Effect of intestinal iron reduction process on reactive oxygen species formation in earthworm
ZHANG Ying1,2, GAO Ze-ping1,2, WANG Xu1, LI Shun-shun1,2, HUANG Tao1,2, ZHOU Guo-wei1,2
1. College of Resource and Environmental Engineering, Anhui University, Hefei 230601, China; 2. Anhui Provincial Key Laboratory of Wetland Ecological Protection and Restoration, Anhui University, Hefei 230601, China
Abstract:Earthworm (Pheretima guillelmi) was selected as the model animal. Combination of in situ determination, high-throughput sequencing and biochemical analysis, the results indicated that the production of Fe(Ⅱ) was highest in the glucose treatment group and lowest in the amino acid setup. During the iron(Ⅲ) reduction process, the content of surface-adsorbed Fe(Ⅱ) was the highest, ranging from 0.6 to 24.38mmol/L;whereas the content of ionic Fe(Ⅱ) was the lowest, ranging from 0.02 to 2.21mmol/L. The community structure of iron(Ⅲ)-reducing bacteria was significantly influenced by the type of organic matter,and the dominant iron(Ⅲ)-reducing bacteria in different treatment groups were diverse. Additionally, the iron(Ⅲ) reduction process was accompanied by the generation of reactive oxygen species (ROS). The content of hydrogen peroxide (H2O2) was the highest, ranging from 0.32 to 0.73mmol/L, and be show a significant positive correlation with the contents of ionic Fe2+, surface-adsorbed Fe(Ⅱ), and high-crystalline iron, while exhibiting a significant negative correlation with the content of iron in organic complex state. Hydroxyl radical (•OH) has a significant positive correlation with ionic Fe2+, adsorbed Fe(Ⅱ), and high-crystalline iron. Superoxide anion (O2•−) has a significant positive correlation with low-crystalline iron and a significant negative correlation with adsorbed Fe(Ⅱ) and high-crystalline iron. The research results provide a new perspective for understanding the role of earthworms gut microbiota in soil iron cycling and ROS formation, which can be applied for pollutant control and degradation.
张颖, 高泽萍, 王旭, 李顺顺, 黄涛, 周国伟. 蚯蚓肠道铁还原过程对活性氧形成的影响[J]. 中国环境科学, 2025, 45(4): 2053-2062.
ZHANG Ying, GAO Ze-ping, WANG Xu, LI Shun-shun, HUANG Tao, ZHOU Guo-wei. Effect of intestinal iron reduction process on reactive oxygen species formation in earthworm. CHINA ENVIRONMENTAL SCIENCECE, 2025, 45(4): 2053-2062.
[1] 王洪涛,丁晶,邵元虎,等.4种蚯蚓肠道微生物对砷毒性的响应差异研究[J].生态学报, 2022,42(1):379-389. Wang H T, Ding J, Shao Y H, et al. Comparative study on the responses of gut microbiota of four species of earthworms to arsenic toxicity[J]. Acta Ecologica Sinica, 2022,42(1):379-389. [2] 晁会珍,孙明明,朱国繁,等.蚯蚓肠道细菌生态功能及毒理学研究进展[J].生态毒理学报, 2020,15(5):35-48. Chao H Z, Sun M M, Zhu G F, et al. Ecological functioning of the earthworm intestinal bacteria and their role in toxicology research[J]. Asian Journal of Ecotoxicology, 2020,15(5):35-48. [3] 宋旭昕,刘同旭.土壤铁矿物形态转化影响有机碳固定研究进展[J].生态学报, 2021,41(20)7928-7938. Song X X, Liu T X. Effects of soil iron mineral transformation on organic carbon sequestration:a review[J]. Acta Ecologica Sinica, 2021,41(20)7928-7938. [4] Drake H L, Horn M A. As the worm turns:the earthworm gut as a transient habitat for soil microbial biomes[J]. Annual Review of Microbiology, 2007,61(1):169-189. [5] Zhou G W, Yang X R, Sun A Q, et al. Mobile incubator for iron (Ⅲ) reduction in the gut of the soil-feeding earthworm Pheretima guillelmi and interaction with denitrification[J]. Environmental Science& Technology, 2019,53(8):4215-4223. [6] Schaefer CE, Ho P, Berns E, et al. Mechanisms for abiotic dechlorination of trichloroethene by ferrous minerals under oxic and anoxic conditions in natural sediments[J]. Environmental Science& Technology, 2018,52(23):13747-13755. [7] Liao P, Yu K, Lu Y, et al. Extensive dark production of hydroxyl radicals from oxygenation of polluted river sediments[J]. Chemical Engineering Journal, 2019,368:700-709. [8] Fang G, Liu C, Wang Y, et al. Photogeneration of reactive oxygen species