The Contact Toxicity of Arsenic to Earthworms and Regulatory Effect of Selenium

doi:10.11924/j.issn.1000-6850.casb2023-0525

Abstract

Abstract:

To investigate the acute filter paper contact toxicity of heavy metal arsenic (As) to earthworms and the regulatory effect of selenium (Se), Eisenia fetida was exposed to two media (filter paper and soil) with different concentrations of Se, and then the acute toxicity test of As was conducted by filter paper contact method. The results showed that the half lethal concentrations (LC₅₀) on E. fetida directly exposed to As (V) contaminated filter paper for 24 and 48 h were 31.33 and 12.30 μg/cm², respectively. After a 6 h period of adaptation on wet filter paper with Se concentration of 0.5 μg/cm², the LC₅₀ of As on E. fetida were 30.20 (24 h) and 15.85 μg/cm² (48 h), respectively. After adapting to soil with Se concentrations of 6 and 12 mg/kg for one week, the LC₅₀ of As to earthworms were 34.67-35.48 μg/cm²(24 h) and 18.62-21.88 μg/cm² (48 h), respectively. In conclusion, the pre-exposure of earthworms in Se-containing filter paper and soil both stimulated the improvement of LC₅₀ values at 48 h, indicating that Se can improve the ability of earthworms to tolerate As stress during short exposure periods. This study provides new research ideas and methods for alleviating heavy metal pollution stress on soil biota.

Key words: arsenic, selenium, Eisenia fetida, exposure toxicity, alleviate

YANG Ying, WANG Zhimin, DU Jingjing, ZHOU Zihan, ZHOU Shengzhi, FU Xiaowen, WANG Ruiping, YUE Shizhong. The Contact Toxicity of Arsenic to Earthworms and Regulatory Effect of Selenium[J]. Chinese Agricultural Science Bulletin, 2024, 40(17): 49-55.

