Abstract
Purpose
Iron plaque (IP) formation via radial oxygen loss (ROL) of wetland plant has been predominantly recognized as the reason for heavy metal sequestration in the rhizosphere. However, the same contribution of the microbes living in a potential rhizoplane biofilm matrix has not been comprehensively elucidated. In this review, we proposed a conceptional model of the wetland plant rhizoplane biofilm and summarized the possible pathways therein for heavy metal precipitation and iron-sulfur cycle termination.
Materials and methods
After an introduction of the effects of IP and microbes on the phytoremediation of heavy metal-contaminated wetland, the distribution of rhizospheric bacteria and different metal speciations resulted from wetland plant ROL were demonstrated. Based on the studies of microflora in the rhizosphere and IP, coupled with the ROL nature, we proposed an existence of rhizoplane biofilm with a special structure that could contribute to the rhizospheric iron-sulfur cycle termination by the production of heavy metal precipitates (metal sulfides).
Results and discussion
The ROL leads to the diffusion of oxygen with a decreasing gradient from the root surface (rhizoplane) to the bulk soil, allowing the formation of an unconventional rhizoplane biofilm comprising an aerobic inner layer and an anaerobic outer layer. Thus, aerobic bacteria, e.g., iron-oxidizing bacteria (IOB) and sulfur-oxidizing bacteria (SOB), as well as anaerobic bacteria, e.g., iron-reducing bacteria (IRB) and sulfate-reducing bacteria (SRB), are favored in the inner layer and outer layer of the rhizoplane biofilm, respectively. In the inner layer, ferrous sulfide is oxidized by IOB and SOB to Fe3+ and SO42−. Fe3+ is thereafter bound with oxygen into iron (hydro)oxides, aggregating into a barrier of iron plaque for heavy metal sequestration and O2 diffusion. Excessive SO42− diffused to the outer layer is reduced to S2− by SRB, forming sufficient metal sulfide precipitates that on one hand immobilize those heavy metal ions released by H+, and on the other hand serve as a barrier for preventing the contact of ferrous sulfide from O2. Hence, further oxidization of ferrous sulfide is terminated.
Conclusions
This rhizoplane biofilm co-existing with IP contributes to the rhizosphere element circulation. Further investigation and demonstration of its composition, structure, and function will help us better interpret the survival strategy and bioremediation potential of wetland plants in flooded mining areas, such as mine tailing ponds in tropical and sub-tropical regions with abundant rainfall.
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References
Alloway BJ (1995) Soil processes and the behaviour of metals. Heavy metals in soils. John Wiley & Sons, New York
Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–332
Armstrong (2010) Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiol Plant 25:192–197
Aucour AM, Bedell JP, Queyron M, Thole R, Lamboux A, Sarret G (2017) Zn speciation and stable isotope fractionation in a contaminated urban wetland soil-Typha latifolia system. Environ Sci Technol 51:8350–8358
Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152
Banik A, Pandya P, Patel B, Rathod C, Dangar M (2018) Characterization of halotolerant, pigmented, plant growth promoting bacteria of groundnut rhizosphere and its in-vitro evaluation of plant-microbe protocooperation to withstand salinity and metal stress. Sci Total Environ 630:231–242
Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A 110:1621–1630
Blute NK, Brabander DJ, Hemond HF, Sutton SR, Newville MG, Rivers ML (2004) Arsenic sequestration by ferric iron plaque on cattail roots. Environ Sci Technol 38:6074–6077
Bonnefoy V, Holmes DS (2012) Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ Microbiol 14:1597–1611
Briones AM, Okabe S, Umemiya Y, Ramsing NB, Reichardt W, Okuyama H (2002) Influence of different cultivars on populations of ammonia-oxidizing bacteria in the root environment of rice. Appl Environ Microbiol 68:3067–3075
Brix H, Dyhrjensen K, Lorenzen B (2002) Root-zone acidity and nitrogen source affects Typha latifolia L. growth and uptake kinetics of ammonium and nitrate. J Exp Bot 53:2441–2450