from biochar suspension for diethyl phthalate degradation[J]. Applied Catalysis B:Environmental, 2017,214:34-45. [9] Yuan C, Chin Y P, Weavers L K. Photochemical acetochlor degradation induced by hydroxyl radical in Fe-amended wetland waters:impact of pH and dissolved organic matter[J]. Water Research, 2018,132:52-60. [10] Zhong Y, Liang X, Zhong Y, et al. Heterogeneous UV/Fenton degradation of TBBPA catalyzed by titanomagnetite:catalyst characterization, performance and degradation products[J]. Water Research, 2012,46(15):4633-4644. [11] Pignatello JJ, Oliveros E, MacKay A. Advanced oxidation processes for organic contaminant destruction based on the Fenton reaction and related chemistry[J]. Critical Reviews in Environmental Science and Technology, 2006,36(1):1-84. [12] Tong M, Yuan S, Ma S, et al. Production of abundant hydroxyl radicals from oxygenation of subsurface sediments[J]. Environmental Science& Technology, 2016,50:214−221. [13] Hester E T, Gooseff M N. Moving beyond the banks:hyporheic restoration is fundamental to restoring ecological services and functions of streams[J]. Environmental Science& Technology, 2010, 44:1521−1525. [14] Beck M, Dellwig O, Schnetger B, et al. Cycling of trace metals (Mn, Fe, Mo, U, V, Cr) in deep pore waters of intertidal flat sediments[J]. Geochimica et Cosmochimica Acta, 2008,72(12):2822-2840. [15] Kumar A R, Riyazuddin P. Seasonal variation of redox species and redox potentials in shallow groundwater:a comparison of measured and calculated redox potentials[J]. Journal of Hydrology, 2012,444:187-198. [16] 鲁如坤.土壤农业化学分析方法[M].北京:中国农业科技出版社, 2000:106-109. Lu R K. Analytical methods of soil agricultural chemistry[M]. Beijing:China Agricultural Science and Technology Press, 2000:106-109. [17] 王亚婷.元素分析仪同时测定土壤中的全氮和总碳[J].城市地质, 2022,17(2):249-254. Wang Y T. Concurrent determination by elemental analyzer of total nitrogen and total carbon in soil samples[J]. Urban Geology, 2020, 17(2):249-254. [18] Wang H T, Zhu D, Li G, et al. Effects of arsenic on gut microbiota and its biotransformation genes in earthworm Metaphire sieboldi [J]. Environmental Science& Technology, 2019,53(7):3841-3849. [19] Klueglein N, Kappler A. Abiotic oxidation of Fe (Ⅱ) by reactive nitrogen species in cultures of the nitrate-reducing Fe (Ⅱ) oxidizer Acidovorax sp. BoFeN1-questioning the existence of enzymatic Fe (Ⅱ) oxidation[J]. Geobiology, 2013,11(2):180-190. [20] Wang W, Huang D, Wang D, et al. Extensive production of hydroxyl radicals during oxygenation of anoxic paddy soils:Implications to imidacloprid degradation[J]. Chemosphere, 2022,286:131565. [21] Updegraff D M. Semimicro determination of cellulose inbiological materials[J]. Analytical Biochemistry, 1969,32(3):420-424. [22] 韩瑞霞,吕继涛,张淑贞.一种适用于复杂异相体系中羟基自由基定量检测的探针分子--香豆素[J].高等学校化学学报, 2018, 39(12):2658-2664. Han R X, Lv J T, Zhang S Z. Molecular probe for the determination of hydroxyl radicals in heterogeneous systems:coumarin[J]. Chemical Journal of Chinese Universities, 2018,39(12):2658-2664. [23] 王爱国,罗广华.植物的超氧物自由基与羟胺反应的定量关系[J].植物生理学通讯, 1990,(6):55-57. Wang A G, Luo G H. Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants[J]. Plant Physiology Communications, 1990,(6):55-57. [24] Bai Y, Mellage A, Cirpka O A, et al. AQDS and redox-active NOM enables microbial Fe (Ⅲ)-mineral reduction at cm-scales[J]. Environmental Science& Technology, 2020,54(7):4131-4139. [25] 赵隽隽.小分子有机酸与希瓦氏菌对针铁矿吸附态Cd的影响研究[D].西安:陕西科技大学, 2023. Zhao J J. Research on impact of adsorbed cadmium of goethite by low molecular weight organic acids couple with Shewanella Oneidensis MR-1[D]. Xi'an:Shaanxi University of Science& Technology, 2023. [26] 李远航.溶解性有机质-水铁矿-重金属三元体系对湿地土壤铜、铬环境行为的影响机制[D].