Elevated methylmercury production in mercury-contaminated soil and its bioaccumulation in rice: key roles of algal decomposition

Abstract

● AOM input elevates water-soluble cysteine and labile DOM fractions in soil.

● AOM input fuels potential Hg methylators and non-Hg methylators in soil.

● Decayed algal aggregate is Hg methylating “hotspot” and MeHg source in soil.

● AOM-driven SDOM variations elevate soil MeHg production and bioaccumulation in rice.

Algal-derived organic matter (AOM) regulates methylmercury (MeHg) fate in aquatic ecosystems, whereas its role in MeHg production and bioaccumulation in Hg-contaminated paddies is unclear. Pot and microcosm experiments were thus performed to understand the response characteristics of MeHg concentrations in soil and rice in different rice-growing periods to algal decomposition. Compared to the control, algal decomposition significantly increased soil water-soluble cysteine concentrations during the rice-tillering and grain-filling periods (P < 0.05). It also significantly lowered the molecular weight of soil-dissolved organic matter (SDOM) during the rice-tillering period (P < 0.05) and SDOM humification/aromaticity during the grain-filling period. Compared to the control, AOM input increased the abundance of potential Hg and non-Hg methylators in soil. Furthermore, it also greatly increased soil MeHg concentrations by 25.6%–80.2% and 12.6%–66.1% during the rice-tillering and grain-filling periods, with an average of 42.25% and 38.42%, respectively, which were significantly related to the elevated cysteine in soil and the decrease in SDOM molecular weight (P < 0.01). In the early stage (within 10 days of microcosm experiments), the MeHg concentrations in decayed algal particles showed a great decrease (P < 0.01), suggesting a potential MeHg source in soil. Ultimately, algal decomposition greatly increased the MeHg concentrations and bioaccumulation factors in rice grains, by 72.30% and 16.77%, respectively. Overall, algal decomposition in Hg-contaminated paddies is a non-negligible factor promoting MeHg accumulation in soil-rice systems.

Graphical abstract

Keywords

Mercury / Methylmercury / Algae / Organic matter / Rice ( Oryza sativa L.)

References

[1] Bai L , Cao C , Wang C , Xu H , Zhang H , Slaveykova V I , Jiang H . (2017). Toward quantitative understanding of the bioavailability of dissolved organic matter in freshwater lake during cyanobacteria blooming. Environmental Science & Technology, 51(11): 6018–6026

[2] Bouchet S , Goñi-Urriza M , Monperrus M , Guyoneaud R , Fernandez P , Heredia C , Tessier E , Gassie C , Point D , Guédron S , Achá D , Amouroux D . (2018). Linking microbial activities and low-molecular-weight thiols to Hg methylation in biofilms and periphyton from high-altitude tropical lakes in the bolivian altiplano. Environmental Science & Technology, 52(17): 9758–9767

[3] Bravo A G , Bouchet S , Tolu J , Björn E , Mateosrivera A , Bertilsson S . (2017). Molecular composition of organic matter controls methylmercury formation in boreal lakes. Nature Communications, 8(1): 14255

[4] Fang F , Yang Y , Guo J , Zhou H , Fu C , Li Z . (2011). Three-dimensional fluorescence spectral characterization of soil dissolved organic matters in the fluctuating water-level zone of Kai County, Three Gorges Reservoir. Frontiers of Environmental Science & Engineering, 5(3): 426–434

[5] Gascón Díez E , Loizeau J L , Cosio C , Bouchet S , Adatte T , Amouroux D , Bravo A G . (2016). Role of settling particles on mercury methylation in the oxic water column of freshwater systems. Environmental Science & Technology, 50(21): 11672–11679

[6] Gionfriddo C, Capo E, Peterson B, Lin H, Jones D, Bravo A, Bertilsson S, Moreau J, Mcmahon K, Elias D, Gilmour C (2021). Hg-MATE-Db.v1.01142021: Hg-cycling microorganisms in aquatic and terrestrial ecosystems database, doi:10.5281/zenodo.6687122

