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Periphyton growth reduces cadmium but enhances arsenic accumulation in rice (Oryza sativa) seedlings from contaminated soil

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Abstract

Background and aims

Periphyton is ubiquitous in paddy fields, but its role in arsenic (As) and cadmium (Cd) bioavailability to rice plants remains unknown.

Methods

A paddy field was simulated under controlled conditions to investigate the influences of periphyton on As and Cd accumulation in rice seedlings grown in soil contaminated with both As and Cd.

Results

The presence of periphyton significantly enhanced the growth of rice seedlings in As and Cd contaminated soil. Periphyton had significant effects on soil pH and Eh, resulting in a substantial decrease in the Cd concentration, but in an increase in the total As and As (III) concentrations in soil solution. Corresponding with these changes, Cd concentrations in rice roots and shoots were significantly decreased in the presence of periphyton, while As concentrations increased.

Conclusions

This study demonstrates that periphyton growth can significantly affect soil As, Cd bioavailability and soil As speciation by changing soil pH and Eh, which affect As and Cd accumulation in rice seedlings as a result. These results suggest that controlling native periphyton growth may be an effective strategy to regulate As and Cd translocation to the edible organs of food crops.

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References

  • Ali B, Wang B, Ali S, Ghani MA, Hayat MT, Yang HC, Xu L, Zhou WJ (2013) 5-Aminolevulinic acid ameliorates the growth, photosynthetic gas exchange capacity, and ultrastructural changes under cadmium stress in Brassica napus L. J Plant Growth Regul 32:604–614

    Article  CAS  Google Scholar 

  • Bradac P, Wagner B, Kistler D, Traber J, Behra R, Sigg L (2010) Cadmium speciation and accumulation in periphyton in a small stream with dynamic concentration variations. Environ Pollut 158:641–648

    Article  CAS  PubMed  Google Scholar 

  • Brennan A, Jiménez EM, Puschenreiter M, Alburquerque JA, Switzer C (2014) Effects of biochar amendment on root traits and contaminant availability of maize plants in a copper and arsenic impacted soil. Plant Soil 379:351–360

    Article  CAS  Google Scholar 

  • Bustingorri C, Noriega G, Lavado R, Balestrasse K (2017) Protective effect exerted by soil phosphorus on soybean subjected to arsenic and fluoride. Redox Rep. https:/doi.org/10.1080/13510002.2016.1276253

  • Christen K (2001) The arsenic threat worsens. Environ Sci Technol 35:286A–291A

    Article  CAS  PubMed  Google Scholar 

  • Dong D, Li Y, Zhang J, Hua X (2003) Comparison of the adsorption of lead, cadmium, copper, zinc and barium to freshwater surface coatings. Chemosphere 51:369–373

    Article  CAS  PubMed  Google Scholar 

  • Fan Y, Sun X, Yang W, Ma N, Xin Z, Fu J, Liu X, Liu M, Mariga AM, Zhu X, Hu Q (2014) Concentrations and health risks of lead, cadmium, arsenic, and mercury in rice and edible mushrooms in China. Food Chem 147:147–151

    Article  Google Scholar 

  • Gunes A, Pilbeam D, Inal A (2009) Effect of arsenic–phosphorus interaction on arsenic-induced oxidative stress in chickpea plants. Plant Soil 314:211–220

    Article  CAS  Google Scholar 

  • He BY, Ling L, Zhang LY, Li MR, Li QS, Mei XQ, Li H, Tan L (2015) Cultivar-specific differences in heavy metal (Cd, Cr, Cu, Pb, and Zn) concentrations in water spinach (Ipomoea aquatic ‘Forsk’) grown on metal-contaminated soil. Plant Soil 386:251–262

    Article  CAS  Google Scholar 

  • Honma T, Ohba H, Kaneko-Kadokura A, Makino T, Nakamura K, Katou H (2016) Optimal soil Eh, pH, and water management for simultaneously minimizing arsenic and cadmium concentrations in rice grains. Environ Sci Technol 50:4178–4185

    Article  CAS  PubMed  Google Scholar 

  • Inglett P, Reddy K, McCormick P (2004) Periphyton chemistry and nitrogenase activity in a northern Everglades ecosystem. Biogeochemistry 67:213–233

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Stroud JL, Zhu YG, McGrath SP, Zhao FJ (2010) Arsenic bioavailability to rice is elevated in Bangladeshi paddy soils. Environ Sci Technol 44:8515–8521