Figures/Tables 5

References 40

[1]	RODRIGUEZ-LADO L, SUN G, BERG M, et al. Groundwater arsenic contamination throughout China[J]. Science, 2013, 341(6148):866-868.
[2]	PODGORSKI J, BERG M. Global threat of arsenic in groundwater[J]. Science, 2020, 368(6493):845-850. doi: 10.1126/science.aba1510 pmid: 32439786
[3]	段桂兰, 崔慧灵, 杨雨萍, 等. 重金属污染土壤中生物间相互作用及其协同修复应用[J]. 生物工程学报, 2020, 36(3):455-470.
[4]	TANG R, LAN P, DING C, et al. A new perspective on the toxicity of arsenic-contaminated soil: Tandem mass tag proteomics and metabolomics in earthworms[J]. Journal of hazardous materials, 2020,398:122825.
[5]	RONALD S O, JOHN F S. The ecology of arsenic[J]. Science, 2003,300:939-944.
[6]	WANG Y, WU Y, CAVANAGH J, et al. Toxicity of arsenite to earthworms and subsequent effects on soil properties[J]. Soil biology and biochemistry, 2018,117,36-47.
[7]	HU L, FAN H, WU D, et al. Effects of selenium on antioxidant enzyme activity and bioaccessibility of arsenic in arsenic-stressed radish[J]. Ecotoxicology and environmental safety, 2020,200:110768.
[8]	SUN H J, RATHINASABAPATHI B, WU B, et al. Arsenic and selenium toxicity and their interactive effects in humans[J]. Environment International, 2014,69:148-158.
[9]	RAHMAN M M, USON-LOPEZ R A, SIKDER M T, et al. Ameliorative effects of selenium on arsenic-induced cytotoxicity in PC12cells via modulating autophagy/apoptosis[J]. Chemosphere, 2018,196:453-466.
[10]	岳士忠, 张慧琦, 黄财德, 等. 不同基质及硒添加量对蚯蚓生长、繁殖和富硒能力的影响[J]. 应用与环境生物学报, 2019, 25(4):885-891.
[11]	岳士忠. 赤子爱胜蚓对硒的富集转化及其活性成分生物功能研究[D]. 北京: 中国农业大学, 2019.
[12]	OECD. Test No.317: Bioaccumulation in terrestrial oligochaetes[S]. 2010.
[13]	YUE S Z, HUANG C D, WANG R P, et al. Selenium toxicity, bioaccumulation, and distribution in earthworms (Eisenia fetida) exposed to different substrates[J]. Ecotoxicology and environmental safety, 2021,217:112250.
[14]	RICHARDSON J B, GORRES J H, SIZMUR T. Synthesis of earthworm trace metal uptake and bioaccumulation data: Role of soil concentration, earthworm ecophysiology, and experimental design[J]. Environmental pollution, 2020,262:114126.
[15]	王亚利. 砷胁迫下蚯蚓的应激响应及对土壤理化性质的影响研究[D]. 上海: 上海交通大学, 2019.
[16]	BÁLINT B, BALOGH K, MÉZES M, et al. Differences in the effects of sodium selenate and sodium selenite on the mortality, reproduction, lipid peroxidation and glutathione redox status of Folsomia candida Willem 1902 (Collembola)[J]. European journal of soil biology, 2021,107:103361.
[17]	DA SILVA E, NAHMANI J, LAPIED E, et al. Toxicity of mercury to the earthworm Pontoscolex corethrurus in a tropical soil of French Guiana[J]. Applied soil ecology, 2016,104:79-84.
[18]	HEDĚNEC P, CAJTHAML T, PIŽL V, et al. Long-term effects of earthworms (Lumbricus rubellus Hoffmeister, 1843) on activity and composition of soil microbial community under laboratory conditions[J]. Applied soil ecology, 2020,150:103463.
[19]	CONDER J M, LANNO R P. Evaluation of surrogate measures of cadmium, lead, and zinc bioavailability to Eisenia fetida[J]. Chemosphere, 2000, 41(10):1659-1668.
[20]	ECIMOVIC S, VELKI M, VUKOVIC R, et al. Acute toxicity of selenate and selenite and their impacts on oxidative status, efflux pump activity, cellular and genetic parameters in earthworm Eisenia andrei[J]. Chemosphere, 2018,212:307-318.
[21]	王坤. 蚯蚓对长期重金属污染土壤的生态适应性及其解毒机制[D]. 北京: 中国农业大学, 2018.
[22]	BEAUMELLE L, GIMBERT F, HEDDE M, et al. Subcellular partitioning of metals in Aporrectodea caliginosa along a gradient of metal exposure in 31 field-contaminated soils[J]. Science of the total environment, 2015,520:136-145.
[23]	WANG K, QIAO Y H, ZHANG H Q, et al. Influence of metal-contamination on distribution in subcellular fractions of the earthworm (Metaphire californica) from Hunan Province, China[J]. Journal of environmental sciences, 2018,73:127-137.
[24]	BUSTOS V, MONDACA P, VERDEJO J, et al. Thresholds of arsenic toxicity to Eisenia fetida in field-collected agricultural soils exposed to copper mining activities in Chile[J]. Ecotoxicology and environmental safety, 2015,122:448-454.
[25]	LIEBEKE M, GARCIA-PEREZ I, ANDERSON C J, et al. Earthworms produce phytochelatins in response to arsenic[J]. PLoS one, 2013, 8(11):e81271.
[26]	DENG S, TANG H, DUAN H, et al. Mitochondrial bioenergetic, oxidative stress and burrowing responses in earthworm exposed to roxarsone in soil[J]. Ecotoxicology and environmental safety, 2021,228:113003.
[27]	WADGAONKAR S L, Y V, ESPOSITO G, et al. Environmental impact and bioremediation of seleniferous soils and sediments[J]. Critical reviews in biotechnology, 2018, 38(6):941-956. doi: 10.1080/07388551.2017.1420623 pmid: 29302994
[28]	RAHMAN M M, HOSSAIN K F B, BANIK S, et al. Selenium and zinc protections against metal-(loids)-induced toxicity and disease manifestations: A review[J]. Ecotoxicology and environmental safety, 2019,168:146-163.
[29]	ZWOLAK I. The role of selenium in arsenic and cadmium toxicity: an updated review of scientific literature[J]. Biological trace element research, 2020, 193(1):44-63. doi: 10.1007/s12011-019-01691-w pmid: 30877523
[30]	CHAUHAN R, AWASTHI S, SRIVASTAVA S, et al. Understanding selenium metabolism in plants and its role as a beneficial element[J]. Critical reviews in environmental science and technology, 2019, 49(21):1937-1958.
[31]	CABANERO A I, MADRID Y, CAMARA C. Mercury-selenium species ratio in representative fish samples and their bioaccessibility by an in vitro digestion method[J]. Biological trace element research, 2007, 119(3):195-211. pmid: 17916943
[32]	GAN X, HUANG J C, ZHANG M, et al. Remediation of selenium-contaminated soil through combined use of earthworm Eisenia fetida and organic materials[J]. Journal of hazardous materials, 2020,405:124212.
[33]	岳士忠, 王瑞萍, 曹赞霞, 等. 蚯蚓(Eisenia fetida)对硒的富集转化研究进展及其应用潜力[J]. 中国农业科技导报, 2021, 23(11):156-163.
[34]	邵秀清, 秦文友, 张梦, 等. 高效液相色谱串联质谱法检测蚯蚓体内硒代氨基酸[J]. 环境化学, 2019, 38(5):1057-1064.
[35]	XU Q, SHAO X, SHI Y, et al. Is selenium beneficial or detrimental to earthworm? Growth and metabolism responses of Eisenia fetida to Na₂SeO₃ exposure[J]. Science of the total environment, 2021, 807(Pt 2):150770.
[36]	SNIDER G W, RUGGLES E, KHAN N, et al. Selenocysteine confers resistance to inactivation by oxidation in thioredoxin reductase: Comparison of selenium and sulfur enzymes[J]. Biochemistry, 2013, 52(32):5472-5481. doi: 10.1021/bi400462j pmid: 23865454
[37]	CHAPMAN E E V, ROBINSON J, BERRY J, et al. Can a low-dose selenium (Se) additive reduce environmental risks of mercury (Hg) and arsenic (As) in old gold mine tailings?[J]. Water, air, & soil pollution, 2016, 227(6):1-17.
[38]	刘向辉, 戈峰, 徐张红, 等. 亚硒酸钠对蚯蚓的毒性及蚓体富硒作用的研究[J]. 应用与环境生物学报, 2001(5):457-460.
[39]	ŠTOLFA I, VELKI M, VUKOVIĆ R, et al. Effect of different forms of selenium on the plant-soil-earthworm system[J]. Journal of plant nutrition and soil science, 2017, 180(2):231-240.
[40]	FISCHER E, KOSZORUS L. Sublethal effects, accumulation capacities and elimination rates of As, Hg and Se in the manure worm, Eisenia fetida (Oligochaeta, Lumbricidae)[J]. Pedobiologia, 1992, 36(3):172-178.

