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Soil microalgae modulate grain arsenic accumulation by reducing dimethylarsinic acid and enhancing nutrient uptake in rice (Oryza sativa L.)

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Abstract

Background and aims

Microalgae are ubiquitous in paddy soils. However, their roles in arsenic (As) accumulation and transport in rice plants remains unknown.

Methods

Two green algae and five cyanobacteria were used in pot experiments under continuously flooded conditions to ascertain whether a microalgal inoculation could influence rice growth and rice grain As accumulation in plants grown in As-contaminated soils.

Results

The microalgal inoculation greatly enhanced nutrient uptake and rice growth. The presence of representative microalga Anabaena azotica did not significantly differ the grain inorganic As concentrations but remarkably decreased the rice root and grain DMA concentrations. The translocation of As from roots to grains was also markedly decreased by rice inoculated with A. azotica. This subsequently led to a decrease in the total As concentration in rice grains.

Conclusions

The results of the study indicate that the microalgal inoculation had a strong influence on soil pH, soil As speciation, and soil nutrient bioavailability, which significantly affected the rice growth, nutrient uptake, and As accumulation and translocation in rice plants. The results suggest that algae inoculation can be an effective strategy for improving nutrient uptake and reducing As translocation from roots to grains by rice grown in As-contaminated paddy soils.

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References

  • Awasthi S, Chauhan R, Dwivedi S, Srivastava S, Srivastava S, Tripathi RD (2018) A consortium of alga (Chlorella vulgaris) and bacterium (Pseudomonas putida) for amelioration of arsenic toxicity in rice: a promising and feasible approach. Environ Exp Bot 150:115–126

    Article  CAS  Google Scholar 

  • Bahar MM, Megharaj M, Naidu R (2016) Influence of phosphate on toxicity and bioaccumulation of arsenic in a soil isolate of microalga Chlorella sp. Environ Sci Pollut Res 23:2663–2668

    Article  CAS  Google Scholar 

  • Burt R (2009) Soil survey field and laboratory methods manual. US Department of Agriculture, Nebrasca

    Google Scholar 

  • Chen X, Li H, Chan WF, Wu C, Wu F, Wu S, Wong MH (2012) Arsenite transporters expression in rice (Oryza sativa L.) associated with arbuscular mycorrhizal fungi (AMF) colonization under different levels of arsenite stress. Chemosphere 89:1248–1254

    Article  PubMed  CAS  Google Scholar 

  • Codex Alimentarius Commission (2014) Report of the eighth Session of the codex committee on contaminants in foods. Hague, Netherlands. Available online at http://www.fao.org/news/story/en/item/238558/icode/

  • Han YH, Liu X, Rathinasabapathi B, Li HB, Chen Y, Ma LQ (2017a) Mechanisms of efficient As solubilization in soils and As accumulation by As-hyperaccumulator Pteris vittata. Environ Pollut 227:569–577

    Article  PubMed  CAS  Google Scholar 

  • Han YH, Fu JW, Xiang P, Cao Y, Rathinasabapathi B, Chen Y, Ma LQ (2017b) Arsenic and phosphate rock impacted the abundance and diversity of bacterial arsenic oxidase and reductase genes in rhizosphere of As-hyperaccumulator Pteris vittata. J Hazard Mater 321:146–153

    Article  PubMed  CAS  Google Scholar 

  • Jia Y, Sun GX, Huang H, Zhu YG (2013) Biogas slurry application elevated arsenic accumulation in rice plant through increased arsenic release and methylation in paddy soil. Plant Soil 365:387–396

    Article  CAS  Google Scholar 

  • Li RY, Ago Y, Liu WJ, Mitani N, Feldmann J, McGrath SP, Ma JF, Zhao FJ (2009) The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150:2071–2080

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li G, Sun GX, Williams PN, Nunes L, Zhu YG (2011) Inorganic arsenic in Chinese food and its cancer risk. Environ Int 37:1219–1225

    Article  PubMed  CAS  Google Scholar 

  • Lomax C, Liu WJ, Wu L, Xue K, Xiong J, 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  PubMed  CAS  Google Scholar 

  • Ma R, Shen J, Wu J, Tang Z, Shen Q, Zhao FJ (2014) Impact of agronomic practices on arsenic accumulation and speciation in rice grain. Environ Pollut 194:217–223

    Article  PubMed  CAS  Google Scholar 

  • Ministry of Health of the People's Republic of China (2012) Maximum levels of contaminants in foods GB 2762–2012. Beijing, China. Available online at http://www.nhfpc.gov.cn/sps/s7891/201301/16482cd1dec04196a4037d86104dcca9.shtml

