Abstract
Background and aims
Microbial properties are often used to assess the recovery of soil health during phytoremediation. A field survey was conducted to test the effects of different plant metallophytes (excluder and hyperaccumulator) on soil microbial characteristics.
Methods
Microbial properties in the rhizosphere of four metallophytes (Sedum alfredii, Rubus hunanensis, Lysimachia christinae and Clinopodium gracile) growing naturally on highly Cd-, Zn- and Pb-contaminated soils were investigated. Microbial biomass carbon, basal respiration, enzyme activities and phospholipid fatty acids were analyzed to study microbial community function and composition.
Results
The total microbial biomass, bacterial, actinomycete, fungal, and protozoan PLFAs, basal respiration and enzyme activities in the rhizosphere of metallophytes were significantly higher than in bulk soil. Moreover, the largest increases were found in the rhizosphere of the hyperaccumulator S. alfredii. The microbial community composition in the rhizosphere of S. alfredii was significantly different from the other 3 plants. Redundancy analysis showed that soil physico-chemical properties such as metal concentrations, labile carbon and pH explained most of the variation in microbial community biomass, activity and structure.
Conclusions
Metallophytes using different strategies to adapt to metal-rich soils induced different effects on soil microbial properties, which were also influenced by physico-chemical characteristics.
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References
Aghababaei F, Raiesi F, Hosseinpur A (2014) The combined effects of earthworms and arbuscular mycorrhizal fungi on microbial biomass and enzyme activities in a calcareous soil spiked with cadmium. Appl Soil Ecol 75:33–42
Álvarez-López V, Prieto-Fernandez A, Becerra-Castro C, Monterroso C, Kidd PS (2016) Rhizobacterial communities associated with the flora of three serpentine outcrops of the Iberian Peninsula. Plant Soil 403:233–252
Baker AJM (1981) Accumulators and excluders-strategies in theresponse of plants to heavy metals. J Plant Nutr 3:643–654
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
Breulmann M, Schulz E, Weißhuhn K, Buscot F (2012) Impact of the plant community composition on labile soil organic carbon, soil microbial activity and community structure in semi-natural grassland ecosystems of different productivity. Plant Soil 352:253–265
Brooks DD, Twieg BD, Grayston SJ, Jones MD (2013) Physical extent, frequency, and intensity of phosphatase activity varies on soil profiles across a Douglas-fir chronosequence. Soil Biol Biochem 64:1–8
Burges A, Epelde L, Garbisu C (2015) Impact of repeated single-metal and multi-metal pollution events on soil quality. Chemosphere 120:8–15
Cang L, Zhou DM, Wang QY, Wu DY (2009) Effects of electrokinetic treatment of a heavy metal contaminated soil on soil enzyme activities. J Hazard Mater 172:1602–1607
Carrasco L, Gattinger A, Fließbach A, Roldán A, Schloter M, Caravaca F (2010) Estimation by PLFA of microbial community structure associated with the rhizosphere of Lygeum spartum and Piptatherum miliaceumgrowing in semiarid mine tailings. Microb Ecol 60:265–271
Chaudhary DR, Gautam RK, Yousuf B, Mishra A, Jha B (2015) Nutrients, microbial community structure and functional gene abundance of rhizosphere and bulk soils of halophytes. Appl Soil Ecol 91:16–26
Chemidlin Prévost-Bouré N, Soudani K, Damesin C, Berveiller D, Lata JC, Dufrêne E (2010) Increase in aboveground fresh litter quantity over-stimulates soil respiration in a temperate deciduous forest. Appl Soil Ecol 46:26–34
Ciadamidaro L, Madejón P, Madejón E (2014) Soil chemical and biochemical properties under Populusalba growing: three years study in trace element contaminated soils. Appl Soil Ecol 73:26–33
Colzi I, Rocchi S, Rangoni M, Del Bubba M, Gonnelli C (2014) Specificity of metal tolerance and use of excluder metallophytes for the phytostabilization of metal polluted soils: the case of Sileneparadoxa L. Environ Sci Pollut R 21:10960–10969
