Abstract
The recovery of microbial community and activities is crucial to the remediation of contaminated soils. Distance-dependent variations of microbial community composition and metabolic characteristics in the rhizospheric soil of hyperaccumulator during phytoextraction are poorly understood. A 12-month phytoextraction experiment with Sedum alfredii in a Cd-contaminated soil was conducted. A pre-stratified rhizobox was used for separating sub-layer rhizospheric (0–2, 2–4, 4–6, 6–8, 8–10 mm from the root mat)/bulk soils. Soil microbial structure and function were analyzed by phospholipid fatty acid (PLFA) and MicroResp™ methods. The concentrations of total and specified PLFA biomarkers and the utilization rates for the 14 substrates (organic carbon) in the 0–2-mm sub-layer rhizospheric soil were significantly increased, as well as decreased with the increase in the distance from the root mat. Microbial structure measured by the ratios of different groups of PLFAs such as fungal/bacterial, monounsaturated/saturated, ratios of Gram-positive to Gram-negative (GP/GN) bacterial, and cyclopropyl/monoenoic precursors and 19:0 cyclo/18:1ω7c were significantly changed in the 0–2-mm soil. The PLFA contents and substrate utilization rates were negatively correlated with pH and total, acid-soluble, and reducible fractions of Cd, while positively correlated with labile carbon. The dynamics of microbial community were likely due to root exudates and Cd uptake by S. alfredii. This study revealed the stimulations and gradient changes of rhizosphere microbial community through phytoextraction, as reduced Cd concentration, pH, and increased labile carbons are due to the microbial community responses.
Similar content being viewed by others
References
Aghababaei F, Raiesi F, Hosseinpur A (2014) The influence of earthworm and mycorrhizal co-inoculation on Cd speciation in a contaminated soil. Soil Biol Biochem 78:21–295
Alford ÉR, Pilon-Smits EA, Paschke MW (2010) Metallophytes—a view from the rhizosphere. Plant Soil 337:33–50
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881
André A, Antunes SC, Gonçalves F, Pereira R (2009) Bait-lamina assay as a tool to assess the effects of metal contamination in the feeding activity of soil invertebrates within a uranium mine area. Environ Pollut 157:2368–2377
Anju M, Banerjee DK (2010) Comparison of two sequential extraction procedures for heavy metal partitioning in mine tailings. Chemosphere 78:1393–1402
Aviani I, Laor Y, Raviv M (2006) Limitations and potential of in situ rhizobox sampling for assessing microbial activity in fruit tree rhizosphere. Plant Soil 279:327–332
Azarbad H, van Straalen NM, Laskowski R, Nikiel K, Röling WF, Niklińska M (2016) Susceptibility to additional stressors in metal-tolerant soil microbial communities from two pollution gradients. Appl Soil Ecol 98:233–242
Bérard A, Mazzia C, Sappin-Didier V, Capowiez L, Capowiez Y (2014) Use of the MicroResp™ method to assess pollution-induced community tolerance in the context of metal soil contamination. Ecol Indic 40:27–33
Boshoff M, De Jonge M, Dardenne F, Blust R, Bervoets L (2014) The impact of metal pollution on soil faunal and microbial activity in two grassland ecosystems. Environ Res 134:169–180
Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278
Breulmann M, Schulz E, Weibhuhn 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
Burges A, Epelde L, Garbisu C (2015) Impact of repeated single-metal and multi-metal pollution events on soil quality. Chemosphere 120:8–15
Burton J, Chen C, Xu Z, Ghadir H (2010) Soil microbial biomass, activity and community composition in adjacent native and plantation forests of subtropical Australia. J Soil Sediments 10:1267–1277
Campbell CD, Grayston SJ, Hirst DJ (1997) Use of rhizosphere carbon sources in sole carbon source tests to discriminate soil microbial communities. J Microbiol Meth 30:33–41
Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JMA (2003) Rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microb 69:3593–3599