  • Mishra S, Mattusch J, Wennrich R (2017) Accumulation and transformation of inorganic and organic arsenic in rice and role of thiol-complexation to restrict their translocation to shoot. Sci Rep 7:40522

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Naveed S, Dong B, Zhang C, Ge Y (2018) Microalgae and their effects on metal bioavailability in paddy fields. J Soils Sediments 18:936–945

    Article  CAS  Google Scholar 

  • Norton GJ, Pinson SRM, Alexander J, McKay S, Hansen H, Duan GL, Rafiqul Islam M, Islam S, Stroud JL, Zhao FJ, McGrath SP, Zhu YG, Lahner B, Yakubova E, Guerinot ML, Tarpley L, Eizenga GC, Salt DE, Meharg AA, Price AH (2012) Variation in grain arsenic assessed in a diverse panel of rice (Oryza sativa) grown in multiple sites. New Phytol 193:650–664

    Article  PubMed  CAS  Google Scholar 

  • Panaullah GM, Alam T, Hossain MB, Loeppert RH, Lauren JG, Meisner CA, Ahmed ZU, Duxbury JM (2009) Arsenic toxicity to rice (Oryza sativa L.) in Bangladesh. Plant Soil 317:31–39

    Article  CAS  Google Scholar 

  • Rahman MA, Hasegawa H, Rahman MM, Miah MAM, Tasmin A (2008) Arsenic accumulation in rice (Oryza sativa L.): human exposure through food chain. Ecotoxicol Environ Saf 69:317–324

    Article  CAS  Google Scholar 

  • Ranjan K, Priya H, Ramakrishnan B, Prasanna R, Venkatachalam S, Thapa S, Tiwari R, Nain L, Singh R, Shivay YS (2016) Cyanobacterial inoculation modifies the rhizosphere microbiome of rice planted to a tropical alluvial soil. Appl Soil Ecol 108:195–203

    Article  Google Scholar 

  • Ranjan R, Kumar N, Dubey AK, Gautam A, Pandey SN, Mallick S (2018) Diminution of arsenic accumulation in rice seedlings co-cultured with Anabaena sp.: modulation in the expression of lower silicon transporters, two nitrogen dependent genes and lowering of antioxidants activity. Ecotoxicol Environ Saf 151:109–117

    Article  PubMed  CAS  Google Scholar 

  • Rossi F, Li H, Liu Y, De Philippis R (2017) Cyanobacterial inoculation (cyanobacterisation): perspectives for the development of a standardized multifunctional technology for soil fertilization and desertification reversal. Earth-Sci Rev 171:28–43

    Article  Google Scholar 

  • Saadatnia H, Riahi H (2009) Cyanobacteria from paddy fields in Iran as a biofertilizer in rice plants. Plant Soil Environ 55:207–212

    Article  Google Scholar 

  • Shi GL, Lu HY, Liu JZ, Lou LQ, Tang XJ, Wu YH, Ma HX (2017) Periphyton growth reduces cadmium but enhances arsenic accumulation in rice (Oryza sativa) seedlings from contaminated soil. Plant Soil 421:137–146

    Article  CAS  Google Scholar 

  • Srivastava S, Srivastava S, Bist V, Awasthi S, Chauhan R, Chaudhry V, Singh PC, Dwivedi S, Niranjan A, Agrawal L, Chauhan PS, Tripathi RD, Nautiyal CS (2018) Chlorella vulgaris and Pseudomonas putida interaction modulates phosphate trafficking for reduced arsenic uptake in rice (Oryza sativa L.). J Hazard Mater 351:177–187

    Article  PubMed  CAS  Google Scholar 

  • Su YH, McGrath SP, Zhao FJ (2010) Rice is more efficient in arsenite uptake and translocation than wheat and barley. Plant Soil 328:27–34

    Article  CAS  Google Scholar 

  • Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R (2013) Mixotrophic cyanobacteria and microalgae as distinctive biological agents for organic pollutant degradation. Environ Int 51:59–72

    Article  PubMed  CAS  Google Scholar 

  • Subashchandrabose SR, Megharaj M, Venkateswarlu K, Naidu R (2015) Interaction effects of polycyclic aromatic hydrocarbons and heavy metals on a soil microalga, Chlorococcum sp. MM11. Environ Sci Pollut Res 22:8876–8889

    Article  CAS  Google Scholar 

  • Sundaram S, Rathinasabapathi B, Ma LQ, Rosen BP (2008) An arsenate-activated glutaredoxin from the arsenic hyperaccumulator fern Pteris vittata L. regulates intracellular arsenite. J Biol Chem 283:6095–6101