Dai J, Becquer T, Rouiller JH, Reversat G, Bernhard-Reversat F, Nahmani J, Lavelle P (2004) Heavy metal accumulation by two earthworm species and its relationship to total and DTPA-extractable metals in soils. Soil Biol Biochem 36:91–98
De la Iglesia R, Castro D, Ginocchio R, van der Lelie D, González B (2006) Factors influencing the composition of bacterial communities found at abandoned copper-tailings dumps. J Appl Microbiol 100:537–544
Delorme TA, Gagliardi JV, Angle JS, Chaney RL (2001) Influence of the zinc hyperaccumulator Thlaspi caerulescens J.&C. Presl. and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can J Microbiol 47:773–776
Epelde L, Mijangos I, Becerril JM, Garbisu C (2009) Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol Biochem 41:1788–1794
Epelde L, Becerril JM, Barrutia O, González-Oreja JA, Garbisu C (2010) Interactions between plant and rhizosphere microbial communities in a metalliferous soil. Environ Pollut 158:1576–1583
Epelde L, Lanzén A, Blanco F, Urich T, Garbisu C (2015) Adaptation of soil microbial community structure and function to chronic metal contamination at an abandoned Pb-Zn mine. FEMS Microbiol Ecol 91:1–11
Epelde L, Muñiz O, Garbisu C (2016) Microbial properties for the derivation of critical risk limits in cadmium contaminated soil. Appl Soil Ecol 99:19–28
Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837
Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65
Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass and activity of microbial communities fromtwo soil types experimentally exposed to different heavy metal. Appl Environ Microbiol 59:3605–3617
Ge Y, Zhang C, Jiang Y, Yue C, Jiang Q, Min H, Fan H, Zeng Q, Chang J (2011) Soil microbial abundances and enzyme activities in different rhizospheres in an integrated vertical flow constructed wetland. CLEAN Soil Air Water 39:206–211
Gianfreda L (2015) Enzymes of importance to rhizosphere processes. J Soil Sci Plant Nutr 15:283–306
Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414
Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378
Gremion F, Chatzinotas A, Harms H (2003) Comparative 16s rDNA and 16s rRNA sequence analysis indicates that actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907
Gu Y, Wang P, Kong CH (2009) Urease, invertase, dehydrogenase and polyphenoloxidase activities in paddy soil influenced by allelopathic rice variety. Eur J Soil Biol 45:436–441
Gülser F, Erdoğan E (2008) The effects of heavy metal pollution on enzyme activities and basal soil respiration of roadside soils. Environ Monit Assess 145:127–133
Hernandez-Allica J, Becerril JM, Zarate O, Garbisu C (2006) Assessment of the efficiency of a metal phytoextraction process with biological indicators of soil health. Plant Soil 281:147–158
Hinojosa MB, Carreira JA, García-Ruíz R, Dick RP (2005) Microbial response to heavy metal-polluted soils: community analysis from phospholipid-linked fatty acids and ester-linked fatty acids extracts. J Environ Qual 34:1789–1800
Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677
Igalavithana AD, Lee SE, Lee YH, Tsang DC, Rinklebe J, Kwon EE, Ok YS (2017) Heavy metal immobilization and microbial community abundance by vegetable waste and pine cone biochar of agricultural soils. Chemosphere 174:593–603
Ilunga EIW, Mahy G, Piqueray J, Séleck M, Shutcha MN, Meerts P, Faucon MP (2015) Plant functional traits as a promising tool for the ecological restoration of degraded tropical metal-rich habitats and revegetation of metal-rich bare soils: a case study in copper vegetation of Katanga, DRC. Ecol Eng 82:214–221
Kaplan H, Ratering S, Hanauer T, Felix-Henningsen P, Schnell S (2014) Impact of trace metal contamination and in situ remediation on microbial diversity and respiratory activity of heavily polluted Kastanozems. Biol Fertil Soils 50:735–744
Kaur ACA, Choudhary R, Kaushik R (2005) Phospholipid fatty acid as bioindicator of environment monitoring and assessment in soil ecosystem. Curr Sci 89:P1103–P1112
Kohler J, Caravaca F, Azcón R, Díaz G, Roldán A (2016) Suitability of the microbial community composition and function in a semiarid mine soil for assessing phyto-management practices based on mycorrhizal inoculation and amendment addition. J Environ Manag 169:236–246
