Abstract
Due to the emerging environmental issues related to heavy metals, concern about the soil quality of farming lands near manufacturing district is increasing. Investigating the function of soil microorganisms exposed to long-term heavy metal contamination is meaningful and important for agricultural soil utilization. This article studied the potential influence of several heavy metals on microbial biomass, activity, abundance, and community composition in arable soil near industrial estate in Zhuzhou, Hunan province, China. The results showed that soil organic contents (SOC) were significantly positive correlated with heavy metals, whereas dehydrogenase activity (DHA) was greatly depressed by the heavy metal stress. Negative correlation was found between heavy metals and basal soil respiration (BSR), and no correlation was found between heavy metals and microbial biomass content (MBC). The quantitative PCR (QPCR) and polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) analysis could suggest that heavy metal pollution has significantly decreased abundance of bacteria and fungi and also changed their community structure. The results could contribute to evaluate heavy metal pollution level in soil. By combining different environmental parameters, it would promote the better understanding of heavy metal effect on the size, structure, and activity of microbial community in arable soil.
Similar content being viewed by others
References
Abaye DA, Lawlor K, Hirsch PR, Brookes PC (2005) Changes in the microbial community of an arable soil caused by long-term metal contamination. Eur J Soil Sci 56(1):93–102. doi:10.1111/j.1365-2389.2004.00648.x
Aceves MB, Grace C, Ansorena J, Dendooven L, Brookes P (1999) Soil microbial biomass and organic C in a gradient of zinc concentrations in soils around a mine spoil tip. Soil Biol Biochem 31(6):867–876. doi:10.1016/S0038-0717(98)00187-4
Akcay H, Oguz A, Karapire C (2003) Study of heavy metal pollution and speciation in Buyak Menderes and Gediz river sediments. Water Res 37(4):813–822. doi:10.1016/S0043-1354(02)00392-5
Anderson JPE, Domsch KH (1973) Quantification of bacterial and fungal contributions to soil respiration. Arch Microbiol 93(2):113–127. doi:10.1007/BF00424942
Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations (a review). Water Air Soil Poll 47(3–4):335–379. doi:10.1007/BF00279331
Cebron A, Arsene-Ploetze F, Bauda P, Bertin PN, Billard P, Carapito C, Devin S, Goulhen-Chollet F, Poirel J, Leyval C (2014) Rapid impact of phenanthrene and arsenic on bacterial community structure and activities in sand batches. Microb Ecol 67(1):129–144. doi:10.1007/s00248-013-0313-1
Chen JH, He F, Zhang XH, Sun X, Zheng JF, Zheng JW (2014) Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiol Ecol 87(1):164–181. doi:10.1111/1574-6941.12212
Eguchi M, Ostrowski M, Fegatella F, Bowman J, Nichols D, Nishino T, Cavicchioli R (2001) Sphingomonas alaskensis strain AFO1, an abundant oligotrophic ultramicrobacterium from the North Pacific. Appl Environ Microbiol 67(11):4945–4954. doi:10.1128/Aem.67.11.4945-4954.2001
Frey SD, Six J, Elliott ET (2003) Reciprocal transfer of carbon and nitrogen by decomposer fungi at the soil-litter interface. Soil Biol Biochem 35(7):1001–1004. doi:10.1016/S0038-0717(03)00155-X
Frische T, Hoper H (2003) Soil microbial parameters and luminescent bacteria assays as indicators for in situ bioremediation of TNT-contaminated soils. Chemosphere 50(3):415–427. doi:10.1016/S0045-6535(02)00603-3
Frostegård Å, Tunlid A, Bååth E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28(1):55–63. doi:10.1016/0038-0717(95)00100-X
Galli U, Schüepp H, Brunold C (1994) Heavy metal binding by mycorrhizal fungi. Physiol Plant 92(2):364–368. doi:10.1111/j.1399-3054.1994.tb05349.x
Ge CR, Zhang QC (2011) Microbial community structure and enzyme activities in a sequence of copper-polluted soils. Pedosphere 21(2):164–169. doi:10.1016/S1002-0160(11)60114-8
Gong JL, Wang B, Zeng GM, Yang CP, Niu CG, Niu QY, Zhou WJ, Liang Y (2009) Removal of cationic dyes from aqueous solution using magnetic multi-wall carbon nanotube nanocomposite as adsorbent. J Hazard Mater 164(2–3):1517–1522. doi:10.1016/j.jhazmat.2008.09.072
Gremion F, Chatzinotas A, Kaufmann K, Sigler W, Harms H (2004) Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS Microbiol Ecol 48(2):273–283. doi:10.1016/j.femsec.2004.02.004