    Article  PubMed  CAS  Google Scholar 

  • The ministry of environmental protection (2014) The ministry of land and resources report on the national soil contamination survey. Beijing, China. Available online at http://www.mep.gov.cn/gkml/hbb/qt/201404/t20140417_270670.htm

  • Upadhyay AK, Singh NK, Singh R, Rai UN (2016) Amelioration of arsenic toxicity in rice: comparative effect of inoculation of Chlorella vulgaris and Nannochloropsis sp. on growth, biochemical changes and arsenic uptake. Ecotoxicol Environ Saf 124:68–73

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Wang S, Xu P, Liu C, Liu M, Wang Y, Wang C, Zhang C, Ge Y (2015) Review of arsenic speciation, toxicity and metabolism in microalgae. Rev Environ Sci Biotechnol 14:427–451

    Article  CAS  Google Scholar 

  • Wang Y, Zhang CH, Lin MM, Ge Y (2016) A symbiotic bacterium differentially influences arsenate absorption and transformation in Dunaliella salina under different phosphate regimes. J Hazard Mater 318:443–451

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Zhang C, Zheng Y, Ge Y (2017a) Bioaccumulation kinetics of arsenite and arsenate in Dunaliella salina under different phosphate regimes. Environ Sci Pollut Res 24:21213–21221

    Article  CAS  Google Scholar 

  • Wang Y, Zhang C, Zheng Y, Ge Y (2017b) Phytochelatin synthesis in Dunaliella salina induced by arsenite and arsenate under various phosphate regimes. Ecotoxicol Environ Saf 136:150–160

    Article  PubMed  CAS  Google Scholar 

  • Wenzel WW, Kirchbaumer N, Prohaska T, Stingeder G, Lombi E, Adriano DC (2001) Arsenic fractionation in soils using an improved sequential extraction procedure. Anal Chim Acta 436:309–323

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Rensing C, Zhu YG (2014) Cyanobacteria-mediated arsenic redox dynamics is regulated by phosphate in aquatic environments. Environ Sci Technol 48:994–1000

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Zhou W, Liu B, He J, Shen Q, Zhao FJ (2015) Anaerobic arsenite oxidation by an autotrophic arsenite-oxidizing bacterium from an arsenic-contaminated paddy soil. Environ Sci Technol 49:5956–5964

    Article  PubMed  CAS  Google Scholar 

  • Zhao FJ, McGrath SP, Meharg AA (2010a) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559

    Article  PubMed  CAS  Google Scholar 

  • Zhao K, Liu X, Xu J, Selim H (2010b) Heavy metal contaminations in a soil-rice system: identification of spatial dependence in relation to soil properties of paddy fields. J Hazard Mater 181:778–787

    Article  PubMed  CAS  Google Scholar 

  • Zhao FJ, Harris E, Yan J, Ma J, Wu L, Liu W, McGrath SP, Zhou J, Zhu YG (2013a) Arsenic methylation in soils and its relationship with microbial arsM abundance and diversity, and As speciation in rice. Environ Sci Technol 47:7147–7154

    Article  PubMed  CAS  Google Scholar 

  • Zhao FJ, Zhu YG, Meharg AA (2013b) Methylated arsenic species in rice: geographical variation, origin, and uptake mechanisms. Environ Sci Technol 47:3957–3966

    Article  PubMed  CAS  Google Scholar 

  • Zhao FJ, Ma Y, Zhu YG, Tang Z, McGrath SP (2015) Soil contamination in China: current status and mitigation strategies. Environ Sci Technol 49:750–759

    Article  PubMed  CAS  Google Scholar 

  • Zheng MZ, Li G, Sun GX, Shim H, Cai C (2013) Differential toxicity and accumulation of inorganic and methylated arsenic in rice. Plant Soil 365:227–238

    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  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

This research is supported by the National Natural Science Foundation of China (41701373, 31772197) and China Postdoctoral Science Foundation funded project (2017 M621667). The authors are grateful to Associate Professor Gaoling Shi in Jiangsu Academy of Agricultural Sciences and Dr. Yong-He Han in the Fujian Normal University for their constructive suggestions in manuscript preparation. We also thank Dr. Shuo Liu and Jiali Yan in State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University for providing rice seed.

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Correspondence to Ying Ge or Xiang Yang Yu.

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Responsible Editor: Juan Barcelo.

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Wang, Y., Li, Y.Q., Lv, K. et al. Soil microalgae modulate grain arsenic accumulation by reducing dimethylarsinic acid and enhancing nutrient uptake in rice (Oryza sativa L.). Plant Soil 430, 99–111 (2018). https://doi.org/10.1007/s11104-018-3719-1

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