[7] Guo P , Du H , Wang D , Ma M . (2021). Effects of mercury stress on methylmercury production in rice rhizosphere, methylmercury uptake in rice and physiological changes of leaves. Science of the Total Environment, 765: 142682

[8] Hanamachi Y , Hama T , Yanai T . (2008). Decomposition process of organic matter derived from freshwater phytoplankton. Limnology, 9(1): 57–69

[9] Hao Y , Zhu Y , Yan R , Gu B , Zhou X , Wei R , Wang C , Feng J , Huang Q , Liu Y . (2022). Important roles of thiols in methylmercury uptake and translocation by rice plants. Environmental Science & Technology, 56(10): 6765–6773

[10] He M, Tian L, Braaten H F V, Wu Q, Luo J, Cai L, Meng J, Lin Y (2019). Mercury-organic matter interactions in soils and sediments: angel or devil? Bulletin of Environmental Contamination and Toxicology, 102(5): 621–627

[11] Helms J R , Stubbins A , Ritchie J D , Minor E C , Kieber D J , Mopper K . (2008). Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter. Limnology and Oceanography, 54(3): 955–969

[12] Herrero Ortega S , Catalán N , Björn E , Gröntoft H , Hilmarsson T G , Bertilsson S , Wu P , Bishop K , Levanoni O , Bravo A G . (2018). High methylmercury formation in ponds fueled by fresh humic and algal derived organic matter. Limnology and Oceanography, 63(S1): S44–S53

[13] Huang M , Li Z , Wen J , Ding X , Zhou M , Cai C , Shen F . (2021). Molecular insights into the effects of pyrolysis temperature on composition and copper binding properties of biochar-derived dissolved organic matter. Journal of Hazardous Materials, 410: 124537

[14] Hulatt C J , Thomas D N , Bowers D G , Norman L , Zhang C . (2009). Exudation and decomposition of chromophoric dissolved organic matter (CDOM) from some temperate macroalgae. Estuarine, Coastal and Shelf Science, 84(1): 147–153

[15] Lázaro W L , Díez S , Bravo A G , Da Silva C J , Ignácio Á R A , Guimaraes J R D . (2019). Cyanobacteria as regulators of methylmercury production in periphyton. Science of the Total Environment, 668: 723–729

[16] Lázaro W L, Guimarães J R D, Ignácio A R A, Da Silva C J, Díez S (2013). Cyanobacteria enhance methylmercury production: a hypothesis tested in the periphyton of two lakes in the Pantanal floodplain, Brazil. Science of the Total Environment, 456–457: 231–238

[17] Leclerc M , Planas D , Amyot M . (2015). Relationship between extracellular low-molecular-weight thiols and mercury species in natural lake periphytic biofilms. Environmental Science & Technology, 49(13): 7709–7716

[18] Lei P , Nunes L M , Liu Y , Zhong H , Pan K . (2019). Mechanisms of algal biomass input enhanced microbial Hg methylation in lake sediments. Environment International, 126: 279–288

[19] Lei P , Zhang J , Zhu J , Tan Q , Kwong R W M , Pan K , Jiang T , Naderi M , Zhong H . (2021). Algal organic matter drives methanogen-mediated methylmercury production in water from eutrophic shallow lakes. Environmental Science & Technology, 55(15): 10811–10820

[20] Leite M F A , Pan Y , Bloem J , Berge H T , Kuramae E E . (2017). Organic nitrogen rearranges both structure and activity of the soil-borne microbial seedbank. Scientific Reports, 7(1): 42634

[21] Li J , Deng K , Cai S , Lu H , Xu R . (2020). Periphyton has the potential to increase phosphorus use efficiency in paddy fields. Science of the Total Environment, 720: 137711

[22] Li Z , Chi J , Wu Z , Zhang Y , Liu Y , Huang L , Lu Y , Uddin M , Zhang W , Wang X , Lin Y , Tong Y . (2022). Characteristics of plankton Hg bioaccumulations based on a global data set and the implications for aquatic systems with aggravating nutrient imbalance. Frontiers of Environmental Science & Engineering, 16(3): 37