    Article  CAS  PubMed  Google Scholar 

  • Kim M, Wolt JD (2008) Cadmium exposure in the South Korean population: implications of input assumptions for deterministic dietary assessment. Hum Ecol Risk Assess 14:835–850

    Article  CAS  Google Scholar 

  • Larned ST, Nikora VI, Biggs BJF (2004) Mass-transfer-limited nitrogen and phosphorus uptake by stream periphyton: A conceptual model and experimental evidence. Limnol Oceanogr 49:1992–2000

    Article  CAS  Google Scholar 

  • Lee DA, Chen A, Schroeder JI (2003) ars1, an Arabidopsis mutant exhibiting increased tolerance to arsenate and increased phosphate uptake. Plant J 35:637–646

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Donner E, Lombi E, Li R, Wu Z, Zhao FJ, Wu P (2013) Assessing the contributions of lateral roots to element uptake in rice using an auxin-related lateral root mutant. Plant Soil 372:125–136

    Article  CAS  Google Scholar 

  • Liu H, Wang H, Ma Y, Wang H, Shi Y (2016a) Role of transpiration and metabolism in translocation and accumulation of cadmium in tobacco plants (Nicotiana tabacum L.) Chemosphere 144:1960–1965

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Danneels B, Vanormelingen P, Vyverman W (2016b) Nutrient removal from horticultural wastewater by benthic filamentous algae Klebsormidium sp., Stigeoclonium spp. and their communities: from laboratory flask to outdoor algal turf scrubber (ATS). Water Res 92:61–68

    Article  CAS  PubMed  Google Scholar 

  • Lomax C, Liu WJ, LY W, Xue K, Xiong JB, Zhou J, McGrath SP, Meharg AA, Miller AJ, Zhao FJ (2012) Methylated arsenic species in plants originate from soil microorganisms. New Phytol 193:665–672

    Article  CAS  PubMed  Google Scholar 

  • Lou LQ, Shi GL, JH W, Zhu S, Qian M, Wang HZ, Cai QS (2015) The influence of phosphorus on arsenic uptake/efflux and As toxicity to wheat roots in comparison with sulfur and silicon. J Plant Growth Regul 20:242–250

    Article  Google Scholar 

  • Lu Z, Zhang Z, Su Y, Liu C, Shi G (2013) Cultivar variation in morphological response of peanut roots to cadmium stress and its relation to cadmium accumulation. Ecotox Environ Safe 91:147–155

    Article  CAS  Google Scholar 

  • Lu H, Yang L, Zhang S, Wu Y (2014) The behavior of organic phosphorus under nonpoint source wastewater in the presence of phototrophic periphyton. PLoS One 9:e85910

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu H, Wan J, Li Y, Shao H, Wu Y (2016) Periphytic biofilm: A buffer for phosphorus precipitation and release between sediments and water. Chemosphere 144:2058–2064

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Liu J, Kerr PG, Shao H, Wu Y (2017) The effect of periphyton on seed germination and seedling growth of rice (Oryza sativa) in paddy area. Sci Total Environ 578:74–80

    Article  CAS  PubMed  Google Scholar 

  • Luo XS, Yu S, Li XD (2012) The mobility, bioavailability, and human bioaccessibility of trace metals in urban soils of Hong Kong. Appl Geochem 27:995–1004

    Article  CAS  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Xu X, Su Y, McGrath SP, Zhao F (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci U S A 105:9931–9935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C, Villada A, Cambell RCJ, Sun GX, Zhu YG, Feldmann J, Raab A, Zhao FJ, Islam R, Hossain S, Yanai J (2009) Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol 43:1612–1617

    Article  CAS  PubMed  Google Scholar 

  • Meharg AA, Norton G, Deacon C, Williams P, Adomako EE, Price A, Zhu Y, Li G, Zhao FJ, McGrath S, Villada A, Sommella A, De Silva PMCS, Brammer H, Dasgupta T, Islam MR (2013) Variation in rice cadmium related to human exposure. Environ Sci Technol 47:5613–5618

    Article  CAS  PubMed  Google Scholar 

  • Mondal D, Polya DA (2008) Rice is a major exposure route for arsenic in Chakdaha block, Nadia district, West Bengal, India: A probabilistic risk assessment. Appl Geochem 23:2987–2998