Gupta V, Germida J (1988) Distribution of microbial biomass and its activity in different soil aggregate size classes as affected by cultivation. Soil Biol Biochem 20(6):777–786. doi:10.1016/0038-0717(88)90082-X
Insam H (2001) Developments in soil microbiology since the mid 1960s. Geoderma 100(3):389–402. doi:10.1016/S0016-7061(01)00029-5
Jiang M, Zeng GM, Zhang C, Ma XY, Chen M, Zhang JC, Lu LH, Yu Q, Hu LP, Liu LF (2013) Assessment of heavy metal contamination in the surrounding soils and surface sediments in Xiawangang River, Qingshuitang District. PloS one 8(8) doi:10.1371/journal.pone.0071176
Joynt J, Bischoff M, Turco R, Konopka A, Nakatsu CH (2006) Microbial community analysis of soils contaminated with lead, chromium and petroleum hydrocarbons. Microb Ecol 51(2):209–219. doi:10.1007/s00248-005-0205-0
Kelly J, Häggblom M, Tate R III (1999) Changes in soil microbial communities over time resulting from one time application of zinc: a laboratory microcosm study. Soil Biol Biochem 31(10):1455–1465. doi:10.1016/S0038-0717(99)00059-0
Khan S, Hesham AEL, Qiao M, Rehman S, He JZ (2010) Effects of Cd and Pb on soil microbial community structure and activities. Environ Sci Pollut Res Int 17(2):288–296. doi:10.1007/s11356-009-0134-4
Kızılkaya R, Aşkın T, Bayraklı B, Sağlam M (2004) Microbiological characteristics of soils contaminated with heavy metals. Eur J Soil Sci 40(2):95–102. doi:10.1016/j.ejsobi.2004.10.002
Leirós MC, Trasar-Cepeda C, Seoane S, Gil-Sotres F (2000) Biochemical properties of acid soils under climax vegetation (Atlantic oakwood) in an area of the European temperate–humid zone (Galicia, NW Spain): general parameters. Soil Biol Biochem 32(6):733–745. doi:10.1016/S0038-0717(99)00195-9
Liu YZ, Zhou T, Crowley D, Li LQ, Liu DW, Zheng JW, Yu XY, Pan GX, Hussain Q, Zhang XH, Zheng JF (2012) Decline in topsoil microbial quotient, fungal abundance and C utilization efficiency of rice paddies under heavy metal pollution across South China. PLoS One 7(6):e38858. doi:10.1371/journal.pone.0038858
Lobinski R, Boutron CF, Candelone JP, Hong S, Szpunar-Lobinska J, Adams FC (1994) Present century snow core record of organolead pollution in Greenland. Environ Sci Technol 28(8):1467–1471. doi:10.1021/es00057a014
Lu LH, Zeng GM, Fan CZ, Zhang JC, Chen AW, Chen M, Jiang M, Yuan YJ, Wu HP, Lai MY, He YB (2014) Diversity of two-domain laccase-like multicopper oxidase genes in Streptomyces spp. identification of genes potentially involved in extracellular activities and lignocellulose degradation during composting of agricultural waste. Appl Environ Microbiol 80(11):3305–3314. doi:10.1128/aem.00223-14
Mitchell JI, Zuccaro A (2006) Sequences, the environment and fungi. Mycologist 20(2):62–74. doi:10.1016/j.mycol.2005.11.004
Niklińska M, Chodak M, Laskowski R (2006) Pollution-induced community tolerance of microorganisms from forest soil organic layers polluted with Zn or Cu. Appl Soil Ecol 32(3):265–272. doi:10.1016/j.apsoil.2005.08.002
Ok YS, Usman ARA, Lee SS, Abd El-Azeem SAM, Choi B, Hashimoto Y, Yang JE (2011) Effects of rapeseed residue on lead and cadmium availability and uptake by rice plants in heavy metal contaminated paddy soil. Chemosphere 85(4):677–682. doi:10.1016/j.chemosphere.2011.06.073
Oliveira A, Pampulha ME (2006) Effects of long-term heavy metal contamination on soil microbial characteristics. J Biosci Bioeng 102(3):157–161. doi:10.1263/jbb.102.157
Ovreås L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63(9):3367–3373
Park JH, Lamb D, Paneerselvam P, Choppala G, Bolan N, Chung JW (2011) Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. J Hazard Mater 185(2–3):549–574. doi:10.1016/j.jhazmat.2010.09.082
Ronnenberg K, Wesche K (2011) Effects of fertilization and irrigation on productivity, plant nutrient contents and soil nutrients in southern Mongolia. Plant Soil 340(1–2):239–251. doi:10.1007/s11104-010-0409-z
Sabater S, Buchaca T, Cambra J, Catalan J, Guasch H, Ivorra N, Munoz I, Navarro E, Real M, Romani A (2003) Structure and function of benthic algal communities in an extremely acid river. J Phycol 39(3):481–489. doi:10.1046/j.1529-8817.2003.02104.x
Sanderson P, Naidu R, Bolan N, Bowman M, Mclure S (2012) Effect of soil type on distribution and bioaccessibility of metal contaminants in shooting range soils. Sci Total Environ 438:452–462. doi:10.1016/j.scitotenv.2012.08.014