Campbell CD, Cameron CM, Bastias BA, Chen CR, Cairney JWG (2008) Long term repeated burning in a wet scleophyll forest reduces fungal and bacterial biomass and responses to carbon substrates. Soil Biol Biochem 40:2246–2252
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 and growing in semiarid mine tailings. Microb Ecol 2:265–271
Chang EH, Chen TH, Tian G, Chiu CY (2016) The effect of altitudinal gradient on soil microbial community activity and structure in moso bamboo plantations. Appl Soil Ecol 98:213–220
Chapman SJ, Campbell CD, Artz RRE (2007) Assessing CLPPs using MicroResp: a comparison with Biolog and multi-SIR. J Soil Sediments 7:406–410
Chen Z, Ai Y, Fang C, Wang K, Li W, Liu S, Li C, Xiao J, Huang Z (2014) Distribution and phytoavailability of heavy metal chemical fractions in artificial soil on rock cut slopes alongside railways. J Hazard Mater 273:165–173
Chlopecka A (1996) Assessment of form of Cd, Zn and Pb in contaminated calcareous and gleyed soils in southwest Poland. Sci Total Environ 188:253–262
Chodak M, Gołębiewski M, Morawska-Płoskonka J, Kuduk K, Niklińska M (2013) Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl Soil Ecol 64:7–14
Columbus MP, Macfie SM (2015) It takes an individual plant to raise a community: TRFLP analysis of the rhizosphere microbial community of two pairs of high- and low-metal-accumulating plants. Soil Biol Biochem 81:77–80
Creamer RE, Stone D, Berry P, Kuiper I (2016) Measuring respiration profiles of soil microbial communities across Europe using MicroResp™ method. Appl Soil Ecol 97:36–43
Cui H, Fan Y, Yang J, Xu L, Zhou J, Zhu Z (2016) In situ phytoextraction of copper and cadmium and its biological impacts in acidic soil. Chemosphere 161:233–241
Davari M, Homaee M, Rahnemaie R (2015) An analytical deterministic model for simultaneous phytoremediation of Ni and Cd from contaminated soils. Environ Sci Pollu Res 22:4609–4620
Dessureault-Rompre J, Luster J, Schulin R, Tercier-Waeber ML, Nowack B (2010) Decrease of labile Zn and Cd in the rhizosphere of hyperaccumulating Thlaspi caerulescens with time. Environ Pollut 158:1955–1962
Epelde L, Becerril JM, Kowalchuk GA, Deng Y, Zhou J, Garbisu C (2010) Impact of metal pollution and Thlaspi caerulescens growth on soil microbial communities. Appl Environ Microb 76:7843–7853
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
Fitz WJ, Wenzel WW (2002) Arsenic transformation in the soil–rhizosphere–plant system, fundamentals and potential application of phytoremediation. J Biotechnol 99:259–278
Ferris H, Tuomisto H (2015) Unearthing the role of biological diversity in soil health. Soil Biol Biochem 85:101–109
Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fert Soils 22:59–65
Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass and activity of microbial communities from two soil types experimentally exposed to different heavy metal. Appl Environ Microbiol 59:3605–3617
Garcia-Sánchez M, Garcia-Romera I, Cajthaml T, Tlustoš P, Száková J (2015) Changes in soil microbial community functionality and structure in a metal-polluted site: the effect of digestate and fly ash applications. J Environ Manag 162:63–73
Gartzia-Bengoetxea N, Kandeler E, de Arano IM, Arias-González A (2016) Soil microbial functional activity is governed by a combination of tree species composition and soil properties in temperate forests. Appl Soil Ecol 100:57–64
Ge T, Chen X, Yuan H, Li B, Zhu H, Peng P, Li K, Jones DL, Wu J (2013) Microbial biomass, activity, and community structure in horticultural soils under conventional and organic management strategies. Eur J Soil Biol 58:122–128
Ghnaya T, Mnassri M, Ghabriche R, Wali M, Poschenrieder C, Lutts S, Abdelly C (2015) Nodulation by Sinorhizobium meliloti originated from a mining soil alleviates Cd toxicity and increases Cd-phytoextraction in Medicago sativa L. Front Plant Sci 6:863
Gómez-Sagasti MT, Alkorta I, Becerril JM, Epelde L, Anza M, Garbisu C (2012) Microbial monitoring of the recovery of soil quality during heavy metal phytoremediation. Water Air Soil Poll 223:3249–3262