Chen LX, Li JT, Chen YT, Huang LN, Hua ZS, Hu M, Shu WS (2013) Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 15:2431–2444
Cheng H, Wang M, Wong MH, Ye Z (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375:137–148
Chi H, Yang L, Yang W, Li Y, Chen Z, Huang L, Chao Y, Qiu R, Wang S (2018) Variation of the bacterial community in the rhizoplane iron plaque of the wetland plant Typha latifolia. Int J Environ Res Public Health 15:2610–2626
Dold B (2014) Evolution of acid mine drainage formation in sulphidic mine tailings. Minerals 4:621–641
Dong MF, Feng RW, Wang RG, Sun Y, Ding YZ, Xu YM, Fan ZL, Guo JK (2016) Inoculation of Fe/Mn-oxidizing bacteria enhances Fe/Mn plaque formation and reduces Cd and As accumulation in Rice Plant tissues. Plant Soil 404:75–83
Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 112:E911–E920
Emerson D, Weiss JV, Megonigal JP (1999) Iron-oxidizing bacteria are associated with ferric hydroxide precipitates (Fe-plaque) on the roots of wetland plants. Appl Environ Microbiol 65:2758–2761
Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583
Escalante G, Campos VL, Valenzuela C, Yañez J, Zaror C, Mondaca MA (2009) Arsenic resistant bacteria isolated from arsenic contaminated river in the Atacama Desert (Chile). Bull Environ Contam Toxicol 83:657–661
Fellet G, Marchiol L, Vedove GD, Peressotti A (2011) Application of biochar on mine tailings: effects and perspectives for land reclamation. Chemosphere 83:1262–1267
Flemming HC (2002) Biofouling in water systems – cases, causes and countermeasures. Appl Microbiol Biotechnol 59:629–640
Fortin D, Praharaj T (2005) Role of microbial activity in Fe and S cycling in sub-oxic to anoxic sulfide-rich mine tailings : A mini-review. J Nucl Radiochem Sci 6:39–42
Fortin D, Davis B, Beveridge TJ (2010) Role of Thiobacillus and sulfate-reducing bacteria in iron biocycling in oxic and acidic mine tailings. FEMS Microbiol Ecol 21:11–24
Fu YQ, Yang XJ, Ye ZH, Shen H (2016) Identification, separation and component analysis of reddish brown and non-reddish brown iron plaque on rice (Oryza sativa) root surface. Plant Soil 402:277–290
Guo J, Chi J (2014) Effect of Cd-tolerant plant growth-promoting rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr. in Cd-contaminated soil. Plant Soil 375:205–214
Guo L, Cutright TJ (2014) Effect of citric acid and rhizosphere bacteria on metal plaque formation and metal accumulation in reeds in synthetic acid mine drainage solution. Ecotoxicol Environ Saf 104:72–78
Guo L, Cutright TJ (2015) Metal plaque on reeds from an acid mine drainage site. J Environ Qual 44:859–867
Guo L, Cutright TJ, Duirk S (2015) Effect of citric acid, rhizosphere bacteria, and plant age on metal uptake in reeds cultured in acid mine drainage. Water Air Soil Pollut 226
Haaijer SCM, Crienen G, Jetten MSM, den Camp HJMO (2012) Anoxic iron cycling bacteria from an iron sulfide- and nitrate-rich freshwater environment. Front Microbiol 3:26
Hammond CM, Root RA, Maier RM, Chorover J (2018) Mechanisms of arsenic sequestration by Prosopis juliflora during the phytostabilization of metalliferous mine tailings. Environ Sci Technol 52:1156–1164
Hansel CM, Fendorf S, Sutton S, Newville M (2001) Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environ Sci Technol 35:3863–3868
Hansel CM, La Force MJ, Fendorf S, Sutton S (2002) Spatial and temporal association of As and Fe species on aquatic plant roots. Environ Sci Technol 36:1988–1994
Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551–1564
Honeker LK, Root RA, Chorover J, Maier RM (2016) Resolving colocalization of bacteria and metal(loid)s on plant root surfaces by combining fluorescence in situ hybridization (FISH) with multiple-energy micro-focused X-ray fluorescence (ME μXRF). J Microbiol Methods 131:23–33
Huang LN, Zhou WH, Hallberg KB, Wan CY, Li J, Shu WS (2011) Spatial and temporal analysis of the microbial community in the tailings of a Pb-Zn mine generating acidic drainage. Appl Environ Microbiol 77:5540–5544
Huang H, Zhu Y, Chen Z, Yin X, Sun G (2012) Arsenic mobilization and speciation during iron plaque decomposition in a paddy soil. J Soils Sediments 12:402–410