处理	暴露时间/h	半致死浓度(LC₅₀)/(μg/cm²)	95%置信区间/ (μg/cm²)
As直接暴露	24	31.33	24.44~46.68
As直接暴露	48	12.30	10.46~21.76
Se滤纸适应— As暴露	24	30.20	27.91~50.20
Se滤纸适应— As暴露	48	15.85	12.22~23.21
Se0土壤适应— As暴露	24	30.20	27.91~50.20
Se0土壤适应— As暴露	48	20.42	15.77~28.73
Se6土壤适应— As暴露	24	34.67	33.14~58.12
Se6土壤适应— As暴露	48	21.88	18.43~31.26
Se12土壤适应— As暴露	24	35.48	33.84~55.82
Se12土壤适应— As暴露	48	18.62	14.07~25.96

处理	暴露时间/h	半致死浓度(LC₅₀)/(μg/cm²)	95%置信区间/ (μg/cm²)
As直接暴露	24	31.33	24.44~46.68
As直接暴露	48	12.30	10.46~21.76
Se滤纸适应— As暴露	24	30.20	27.91~50.20
Se滤纸适应— As暴露	48	15.85	12.22~23.21
Se0土壤适应— As暴露	24	30.20	27.91~50.20
Se0土壤适应— As暴露	48	20.42	15.77~28.73
Se6土壤适应— As暴露	24	34.67	33.14~58.12
Se6土壤适应— As暴露	48	21.88	18.43~31.26
Se12土壤适应— As暴露	24	35.48	33.84~55.82
Se12土壤适应— As暴露	48	18.62	14.07~25.96