He S, He Z, Yang X, Stoffella PJ, Baligar VC (2015) Soil biogeochemistry, plant physiology, and phytoremediation of cadmium-contaminated soils. Adv Agron 134:135–225
He Y, Xu J, Tang C, Wu Y (2005) Facilitation of pentachlorophenol degradation in the rhizosphere of ryegrass (Loliumperenne L.) Soil Biol Biochem 37:2017–2024
He Y, Xu J, Lv X, Ma Z, Wu J, Shi J (2009) Does the depletion of pentachlorophenol in root-soil interface follow a simple linear dependence on the distance to root surfaces. Soil Biol Biochem 41:1807–1813
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, Garcıa-Ruız 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
Hortal S, Bastida F, Armas C, Lozano YM, Moreno JL, García C, Pugnaire FI (2013) Soil microbial community under a nurse-plant species changes in composition, biomass and activity as the nurse grows. Soil Biol Biochem 64:139–146
Huang G, Cao YF, Wang B, Li Y (2015) Effects of nitrogen addition on soil microbes and their implications for soil Cemission in the Gurbantunggut Desert, center of the Eurasian continent. Sci Total Environ 515–516:215–224
Kenarova A, Boteva S (2015) Functional diversity of microorganisms in heavy metal-polluted soils. In: Heavy metal contamination of soils. Springer International Publishing, pp 245–257
Kenarova A, Radeva G, Traykov I, Boteva S (2014) Community level physiological profiles of bacterial communities inhabiting uranium mining impacted sites. Ecotox Environ Safe 100:226–232
Kim KR, Owens G, Kwon SL (2010) Influence of Indian mustard (Brassica juncea) on rhizosphere soil solution chemistry in long-term contaminated soils: a rhizobox study. J Environ Sci 22:98–105
Klimek B, Sitarz A, Choczyński M, Niklińska M (2016) The effects of heavy metals and total petroleum hydrocarbons on soil bacterial activity and functional diversity in the Upper Silesia Industrial Region (Poland). Water Air Soil Poll 227:1–9
Kohler J, Caravaca F, Azcon R, Díaz G, Roldan A (2016) Suitability of the microbial community composition and function in a semiarid mine soil for assessing phytomanagement practices based on mycorrhizal inoculation and amendment addition. J Environ Manag 169:236–246
Kwonrae K, Owens G, Naidu R, Soonlk K (2010) Influence of plant roots on rhizosphere soil solution composition of long-term contaminated soils. Geoderma 155:86–92
Leita L, De Nobili M, Muhlbachova G, Mondini C, Marchiol L, Zerbi G (1995) Bioavailability and effects of heavy metals on soil microbial biomass survival during laboratory incubation. Biol Fertil Soils 19:103–108
Li Z, Wu LH, Luo YM, Christie P (2014) Dynamics of plant metal uptake and metal changes in whole soil and soil particle fractions during repeated phytoextraction. Plant Soil 374:857–869
Liao QL, Liu C, Wu HY, Jin Y, Hua M, Zhu BW, Chen K, Huang L (2015) Association of soil cadmium contamination with ceramic industry: a case study in a Chinese town. Sci Total Environ 514:26–32
Liu D, Fang S, Tian Y, Dun X (2012) Variation in rhizosphere soil microbial index of tree species on seasonal flooding land: an in situ rhizobox approach. Appl Soil Eco 59:1–11
Liu L, Wu LH, Li N, Luo YM, Li SL, Li Z, Han CL, Jiang YG, Christie P (2011) Rhizosphere concentrations of zinc and cadmium in a metal contaminated soil after repeated phytoextraction by Sedum plumbizincicola. Int J Phytoremediat 13:750–764
Lu H, Li Z, Fu S, Méndez A, Gascó G, Paz-Ferreiro J (2015) Combining phytoextraction and biochar addition improves soil biochemical properties in a soil contaminated with Cd. Chemosphere 119:209–216
Mackie KA, Marhan S, Ditterich F, Schmidt HP, Kandeler E (2015) The effects of biochar and compost amendments on copper immobilization and soil microorganisms in a temperate vineyard. Agric Ecosyst Environ 201:58–69
Mandal A, Purakayastha TJ, Patra AK (2014) Phytoextraction of arsenic contaminated soil by Chinese brake fern (Pteris vittata): effect on soil microbiological activities. Biol Fert Soils 50:1247–1252
McGrath SP, Shen ZG, Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188:153–159