Huang X, Tang K, Xu X, Cai C (2017) Interaction of Fe-Mn plaque and Arthrobacter echigonensis MN1405 and uptake and translocation of Cd by Phytolacca acinosa Roxb. Chemosphere 174:585–592
Huang L, Li Y, Zhao M, Chao Y, Qiu R, Yang Y, Wang S (2018) Potential of Cassia alata L. coupled with biochar for heavy metal stabilization in multi-metal mine tailings. Int J Environ Res Public Health 15:494–508
Ilbert M, Bonnefoy V (2012) Insight into the evolution of the iron oxidation pathways. University of California Press, USA
Jacob DL, Otte ML (2003) Conflicting processes in the wetland plant rhizosphere: metal retention or mobilization? Water Air Soil Pollut 3:91–104
Jacob DL, Otte ML (2004) Long-term effects of submergence and wetland vegetation on metals in a 90-year old abandoned Pb–Zn mine tailings pond. Environ Pollut 130:337–345
Jia Y, Huang H, Chen Z, Zhu YG (2014) Arsenic uptake by rice is influenced by microbe-mediated arsenic redox changes in the rhizosphere. Environ Sci Technol 48:1001–1007
Jia Y, Bao P, Zhu YG (2015) Arsenic bioavailability to rice plant in paddy soil: influence of microbial sulfate reduction. J Soils Sediments 15:1960–1967
Kaplan DI, Kukkadapu R, Seaman JC, Arey BW, Dohnalkova AC, Buettner S, Li D, Varga T, Scheckel KG, Jaffé PR (2016) Iron mineralogy and uranium-binding environment in the rhizosphere of a wetland soil. Sci Total Environ 569–570:53–64
Kelly CN, Peltz CD, Stanton M, Rutherford DW, Rostad CE (2014) Biochar application to hardrock mine tailings: soil quality, microbial activity, and toxic element sorption. Appl Geochem 43:35–48
Korehi H, Blöthe M, Schippers A (2014) Microbial diversity at the moderate acidic stage in three different sulfidic mine tailings dumps generating acid mine drainage. Res Microbiol 165:713–718
Kusel K, Chabbi A, Trinkwalter T (2003) Microbial processes associated with roots of bulbous rush coated with iron plaques. Microb Ecol 46:302–311
Lakshmanan V, Shantharaj D, Li G, Seyfferth AL, Sherrier DJ, Bais HP (2015) A natural rice rhizospheric bacterium abates arsenic accumulation in rice (Oryza sativa L.). Planta 242:1037–1050
Lan CY, Shu WS, Wong MH (1998) Reclamation of Pb/Zn mine tailings at Shaoguan, Guangdong Province, People's Republic of China: the role of river sediment and domestic refuse. Bioresour Technol 65:117–124
Lei M, Tie B, Williams PN, Zheng Y, Huang Y (2011) Arsenic, cadmium, and lead pollution and uptake by rice (Oryza sativa L.) grown in greenhouse. J Soils Sediments 11:115–123
Li X, Huang L, Bond PL, Lu Y, Vink S (2014) Bacterial diversity in response to direct revegetation in the Pb–Zn–Cu tailings under subtropical and semi-arid conditions. Ecol Eng 68:233–240
Li F-L, Yang CM, Syu CH, Lee DY, Tsuang BJ, Juang KW (2016) Combined effect of rice genotypes and soil characteristics on iron plaque formation related to Pb uptake by rice in paddy soils. J Soils Sediments 16:150–158
Liang X, Qin X, Huang Q, Huang R, Yin X, Cai Y, Wang L, Sun Y, Xu Y (2017) Remediation mechanisms of mercapto-grafted palygorskite for cadmium pollutant in paddy soil. Environ Sci Pollut Res 24:23783–23793
Ligi T, Oopkaup K, Truu M, Preem J-K, Nõlvak H, Mitsch WJ, Mander Ü, Truu J (2014) Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing. Ecol Eng 72:56–66
Liu WJ, Zhu YG, Hu Y, Williams PN, Gault AG, Meharg AA, Charnock JM, Smith FA (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza Sativa L.). Environ Sci Technol 40:5730–5736
Liu HJ, Zhang JL, Zhang FS (2007) Role of iron plaque in Cd uptake by and translocation within rice (Oryza sativa L.) seedlings grown in solution culture. Environ Exp Bot 59:314–320
Mallick I, Bhattacharyya C, Mukherji S, Dey D, Sarkar SC, Mukhopadhyay UK, Ghosh A (2018) Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: a step towards arsenic rhizoremediation. Sci Total Environ 610:1239–1250
Martinez GM, Yousef CFUM (2010) LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture. Mol Microbiol 77:549–561
Mayes WM, Batty LC, Younger PL, Jarvis AP, Kõiv M, Vohla C, Mander U (2009) Wetland treatment at extremes of pH: a review. Sci Total Environ 407:3944–3957