Kramer C, Gleixner G (2006) Variable use of plant- and soil-derived carbon by microorganisms in agricultural soils. Soil Biol Biochem 38:3267–3278
Lanzén A, Epelde L, Garbisu C, Anza M, Martín-Sánchez I, Blanco F, Mijangos I (2015) The community structures of prokaryotes and fungi in mountain pasture soils are highly correlated and primarily influenced by pH. Front Microbiol 6:1321
Li R, Dörfler U, Schroll R, Munch JC (2016) Biodegradation of isoproturon in agricultural soils with contrasting pH by exogenous soil microbial communities. Soil Biol Biochem 103:149–159
Mandal A, Purakayastha TJ, Patra AK (2014) Phytoextraction of arsenic contaminated soil by Chinese brake fern (Pteris vittata): effect on soil microbiological activities. Biol Fertil Soils 50:1247–1252
Mandal A, Purakayastha TJ, Patra AK, Sarkar B (2017) Arsenic phytoextraction by Pterisvittata improves microbial properties in contaminated soil under various phosphate fertilizations. Appl Geochem. https://doi.org/10.1016/j.apgeochem.2017.04.008
Masciandaro G, Di Biase A, Macci C, Peruzzi E, Iannelli R, Doni S (2014) Phytoremediation of dredged marine sediment: monitoring of chemical and biochemical processes contributing to sediment reclamation. J Environ Manag 134:166–174
Massaccesi L, Benucci GMN, Gigliotti G, Cocco S, Corti G, Agnelli A (2015) Rhizosphere effect of three plant species of environment under periglacial conditions (majella massif, central Italy). Soil Biol Biochem 89:184–195
Moche M, Gutknecht J, Schulz E, Langer U, Rinklebe J (2015) Monthly dynamics of microbial community structure and their controlling factors in three floodplain soils. Soil Biol Biochem 90:169–178
Myers RT, Zak DR, White DC, Peacock A (2001) Landscape level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367
Nuruzzaman M, Lambers H, Bolland MDA (2006) Distribution of carboxylates ad acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 281:109–120
Olsson PA, Baath E, Jakobsen I, Soderstrom B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99:623–629
Overmann J, van Gemerden H (2000) Microbial interactions involving Sulfur bacteria: Implications for the ecology and evolution of bacterial communities. FEMS Microbiol Rev 24:591–599
Renella G, Landi L, Valori F, Nannipieri P (2007) Microbial and hydrolase activity after release of low molecular weight organic compounds by a model root surface in a clayey and a sandy soil. Appl Soil Ecol 36:124–129
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME J 4:1340–1351
Sinha S, Masto RE, Ram LC, Selvi VA, Srivastava NK, Tripathi RC, George J (2009) Rhizosphere soil microbial index of tree species in a coal mining ecosystem. Soil Biol Biochem 4:1824–1832
Song D, Xi X, Huang S, Liang G, Sun J, Zhou W, Wang X (2016) Short-term responses of soil respiration and c-cycle enzyme activities to additions of biochar and urea in a calcareous soil. PLoS One 11:e 0161694
Steinauer K, Tilman D, Wragg PD, Cesarz S, Cowles JM, Pritsch K, Reich PB, Weisser WW, Eisenhauer N (2015) Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecology 96:99–112
Stepniewska Z, Wolinska A, Ziomek J (2009) Response of soil catalase activity tochromium contamination. J Environ Sci 21:1142–1147
Stewart CE, Roosendaal D, Denef K, Pruessner E, Comas LH, Sarath G, Jin VL, Schmer MR, Soundararajan M (2017) Seasonal switchgrass ecotype contributions to soil organic carbon, deep soil microbial community composition and rhizodeposit uptake during an extreme drought. Soil Biol Biochem 112:191–203
Straathof AL, Chincarini R, Comans RN, Hoffland E (2014) Dynamics of soil dissolved organic carbon pools reveal both hydrophobic and hydrophilic compounds sustain microbial respiration. Soil Biol Biochem 79:109–116
Subrahmanyam G, Shen JP, Liu YR, Archana G, Zhang LM (2016) Effect of long-term industrial waste effluent pollution on soil enzyme activities and bacterial community composition. Environ Monit Assess 188:1–13
Turpeinen R, Kairesalo T, Häggblom MM (2004) Microbial community structure and activity in arsenic-, chromium- and copper- contaminated soils. FEMS Microbiol Ecol 47:39–50