Mitchell PJ, Simpson AJ, Soong R, Simpson MJ (2015) Shifts in microbial community and water-extractable organic matter composition with biochar amendment in a temperate forest soil. Soil Biol Biochem 81:244–254
Muehe EM, Weigold P, Adaktylou IJ, Planer-Friedrich B, Kraemer U, Kappler A, Behrens S (2015) Rhizosphere microbial community composition affects cadmium and zinc uptake by the metal-hyperaccumulating plant Arabidopsis halleri. Appl Environ Microb 81:2173–2181
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
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
Otero XL, Álvarez E, Fernández-Sanjurjo MJ, Macías F (2012) Micronutrients and toxic trace metals in the bulk and rhizospheric soil of the spontaneous vegetation at an abandoned copper mine in Galicia (NW Spain). J Geochem Explor 112:84–92
Pennanen T, Frostegård Å, Fritze H, Bååth E (1996) Phospholipid fatty acids and heavy metal tolerance of soil microbial communities along two heavy metal-polluted gradients in coniferous forests. Appl Environ Microb 62:420–428
Perez-de-Mora A, Burgos P, Madejon E, Cabrera F, Jaeckel P, Schloter M (2006) Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biol Biochem 38:327–341
Pueyo M, Mateu J, Rigol A, Vidal M, Lopez-Sanchez JF, Rauret G (2008) Use of the modified BCR three-step sequential extraction procedure for the study of trace element dynamics in contaminated soils. Environ Pollut 152:330–341
Puschenreiter M, Wieczorek S, Horak O, Wenzel WW (2003) Chemical changes in the rhizosphere of metal hyperaccumulator and excluder Thlaspi species. J Plant Nutr Soil Sci 166:579–584
Qin H, Brookes PC, Xu J (2014) Cucurbita spp. and Cucumis sativus enhance the dissipation of polychlorinated biphenyl congeners by stimulating soil microbial community development. Environ Pollut 184:306–312
Ridl J, Kolar M, Strejcek M, Strnad H, Stursa P, Paces J, Macek T, Uhlik O (2016) Plants rather than mineral fertilization shape microbial community structure and functional potential in legacy contaminated soil. Front Microbiol 7
Robson TC, Braungardt CB, Rieuwerts J, Worsfold P (2014) Cadmium contamination of agricultural soils and crops resulting from sphalerite weathering. Environ Pollut 184:283–289
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
Setälä H, Berg MP, Jones TH (2005) Trophic structure and functional redundancy in soil communities. In: Bardgett RD, Usher MB, Hopkins DW (eds) Biological diversity and function in soils. Cambridge University Press, Cambridge, pp 236–249
Singh BK, Quince C, Macdonald CA, Khachane A, Thomas N, Al-Soud WA, Sørensen SJ, He Z, White D, Sinclair A, Crooks B, Zhou J, Campbell CD (2014) Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environ Microbiol 16:2408–2420
Sousa NR, Ramos MA, Marques APGC, Castro PML (2014) A genotype dependent-response to cadmium contamination in soil is displayed by Pinuspinaster in symbiosis with different mycorrhizal fungi. Appl Soil Eco l76:7–13
Stefanowicz AM, Niklinska M, Kapusta P, Szarek-Łukaszewska G (2010) Pine forest and grassland differently influence the response of soil microbial communities to metal contamination. Sci Total Environ 408:6134–6141
Stefanowicz AM, Kapusta P, Szarek-Łukaszewska G, Grodzińska K, Niklińska M, Vogt RD (2012) Soil fertility and plant diversity enhance microbial performance in metal-polluted soils. Sci Total Environ 439:211–219
Strickland MS, Rousk J (2010) Considering fungal: bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395
Sun Y, Xu Y, Xu Y, Wang L, Liang X, Li Y (2016) Reliability and stability of immobilization remediation of Cd polluted soils using sepiolite under pot and field trials. Environ Pollut 208:739–746
Sungur A, Soylak M, Yilmaz S, Özcan H (2014) Determination of heavy metals in sediments of the Ergene River by BCR sequential extraction method. Environ Earth Sci 72:3293–3305
Tian J, McCormack L, Wang J, Guo D, Wang Q, Zhang X, Yu G, Blagodatskaya E, Kuzyakov Y (2015) Linkages between the soil organic matter fractions and the microbial metabolic functional diversity within a broad-leaved Korean pine forest. Eur J Soil Biol 66:57–64