Mays PA, Edwards GS (2001) Comparison of heavy metal accumulation in a natural wetland and constructed wetlands receiving acid mine drainage. Ecol Eng 16:487–500
Mendelssohn IA, Kleiss BA, Wakeley JS (1995) Factors controlling the formation of oxidized root channels: a review. Wetlands 15:37–46
Mentzer JL, Goodman RM, Balser TC (2006) Microbial response over time to hydrologic and fertilization treatments in a simulated wet prairie. Plant Soil 284:85–100
Morris CE, Monier JM (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41:429–453
Müller G, Patterson JW, Passino R (1990) Chemical decontamination of dredged materials, sludges, combustion residues, soils and other materials contaminated with heavy metals. In: Metals speciation, separation & recovery
Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454
Nadell CD, Drescher K, Wingreen NS, Bassler BL (2015) Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J 9:1700–1709
Nordstrom DK (1982) Aqueous pyrite oxidation and the consequent formation of secondary iron minerals. Vol WI53755. Acid sulfate weathering. Soil Science Society of America, pp 37–56
Peng W, Liu Y, Menzies NW, Wehr JB, Jonge MDD, Howard DL, Kopittke PM, Huang L (2016) Ferric minerals and organic matter change arsenic speciation in copper mine tailings. Environ Pollut 218:835–843
Perlatti F, Ferreira TO, Romero RE, Gomes Costa MC, Luis Otero X (2015) Copper accumulation and changes in soil physical-chemical properties promoted by native plants in an abandoned mine site in northeastern Brazil: implications for restoration of mine sites. Ecol Eng 82:103–111
Qiu R, Zhao B, Liu J, Huang X, Li Q, Brewer E, Wang S, Shi N (2009) Sulfate reduction and copper precipitation by a Citrobacter sp. isolated from a mining area. J Hazard Mater 164:1310–1315
Raiswell R, Canfield DE (2012) The iron biogeochemical cycle past and present. Geochem Perspect 1:1–220
Reddy KR, Delaune RD (2008) Biogeochemistry of wetlands. Vol FL. CRC Press, Boca Raton
Reis MP, Dias MF, Costa PS, MP Á, Leite LR, de Araújo FM, Salim AC, Bucciarellirodriguez M, Oliveira G, Chartonesouza E (2016) Metagenomic signatures of a tropical mining-impacted stream reveal complex microbial and metabolic networks. Chemosphere 161:266–273
Sarand I, Timonen S, Nurmiaholassila EL, Koivula T, Haahtela K, Romantschuk M, Sen R (1998) Microbial biofilms and catabolic plasmid harbouring degradative fluorescent pseudomonads in Scots pine mycorrhizospheres developed on petroleum contaminated soil. FEMS Microbiol Ecol 27:115–126
Schloter M, Borlinghaus R, Bode W, Hartmann A (2011) Direct identification, and localization of Azospirillum in the rhizosphere of wheat using fluorescence-labelled monoclonal antibodies and confocal scanning laser microscopy. J Microsc 171:173–177
Sheik CS, Mitchell TW, Rizvi FZ, Rehman Y, Faisal M, Hasnain S, Mcinerney MJ, Krumholz LR (2012) Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. PLoS One 7:e40059
Sheoran AS, Sheoran V (2006) Heavy metal removal mechanism of acid mine drainage in wetlands: a critical review. Miner Eng 19:105–116
Stein OR, Bordenstewart DJ, Hook PB, Jones WL (2007) Seasonal influence on sulfate reduction and zinc sequestration in subsurface treatment wetlands. Water Res 41:3440–3448
Stewart P, Franklin M (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6:199–210
Suárez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonça-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266
Sun X, Zhou Y, Tan Y, Wu Z, Lu P, Zhang G, Yu F (2018) Restoration with pioneer plants changes soil properties and remodels the diversity and structure of bacterial communities in rhizosphere and bulk soil of copper mine tailings in Jiangxi Province, China. Environ Sci Pollut Res 25:22106–22119
Tan GL, Shu WS, Hallberg KB, Li F, Lan CY, Zhou WH, Huang LN (2008) Culturable and molecular phylogenetic diversity of microorganisms in an open-dumped, extremely acidic Pb/Zn mine tailings. Extremophiles 12:657–664
Tian C, Wang C, Tian Y, Wul X, Xiao B (2015) Effects of root radial oxygen loss on microbial communities involved in Fe redox cycling in wetland plant rhizosphere sediment. Fresenius Environ Bull 24:3956–3962