Van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707
Vogeler I, Vachey A, Deurer M, Bolan N (2008) Impact of plants on the microbial activity in soils with high and low levels of copper. Eur J Soil Biol 44:92–100
Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284
Wang SL, Liao WB, Yu FQ, Liao B, Shu WS (2009) Hyperaccumulation of lead, zinc, and cadmium in plants growing on a lead/zinc outcrop in Yunnan Province, China. Environ Geol 58:471–476
Wang Q, He T, Wang S, Li L (2013) Carbon input manipulation affects soil respiration and microbial community composition in a subtropical coniferous forest. Agric For Meteorol 178-179:152–160
Wójcik M, Gonnelli C, Selvi F, Dresler S, Rostański A, Vangronsveld J (2017) Metallophytes of serpentine and calamine soils-Their unique ecophysiology and potential for phytoremediation. Adv Bot Res 83:1–42
Wong MH (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50:775–780
Wu Y, Ding N, Wang G, Xu J, Wu J, Brookes PC (2009) Effects of different soil weights, storage times and extraction methods on soil phospholipid fatty acid analyses. Geoderma 150:171–178
Xian Y, Wang M, Chen W (2015) Quantitative assessment on soil enzyme activities of heavy metal contaminated soils with various soil properties. Chemosphere 139:604–608
Xiao Y, Huang Z, Lu X (2015) Changes of soil labile organic carbon fractions and their relation to soil microbial characteristics in four typical wetlands of Sanjiang Plain, Northeast China. Ecol Eng 82:381–389
Xu X, Zhang Z, Hu S, Ruan Z, Jiang J, Chen C, Shen Z (2017) Response of soil bacterial communities to lead and zinc pollution revealed by Illumina MiSeq sequencing investigation. Environ Sci Pollut R 24:666–675
Yang W, Hu H, Ru M, Ni W (2013) Changes of microbial properties in (near-) rhizosphere soils after phytoextraction by Sedum alfredii H: A rhizobox approach with an artificial Cd-contaminated soil. Appl Soil Ecol 72:14–21
Yang W, Li H, Zhang T, Lin S, Ni W (2014) Classification and identification of metal-accumulating plant species by cluster analysis. Environ Sci Pollut R 21:10626–10637
Yao HY, Huang CY (2006) Soil microbial ecology and experimental techniques. Science Press, Beijing, p 201 (in Chinese)
Yuan KN (1963) Studies on the organic-mineral complex in soil: the oxidation stability of humus from different organo-mineral complexes in soil. Acta Pedol Sin 11:286–293 (in Chinese)
Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129
Zhang C, Liu G, Xue S, Song Z (2011) Rhizosphere soil microbial activity under different vegetation types on the Loess Plateau, China. Geoderma 161:115–125
Zhang B, He H, Ding X, Zhang X, Zhang X, Yang X, Filley TR (2012) Soil microbial community dynamics over a maize (Zea mays L.) growing season under conventional- and no-tillage practices in a rainfed agroecosystem. Soil Tillage Res 124:153–160
Zhao Q, Zhou L, Zheng X, Wang Y, Lu J (2015) Study on enzymatic activities and behaviors of heavy metal in sediment–plant at muddy tidal flat in yangtze estuary. Environ Earth Sci 73:3207–3216
Zogg GP, Zak DR, Ringelberg DB, MacDonald NW, Pregitzer KS, White DC (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61:475–481
Zou TJ, Li TX, Zhang XZ, Yu HY, Huang HG (2012) Lead accumulation and phytostabilization potential of dominant plant species growing in a lead–zinc mine tailing. Environ Earth Sci 65:621–630
Acknowledgments
We are grateful for the financial support from the National Natural Science Foundation of China (Nos. 41501345), the Natural Science Foundation of Fujian Province (Nos. 2015 J01155) and the Foundation for Distinguished Young Scholars of Fujian Agriculture and Forestry University (Nos. XJQ201628).
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Yang, W., Li, P., Rensing, C. et al. Biomass, activity and structure of rhizosphere soil microbial community under different metallophytes in a mining site. Plant Soil 434, 245–262 (2019). https://doi.org/10.1007/s11104-017-3546-9
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DOI: https://doi.org/10.1007/s11104-017-3546-9