    Article  CAS  Google Scholar 

  • Nordstrom DK (2002) Worldwide occurrences of arsenic in ground water. Science 296:2143–2145

    Article  CAS  PubMed  Google Scholar 

  • Rosén K, Eriksson J, Vinichuk M (2012) Uptake and translocation of 109Cd and stable Cd within tobacco plants (Nicotiana sylvestris). J Environ Radioactiv 113:16–20

    Article  Google Scholar 

  • Shabbir S, Faheem M, Ali N, Kerr PG, Wu Y (2017) Periphyton biofilms: A novel and natural biological system for the effective removal of sulphonated azo dye methyl orange by synergistic mechanism. Chemosphere 167:236–246

    Article  CAS  PubMed  Google Scholar 

  • Shan H, Su S, Liu R, Li S (2016) Cadmium availability and uptake by radish (Raphanus sativus) grown in soils applied with wheat straw or composted pig manure. Environ Sci Pollut Res 23:1–10

    Article  Google Scholar 

  • Shelmerdine PA, Black CR, McGrath SP, Young SD (2009) Modelling phytoremediation by the hyperaccumulating fern, Pteris vittata, of soils historically contaminated with arsenic. Environ Pollut 157:1589–1596

    Article  CAS  PubMed  Google Scholar 

  • Shi GL, Lou LQ, Zhang S, Xia XW, Cai QS (2013) Arsenic, copper, and zinc contamination in soil and wheat during coal mining, with assessment of health risks for the inhabitants of Huaibei, China. Environ Sci Pollut Res 20:8435–8445

    Article  CAS  Google Scholar 

  • Shi GL, Zhu S, Bai S, Xia Y, Lou LQ, Cai QS (2015) The transportation and accumulation of arsenic, cadmium, and phosphorus in 12 wheat cultivars and their relationships with each other. J Hazard Mater 299:94–102

    Article  CAS  PubMed  Google Scholar 

  • Siripornadulsil S, Siripornadulsil K (2013) Cadmium-tolerant bacteria reduce the uptake of cadmium in rice: Potential for microbial bioremediation. Ecotox Environ Safe 94:94–103

    Article  CAS  Google Scholar 

  • Song WY, Yang HC, Shao HB, Zheng AZ, Brestic M (2014) The alleviative effects of salicylic acid on the activities of catalase and superoxide dismutase in malting barley (Hordeum uhulgare L.) seedling leaves stressed by heavy metals. CLEAN–Soil, Air, Water 42:88–97

    Article  CAS  Google Scholar 

  • Stroud JL, Khan MA, Norton GJ, Islam MR, Dasgupta T, Zhu YG, Price AH, Meharg AA, McGrath SP, Zhao FJ (2011) Assessing the labile arsenic pool in contaminated paddy soils by isotopic dilution techniques and simple extractions. Environ Sci Technol 45:4262–4269

    Article  CAS  PubMed  Google Scholar 

  • Suda A, Makino T (2016) Functional effects of manganese and iron oxides on the dynamics of trace elements in soils with a special focus on arsenic and cadmium: a review. Geoderma 270:68–75

    Article  CAS  Google Scholar 

  • Sytar O, Brestic M, Taran N, Zivcak M (2016) Plants used for biomonitoring and phytoremediation of trace elements in soil and water. Plant metal interaction: emerging remediation techniques. Elsevier, Amsterdam, pp 61–384

    Google Scholar 

  • Szlauer-Łukaszewska A (2007) Succession of periphyton developing on artificial substrate immersed in polysaprobic wastewater reservoir. Polish J Environ Stud 16:753–762

    Google Scholar 

  • Takahashi Y, Minamikawa R, Hattori KH, Kurishima K, Kihou N, Yuita K (2004) Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environ Sci Technol 38:1038–1044

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Cui J, Shan B, Wang C, Zhang W (2014) Heavy metal accumulation by periphyton is related to eutrophication in the Hai River Basin, Northern China. PLoS One 9:e86458

    Article  PubMed  PubMed Central  Google Scholar 

  • Tao Y, Zhang S, Jian W, Yuan C, Shan XQ (2006) Effects of oxalate and phosphate on the release of arsenic from contaminated soils and arsenic accumulation in wheat. Chemosphere 65:1281–1287