Tscherko D, Ute H, Marie-Claude M, Ellen K (2004) Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biol Biochem 36:1685–1698
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
Wang J, Zhang CB, Jin ZX (2009) The distribution and phytoavailability of heavy metal fractions in rhizosphere soils of Paulowniufortunei (seem) Hems near a Pb/Zn smelter in Guangdong, PR China. Geoderma 148:299–306
Wei J, Liu X, Zhang X, Chen X, Liu S, Chen L (2014) Rhizosphere effect of Scirpus triqueter on soil microbial structure during phytoremediation of diesel-contaminated wetland. Environ Technol 35:514–520
Wei S, Twardowska I (2013) Main rhizosphere characteristics of the Cd hyperaccumulator Rorippa globosa (Turcz.) Thell. Plant Soil 372(1–2):669–681
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
Yang WH, Hu H, Ru M, Ni WZ (2013a) 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 L, Wang GP, Cheng Z, Liu Y, Shen ZG, Luo CL (2013b) Influence of the application of chelant EDDS on soil enzymatic activity and microbial community structure. J Hazard Mater 262:561–570
Yang WH, Li H, Zhang TX, Lin S, Ni WZ (2014) Classification and identification of metal-accumulating plant species by cluster analysis. Environ Sci Pollut Res 21:10626–10637
Yang Y, Campbell CD, Clark L, Cameron CM, Paterson E (2006) Microbial indicators of heavy metal contamination in urban and rural soils. Chemosphere 63:1942–1952
Yao HY, Campbell CD, Qiao XR (2011) Soil pH controls nitrification and carbon substrate utilization more than urea or charcoal in some highly acidic soils. Biol Fert Soils 47:515–522
Yergeau E, Sanschagrin S, Maynard C, St-Arnaud M, Greer CW (2014) Microbial expression profiles in the rhizosphere of willows depend on soil contamination. The ISME J 8:344–358
Ying JY, Zhang LM, Wei WX, He JZ (2013) Effects of land utilization patterns on soil microbial communities in an acid red soil based on DNA and PLFA analyses. J Soils Sediments 13:1223–1231
Yoshitake S, Fujiyoshi M, Watanabe K, Masuzawa T, Nakatsubo T, Koizumi H (2013) Successional changes in the soil microbial community along a vegetation development sequence in a subalpine volcanic desert on Mount Fuji, Japan. Plant Soil 364:261–272
Yu J, Unc A, Zhang X, Steinberger Y (2016) Responses of the soil microbial catabolic profile and diversity to vegetation rehabilitation in degraded semiarid grassland. Appl Soil Ecol 101:124–131
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)
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fert Soils 29:111–129
Zhou X, Wu H, Koetz E, Xu Z, Chen C (2012) Soil labile carbon and nitrogen pools and microbial metabolic diversity under winter crops in an arid environment. Appl Soil Ecol 53:49–55
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
Zornoza R, Acosta JA, Faz A, Bååth E (2016) Microbial growth and community structure in acid mine soils after addition of different amendments for soil reclamation. Geoderma 272:64–72
Zornoza R, Acosta JA, Martínez-Martínez S, Faz A, Bååth E (2015) Main factors controlling microbial community structure and function after reclamation of a tailing pond with aided phytostabilization. Geoderma 245:1–10
Acknowledgements
We sincerely acknowledge the supports from the National Natural Science Foundation of China (No. 41501345), the Natural Science Foundation of Fujian Province (No. 2015J01155), and the Foundation for Distinguished Young Scholars of Fujian Agriculture and Forestry University (No. XJQ201628).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Robert Duran
Electronic supplementary material
ESM 1
(DOC 185 kb)
Rights and permissions
About this article
Cite this article
Yang, W., Zhang, T., Lin, S. et al. Distance-dependent varieties of microbial community structure and metabolic functions in the rhizosphere of Sedum alfredii Hance during phytoextraction of a cadmium-contaminated soil. Environ Sci Pollut Res 24, 14234–14248 (2017). https://doi.org/10.1007/s11356-017-9007-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-9007-4