4(4): 479-487
doi: 10.1016/0038-0717(72)90064-8
27 Tabatabai M A, Bremner J M. Use of p-nitrophenyl phosphatefor assay of soil phosphatase activity. Soil Biology & Biochemistry , 1969, 1(4): 301-307
doi: 10.1016/0038-0717(69)90012-1
28 Wang Y P, Shi J K, Wang H, Lin Q, Chen X C, Chen Y X. The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicology and Environmental Safety , 2007, 67(1): 75-81
doi: 10.1016/j.ecoenv.2006.03.007 pmid:16828162
29 Nei M, Li W H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America , 1979, 76(10): 5269-5273
doi: 10.1073/pnas.76.10.5269 pmid:291943
30 Lavelle P, Lattaud C, Trigo D, Barois I. Mutualism and biodiversity in soils. Plant and Soil , 1995, 170(1): 23-33
doi: 10.1007/BF02183052
31 Renella G, Mench M, Gelsomin A, Landi L, Nannipieri P. Functional activity and microbial community structure in soils amended with bimetallic sludges. Soil Biology & Biochemistry , 2005, 37(8): 1498-1506
doi: 10.1016/j.soilbio.2005.01.013
32 Gao Y, Mao L, Zhou P, Zhi Y E, Zhang C H. Effect of plant growth on soil enzyme activity and microbe community structure under Cd and Pb stress. Acta Scientiarum Naturalium Universitatis Pekinensis , 2010, 46(3): 339-345 (In Chinese)
33 Fliessbach A, Martens R, Reber H H. Soil microbial biomass and activity in soils treated with heavy metal contaminated sewage sludge. Soil Biology & Biochemistry , 1994, 26(9): 1201-1205
doi: 10.1016/0038-0717(94)90144-9
34 Frosteg?rd ?, Tunlid A, B??th E. Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biology & Biochemistry , 1996, 28(1): 55-63
doi: 10.1016/0038-0717(95)00100-X
35 Walker C, Goodyear C, Anderson D, Titball R W. Identification of arsenic resistant bacteria in the soil of a former munitions factory at Locknitz Germany. Land Contamination and Reclamation , 2000, 8(1): 13-18
36 Lorenz N, Hintemann T, Kramarewa T, Katayama A, Yasuta T, Marschner P, Kandeler E. Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biology & Biochemistry , 2006, 38(6): 1430-1437
doi: 10.1016/j.soilbio.2005.10.020
37 Wardle D A, Bonner K I, Barker G M, Yeates G W, Nicholson K S, Bardgett R D, Watson R N, Ghani A. Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecological Monographs , 1999, 69(4): 535-568
doi: 10.1890/0012-9615(1999)069[0535:PRIPGV]2.0.CO;2
38 Caravaca F, Aiguacil M M, Torres P, Roldán A. Plant type mediates rhizospheric microbial activities and soil aggregation in a semiarid Mediterranean salt marsh. Geoderma , 2005, 124(3-4): 375-382
doi: 10.1016/j.geoderma.2004.05.010
39 Garcia C, Roldan A, Hernandez T. Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma , 2005, 124(1-2): 193-202
doi: 10.1016/j.geoderma.2004.04.013
40 Speir T W, Ross D J. Hydrolytic enzyme activities to assess soil degradation and recovery. In: Burns R G, Dick R P, eds. Enzymes in the Environment . New York: Marcel Dekker, 2002, 407-431
41 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(8): 2042-2050
doi: 10.1890/02-0433
42 Kowalchuk G A, Buna 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 soilborne microorganisms. Antonie Van Leeuwenhoek International Journal of General and Molecular Micro , 2002, 81(1): 509-520
doi: 10.1023/A:1020565523615
43 Waisberg M, Joseph P, Hale B, Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology , 2003, 192(2-3): 95-117
doi: 10.1016/S0300-483X(03)00305-6 pmid:14580780
44 Ates I, Sinan Suzen H, Aydin A, Karakaya A. The oxidative DNA base damage in testes of rats after intraperitoneal cadmium injection. Biometals , 2004, 17(4): 371-377
doi: 10.1023/B:BIOM.0000029416.95488.5f pmid:15259357
45 Atienzar F A, Cordi M, Evenden A J,Jha A N, Depledge M H. Qualitative assessment of genotoxicity using random amplified polymorphic DNA: comparison of genomic template stability with key fitness parameters in Daphnia magna exposed to benzo[a]pyrene. Environmental Toxicology and Chemistry , 1999, 18(10): 2275-2282
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