[23] Liang L , Horvat M , Cernichiari E , Gelein B , Balogh S . (1996). Simple solvent extraction technique for elimination of matrix interferences in the determination of methylmercury in environmental and biological samples by ethylation-gas chromatography-cold vapor atomic fluorescence spectrometry. Talanta, 43(11): 1883–1888

[24] Liem-Nguyen V , Skyllberg U , Nam K , Björn E . (2017). Thermodynamic stability of mercury(II) complexes formed with environmentally relevant low-molecular-mass thiols studied by competing ligand exchange and density functional theory. Environmental Chemistry, 14(4): 243–253

[25] Liu J , Wang L , Zhu Y , Lin C , Jang C , Wang S , Xing J , Yu B , Xu H , Pan Y . (2019). Source attribution for mercury deposition with an updated atmospheric mercury emission inventory in the Pearl River Delta Region, China. Frontiers of Environmental Science & Engineering, 13(1): 2

[26] Liu M D , Zhang Q R , Cheng M H , He Y P , Chen L , Zhang H R , Cao H L , Shen H Z , Zhang W , Tao S , Wang X J . (2019a). Rice life cycle-based global mercury biotransport and human methylmercury exposure. Nature Communications, 10(1): 5164

[27] Liu Y , Yang Z , Zhou X , Qu X , Li Z , Zhong H . (2019b). Overlooked role of putative non-Hg methylators in predicting methylmercury production in paddy soils. Environmental Science & Technology, 53(21): 12330–12338

[28] Ma M , Du H , Wang D . (2019). Mercury methylation by anaerobic microorganisms: a review. Critical Reviews in Environmental Science and Technology, 49(20): 1893–1936

[29] Mangal V , Stenzler B R , Poulain A J , Guéguen C . (2019). Aerobic and anaerobic bacterial mercury uptake is driven by algal organic matter composition and molecular weight. Environmental Science & Technology, 53(1): 157–165

[30] Meng B , Feng X , Qiu G , Liang P , Li P , Chen C , Shang L . (2011). The process of methylmercury accumulation in rice (Oryza sativa L.). Environmental Science & Technology, 45(7): 2711–2717

[31] Nebbioso A , Piccolo A . (2013). Molecular characterization of dissolved organic matter (DOM): a critical review. Analytical and Bioanalytical Chemistry, 405(1): 109–124

[32] Ohno T . (2002). Fluorescence inner-filtering correction for determining the humification index of dissolved organic matter. Environmental Science & Technology, 36(4): 742–746

[33] Pickhardt P C , Folt C L , Chen C Y , Klaue B , Blum J D . (2005). Impacts of zooplankton composition and algal enrichment on the accumulation of mercury in an experimental freshwater food web. Science of the Total Environment, 339(1–3): 89–101

[34] Ravichandran M . (2004). Interactions between mercury and dissolved organic matter: a review. Chemosphere, 55(3): 319–331

[35] Schaefer J K , Morel F M M . (2009). High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens. Nature Geoscience, 2(2): 123–126

[36] Strickman R J , Mitchell C P J . (2017). Accumulation and translocation of methylmercury and inorganic mercury in Oryza sativa: an enriched isotope tracer study. Science of the Total Environment, 574: 1415–1423

[37] Su Y, Kwong R W M, Tang W, Yang Y, Zhong H (2021). Straw return enhances the risks of metals in soil? Ecotoxicology and Environmental Safety, 207: 111201

[38] Tang W , Hintelmann H , Gu B , Feng X , Liu Y , Gao Y , Zhao J , Zhu H , Lei P , Zhong H . (2019). Increased methylmercury accumulation in rice after straw amendment. Environmental Science & Technology, 53(11): 6144–6153

[39] Ullrich S M , Tanton T W , Abdrashitova S A . (2001). Mercury in the aquatic environment: a review of factors affecting methylation. Critical Reviews in Environmental Science and Technology, 31(3): 241–293