Serra-Wittling C, Houot S, Barriuso E (1995) Soil enzymatic response to addition of municipal solid-waste compost. Biol Fert Soils 20(4):226–236. doi:10.1007/BF00336082
Smolders E, Buekers J, Oliver I, McLaughlin MJ (2004) Soil properties affecting toxicity of zinc to soil microbial properties in laboratory-spiked and field-contaminated soils. Environ Toxicol Chem 23(11):2633–2640. doi:10.1897/04-27
Solís-Domínguez FA, Valentín-Vargas A, Chorover J, Maier RM (2011) 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 409(6):1009–1016. doi:10.1016/j.scitotenv.2010.11.020
Stefanowicz AM, Niklińska M, Laskowski R (2008) Metals affect soil bacterial and fungal functional diversity differently materials and methods. Environ Toxicol Chem 27(3):591–598. doi:10.1897/07-288.1
Tang WW, Zeng GM, Gong JL, Liang J, Xu P, Zhang C, Huang BB (2014) Impact of humic/fulvic acid on the removal of heavy metals from aqueous solutions using nanomaterials: A review. Sci Total Environ 468:1014–1027. doi:10.1016/j.scitotenv.2013.09.044
Tonkovic Z (1998) Energetics of enhanced biological phosphorus and nitrogen removal processes. Water Sci Technol 38(1):177–184. doi:10.1016/S0273-1223(98)00402-8
Van de Velde K, Vallelonga P, Candelone JP, Rosman KJR, Gaspari V, Cozzi G, Barbante C, Udisti R, Cescon P, Boutron CF (2005) Pb isotope record over one century in snow from Victoria Land, Antarctica. Earth Planet Sc Lett 232(1–2):95–108. doi:10.1016/j.epsl.2005.01.007
Vance ED, Brokes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707. doi:10.1016/0038-0717(87)90052-6
Wang YP, Shi JY, Wang H, Lin Q, Chen XC, Chen YX (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotox Environ Safe 67(1):75–81. doi:10.1016/j.ecoenv.2006.03.007
Welp G (1999) Inhibitory effects of the total and water-soluble concentrations of nine different metals on the dehydrogenase activity of a loess soil. Biol Fert Soils 30(1–2):132–139. doi:10.1007/s003740050599
Wen F, Hou H, Yao N, Yan ZG, Bai LP, Li FS (2013) Effects of simulated acid rain, EDTA, or their combination, on migration and chemical fraction distribution of extraneous metals in Ferrosol. Chemosphere 90(2):349–357. doi:10.1016/j.chemosphere.2012.07.027
Wu J, Zhang H, He PJ, Shao LM (2011) Insight into the heavy metal binding potential of dissolved organic matter in MSW leachate using EEM quenching combined with PARAFAC analysis. Water Res 45(4):1711–1719. doi:10.1016/j.watres.2010.11.022
Xu P, Zeng GM, Huang DL, Feng CL, Hu S, Zhao MH, Lai C, Wei Z, Huang C, Xie GX, Liu ZF (2012) Use of iron oxide nanomaterials in wastewater treatment: a review. Sci Total Environ 424:1–10. doi:10.1016/j.scitotenv.2012.02.023
Xu P, Leng Y, Zeng GM, Huang DL, Lai C, Zhao MH, Wei Z, Li NJ, Huang C, Zhang C, Li FN, Cheng M (2015) Cadmium induced oxalic acid secretion and its role in metal uptake and detoxification mechanisms in Phanerochaete chrysosporium. Appl Microbiol Biotechnol 99(1):435–443. doi:10.1007/s00253-014-5986-y
Zeng GM, Chen M, Zeng ZT (2013a) Risks of neonicotinoid pesticides. Science 340(6139):1403–1403
Zeng GM, Chen M, Zeng ZT (2013b) Shale gas: surface water also at risk. Nature 499(7457):154–154
Zhang JC, Zeng GM, Chen YN, Yu M, Yu Z, Li H, Yu Y, Huang HL (2011) Effects of physico-chemical parameters on the bacterial and fungal communities during agricultural waste composting. Bioresour Technol 102(3):2950–2956. doi:10.1016/j.biortech.2010.11.089
Zheng SA, Zhang MK (2011) Effect of moisture regime on the redistribution of heavy metals in paddy soil. J Environ Sci-China 23(3):434–443. doi:10.1016/S1001-0742(10)60428-7
Acknowledgments
The authors thank the editors and reviewers for very helpful comments and suggestions. This study was financially supported by the National Natural Science Foundation of China (51378190, 50908079, and 51039001), the Hunan Provincial Natural Science Foundation of China (10JJ7005), the Scholarship Award for Excellent Doctoral Student granted by Ministry of Education.
Conflict of interest
None of the authors has any financial or personal relationships that could inappropriately influence or bias the content of the paper.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Deng, L., Zeng, G., Fan, C. et al. Response of rhizosphere microbial community structure and diversity to heavy metal co-pollution in arable soil. Appl Microbiol Biotechnol 99, 8259–8269 (2015). https://doi.org/10.1007/s00253-015-6662-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-015-6662-6