    Article  CAS  PubMed  Google Scholar 

  • Tuulaikhuu B, Bonet B, Guasch H (2016) Effects of low arsenic concentration exposure on freshwater fish in the presence of fluvial biofilms. Sci Total Environ 544:467–475

    Article  CAS  PubMed  Google Scholar 

  • Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Vadeboncoeur Y, Steinman AD (2002) Periphyton function in lake ecosystems. Sci World J 2:1449–1468

    Article  Google Scholar 

  • Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ, Feldmann J, Meharg AA (2007) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41:6854–6859

    Article  CAS  PubMed  Google Scholar 

  • Writer JH, Ryan JN, Barber LB (2011) Role of biofilms in sorptive removal of steroidal hormones and 4-Nonylphenol compounds from streams. Environ Sci Technol 45:7275–7283

    Article  CAS  PubMed  Google Scholar 

  • Wu YH, Li TL, Yang LZ (2012) Mechanisms of removing pollutants from aqueous solutions by microorganisms and their aggregates: a review. Bioresour Technol 107:10–18

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Liu J, Lu H, Wu C, Kerr P (2016) Periphyton: an important regulator in optimizing soil phosphorus bioavailability in paddy fields. Environ Sci Pollut Res 23:21377–21384

    Article  CAS  Google Scholar 

  • Xu XY, McGrath SP, Meharg A, Zhao FJ (2008) Growing rice aerobically markedly decreases arsenic accumulation. Environ Sci Technol 42:5574–5579

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi N, Nakamura T, Dong D, Takahashi Y, Amachi S, Makino T (2011) Arsenic release from flooded paddy soils is influenced by speciation, Eh, pH, and iron dissolution. Chemosphere 83:925–932

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Tang C, Wang F, Wu Y (2016) Co-contamination of Cu and Cd in paddy fields: Using periphyton to entrap heavy metals. J Hazard Mater 304:150–158

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Liu C, Zhu J, Li F, Deng D, Wang Q, Liu C (2016a) Cadmium availability in rice paddy fields from a mining area: The effects of soil properties highlighting iron fractions and pH value. Environ Pollut 209:38–45

    Article  CAS  PubMed  Google Scholar 

  • Yu HY, Ding X, Li F, Wang X, Zhang S, Yi J, Liu C, Xu X, Wang Q (2016b) The availabilities of arsenic and cadmium in rice paddy fields from a mining area: The role of soil extractable and plant silicon. Environ Pollut 215:258–265

    Article  CAS  PubMed  Google Scholar 

  • Zhong MS, Jiang L, Han D, Xia TX, Yao JJ, Jia XY, Peng C (2015) Cadmium exposure via diet and its implication on the derivation of health-based soil screening values in China. J Expo Sci Environ Epid 25:433–442

    Article  CAS  Google Scholar 

  • Zhu YG, Yoshinaga M, Zhao FJ, Rosen BP (2014) Earth abides arsenic biotransformations. Annu Rev Earth Planet Sci 42:443–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Financial support from the National Natural Science Foundation of China (41601541 and 41601320), the Natural Science Foundation of Jiangsu Province (BK20160593 and BK20160594), and the Open Foundation of the State Key Laboratory of Soil and Sustainable Agriculture of China (Y20160035) are gratefully acknowledged.

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Author notes

  1. Gao Ling Shi and Hai Ying Lu contributed equally to this work.

Authors and Affiliations

  1. Institute of Food Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, People’s Republic of China

    Gao Ling Shi & Hong Xiang Ma

  2. Institute of Agricultural Resources and Environment, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, People’s Republic of China

    Hai Ying Lu

  3. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, People’s Republic of China

    Jun Zhuo Liu & Yong Hong Wu

  4. College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Lai Qing Lou

  5. Institute of Soil and Water Resources and Environmental Science, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Xian Jin Tang

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  1. Gao Ling Shi
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  2. Hai Ying Lu
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  3. Jun Zhuo Liu
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  4. Lai Qing Lou
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Correspondence to Hai Ying Lu or Hong Xiang Ma.

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Shi, G.L., Lu, H.Y., Liu, J.Z. et al. Periphyton growth reduces cadmium but enhances arsenic accumulation in rice (Oryza sativa) seedlings from contaminated soil. Plant Soil 421, 137–146 (2017). https://doi.org/10.1007/s11104-017-3447-y

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  • DOI: https://doi.org/10.1007/s11104-017-3447-y

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