[40] Wang S , Sun P , Zhang G , Gray N , Dolfing J , Esquivel-Elizondo S , Peñuelas J , Wu Y . (2022). Contribution of periphytic biofilm of paddy soils to carbon dioxide fixation and methane emissions. The Innovation, 3(1): 100192

[41] Wei Z , Tang M , Huang Z , Jiao H . (2022). Mercury removal from flue gas using nitrate as an electron acceptor in a membrane biofilm reactor. Frontiers of Environmental Science & Engineering, 16(2): 20

[42] Weishaar J L , Aiken G R , Bergamaschi B A , Fram M S , Fujii R , Mopper K . (2003). Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environmental Science & Technology, 37(20): 4702–4708

[43] Wu Y (2021). Periphyton in Paddy Fields. Beijing: Science Press (in Chinese).

[44] Wu Y , Liu J , Lu H , Wu C , Kerr P . (2016). Periphyton: an important regulator in optimizing soil phosphorus bioavailability in paddy fields. Environmental Science and Pollution Research International, 23(21): 21377–21384

[45] Xiang Y , Liu G , Yin Y , Cai Y . (2021). Periphyton as an important source of methylmercury in Everglades water and food web. Journal of Hazardous Materials, 410: 124551

[46] Xiong Y . (2023). Characterization and variation of dissolved organic matter in composting: a critical review. Frontiers of Environmental Science & Engineering, 17(5): 63

[47] Xu J , Buck M , Eklof K , Ahmed O O , Schaefer J K , Bishop K , Skyllberg U , Bjorn E , Bertilsson S , Bravo A G . (2019). Mercury methylating microbial communities of boreal forest soils. Scientific Reports, 9(1): 518

[48] Yang J , Han M , Zhao Z , Jiang H . (2022). Positive priming effects induced by allochthonous and autochthonous organic matter input in the lake sediments with different salinity. Geophysical Research Letters, 49(5): e2021GL096133

[49] Yin D , He T , Yin R , Zeng L . (2018a). Effects of soil properties on production and bioaccumulation of methylmercury in rice paddies at a mercury mining area, China. Journal of Environmental Sciences (China), 68: 194–205

[50] Yin D , Wang Y , Jiang T , Qin C , Xiang Y , Chen Q , Xue J , Wang D . (2018b). Methylmercury production in soil in the water-level-fluctuating zone of the Three Gorges Reservoir, China: the key role of low-molecular-weight organic acids. Environmental Pollution, 235: 186–196

[51] Zhang H , Feng X , Larssen T , Shang L , Li P . (2010). Bioaccumulation of methylmercury versus inorganic mercury in rice (Oryza sativa L.) grain. Environmental Science & Technology, 44(12): 4499–4504

[52] Zhang T , Ma H , Hong Z , Fu G , Zheng Y , Li Z , Cui F . (2022). Photo-reactivity and photo-transformation of algal dissolved organic matter unraveled by optical spectroscopy and high-resolution mass spectrometry analysis. Environmental Science & Technology, 56(18): 13439–13448

[53] Zhao J , Ye Z , Zhong H . (2018). Rice root exudates affect microbial methylmercury production in paddy soils. Environmental Pollution, 242: 1921–1929

[54] Zhao L , Meng B , Feng X . (2020). Mercury methylation in rice paddy and accumulation in rice plant: a review. Ecotoxicology and Environmental Safety, 195: 110462

[55] Zhao Q , Wang J , Ouyang S , Chen L , Liu M , Li Y , Jiang F . (2021). The exacerbation of mercury methylation by Geobacter sulfurreducens PCA in a freshwater algae-bacteria symbiotic system throughout the lifetime of algae. Journal of Hazardous Materials, 415: 125691

[56] Zhu A, Gao J, Huang J, Wang H, Chen Y, Liu L (2020). Advances in morphology and physiology of root and their relationships with grain quality in rice. Crops, 2: 1–8 (in Chinese with English abstract)

RIGHTS & PERMISSIONS

Higher Education Press