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, Muyzer G, Bodelier PL, Laanbroek HJ (2009) Diversity of iron oxidizers in wetland soils revealed by novel 16S rRNA primers targeting Gallionella-related bacteria. ISME J 3:715–725
Weiss JV, Emerson D, Backer SM, Megonigal JP (2003) Enumeration of Fe(II)-oxidizing and Fe(III)-reducing bacteria in the root zone of wetland plants: implications for a rhizosphere iron cycle. Biogeochemistry 64:77–96
Winch S, Mills HJ, Kostka JE, Fortin D, Lean DRS (2010) Identification of sulfate-reducing bacteria in methylmercury-contaminated mine tailings by analysis of SSU rRNA genes. FEMS Microbiol Ecol 68:94–107
Wind T, Stubner S, Conrad R (1999) Sulfate-reducing bacteria in rice field soil and on rice roots. Syst Appl Microbial 22:269–279
Wu WM, Carley J, Luo J, Ginder-Vogel MA, Cardenas E, Leigh MB, Hwang CC, Kelly SD, Ruan CM, Wu LY, Van Nostrand J, Gentry T, Lowe K, Mehlhorn T, Carroll S, Luo WS, Fields MW, Gu BH, Watson D, Kemner KM, Marsh T, Tiedje J, Zhou JZ, Fendorf S, Kitanidis PK, Jardine PM, Criddle CS (2007) In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ Sci Technol 41:5716–5723
Wu C, Ye Z, Hui L, Wu S, Dan D, Zhu Y, Wong M (2012) Do radial oxygen loss and external aeration affect iron plaque formation and arsenic accumulation and speciation in rice? J Exp Bot 63:2961–2970
Wu C, Zou Q, Xue SG, Pan WS, Huang L, Hartley W, Mo JY, Wong MH (2016) The effect of silicon on iron plaque formation and arsenic accumulation in rice genotypes with different radial oxygen loss (ROL). Environ Pollut 212:27–33
Xu B, Wang F, Zhang Q, Lan Q, Liu C, Guo X, Cai Q, Chen Y, Wang G, Ding J (2018) Influence of iron plaque on the uptake and accumulation of chromium by rice (oryza sativa L.) seedlings: insights from hydroponic and soil cultivation. Ecotoxicol Environ Saf 162:51–58
Yamaguchi N, Ohkura T, Takahashi Y, Maejima Y, Arao T (2014) Arsenic distribution and speciation near rice roots influenced by iron plaques and redox conditions of the soil matrix. Environ Sci Technol 48:1549–1556
Yamauchi T, Shimamura S, Nakazono M, Mochizuki T (2013) Aerenchyma formation in crop species: a review. Field Crop Res 152:8–16
Yang J, Ma Z, Ye Z, Guo X, Qiu R (2010) Heavy metal (Pb, Zn) uptake and chemical changes in rhizosphere soils of four wetland plants with different radial oxygen loss. J Environ Sci 22:696–702
Yang J, Zheng G, Yang J, Wan X, Song B, Cai W, Guo J (2017) Phytoaccumulation of heavy metals (Pb, Zn, and Cd) by 10 wetland plant species under different hydrological regimes. Ecol Eng 107:56–64
Ye ZH, Ajm B, Wong MH, Willis AJ (1997) Zinc, lead and cadmium tolerance, uptake and accumulation by Typha latifolia. New Phytol 136:469–480
Ye ZH, Cheung KC, Wong MH (2003) Cadmium and nickel adsorption and uptake in cattail as affected by iron and manganese plaque on the root surface. Commun Soil Sci Plant Anal 34:2763–2778
Zhang Z, Moon HS, Myneni SCB, Jaffe PR (2017) Phosphate enhanced abiotic and biotic arsenic mobilization in the wetland rhizosphere. Chemosphere 187:130–139
Zhong S, Shi J, Xu J (2010) Influence of iron plaque on accumulation of lead by yellow flag (Iris pseudacorus L.) grown in artificial Pb-contaminated soil. J Soils Sediments 10:964–970
Zhou H, Zeng M, Zhou X, Liao BH, Peng PQ, Hu M, Zhu W, Wu YJ, Zou ZJ (2015) Heavy metal translocation and accumulation in iron plaques and plant tissues for 32 hybrid rice (Oryza sativa L.) cultivars. Plant Soil 386:317–329
Funding
This study was funded by National Natural Science Foundation of China (No. 41671313); National Key R&D Program of China (No. 2018YFD0800700); Science and Technology Planning Project of Guangdong Province, China (No. 2016A020221012; 2017B020216008); Science and Technology Planning Project of Guangzhou, China (No. 201804020021); and the 111 Project of China (No. B18060).
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Li, Y., Feng, W., Chi, H. et al. Could the rhizoplane biofilm of wetland plants lead to rhizospheric heavy metal precipitation and iron-sulfur cycle termination?. J Soils Sediments 19, 3760–3772 (2019). https://doi.org/10.1007/s11368-019-02343-1
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DOI: https://doi.org/10.1007/s11368-019-02343-1