南昌:南昌大学, 2022. Li Y H. Influence mechanism of ternary system with dissolved organic matter, ferrihydrite and heavy metal on the environmental behavior of copper and chromium in wetland soil[D]. Nanchang:Nanchang University, 2022. [27] Du H Y, Yu G H, Sun F S, et al. Iron minerals inhibit the growth of Pseudomonas brassicacearum J12via a free-radical mechanism:implications for soil carbon storage[J]. Biogeosciences, 2019,16(7):1433-1445. [28] Su C, Zhang M, Lin L, et al. Reduction of iron oxides and microbial community composition in iron-rich soils with different organic carbon as electron donors[J]. International Biodeterioration& Biodegradation, 2020,148:104881. [29] Lusk, Bradley. Thermophilic microbial electrochemical cells[D]. Phoenix:Arizona State University, 2015. [30] Nakata H M. Organic nutrients required for growth and sporulation of Bacillus cereus [J]. Journal of Bacteriology, 1964,88(5):1522-1524. [31] García-Balboa C, Cautivo D, Blázquez M L, et al. The influence of disimilatory Fe (Ⅲ) reducers on iron ore dissolution[J]. Advanced Materials Research, 2009,71:501-504. [32] Poehlein A, Berg A, Welsing G, et al. First Insights into the Genome Sequence of the Alkaliphilic Thermotolerant Bacterium Clostridium thermoalcaliphilum JW/YL23-2T [J]. Genome Announcements, 2017,5(20):10-128. [33] Lovley D R, Phillips E J. Requirement for a microbial consortium to completely oxidize glucose in Fe (Ⅲ)-reducing sediments[J]. Applied and Environmental Microbiology, 1989,55(12):3234-3236. [34] Horn M A, Ihssen J, Matthies C, et al. Dechloromonas denitrificans sp. nov., Flavobacterium denitrificans sp. nov., Paenibacillus anaericanus sp. nov. and Paenibacillus terrae strain MH72, N2O-producing bacteria isolated from the gut of the earthworm Aporrectodea caliginosa[J]. International Journal of Systematic and Evolutionary Microbiology, 2005,55(3):1255-1265. [35] 袁文杰.铁还原菌介导载砷混合铁氧化物矿物还原-砷释放动力学特征研究[D].北京:中国地质大学, 2020. Yuan W J. Iron-reducing bacteria mediated reduction of arsenic-bearing mixed iron oxide minerals and arsenic release[D]. Beijing:China University of Geosciences, 2020. [36] Wang X J, Chen X P, Kappler A, et al. Arsenic binding to iron (Ⅱ) minerals produced by An iron (Ⅲ)-Reducing Aeromonas strain isolated from paddy soil[J]. Environmental Toxicology and Chemistry:An International Journal, 2009,28(11):2255-2262. [37] 韦志琦.Fe (Ⅱ)催化氧化铁矿物晶相转变及其重金属固定效应[D].成都:电子科技大学, 2016. Wei Z Q. Iron oxide minerals phase transformation catalyzed by Fe (Ⅱ) and its effect on heavy metals fixation[D]. Chengdu:University of Electronic Science and Technology of China, 2016. [38] Zhang Y, Zhang N, Qian A, et al. Effect of C/Fe molar ratio on H2O2 and •OH production during oxygenation of Fe (Ⅱ)-humic acid coexisting systems[J]. Environmental Science& Technology, 2022, 56(18):13408-13418. [39] Tong M, Yuan S, Ma S, et al. Production of abundant hydroxyl radicals from oxygenation of subsurface sediments[J]. Environmental Science& Technology, 2016,50(1):214-221. [40] Xie W, Yuan S, Tong M, et al. Contaminant degradation by•OH during sediment oxygenation:dependence on Fe (Ⅱ) species[J]. Environmental Science& Technology, 2020,54(5):2975-2984. [41] Zhang N, Liu Y, Wan Z, et al. Dependence of Biotic and Abiotic H2O2 and •OH Production on the Redox Conditions and Compositions of Sediment during Oxygenation[J]. Environmental Science& Technology, 2024,58(8):3849-3857. [42] Sheng Y, Hu J, Kukkadapu R, et al. Inhibition of extracellular enzyme activity by reactive oxygen species upon oxygenation of reduced iron-bearing minerals[J]. Environmental Science& Technology, 2023, 57(8):3425-3433. [43] Liu X, Yuan S, Tong M, et al. Oxidation of trichloroethylene by the hydroxyl radicals produced from oxygenation of reduced nontronite[J]. Water Research, 2017,113:72-79. [44] 张怡.小分子有机酸调控土壤中羟基自由基降解多环芳烃的机制研究[D].南京:南京信息工程大学, 2024. Zhang Y. Mechanistic Investigation on the degradation of polycyclic aromatic hydrocarbons by hydroxyl radicals in soil regulated by small-molecule organic acids[D]. Nanjing:Nanjing University of Information Science& Technology, 2024. [45] Huang L, Zhu J, Xiong W, et al. Tumor-generated reactive oxygen species storm for high-performance ferroptosis therapy[J]. ACS nano, 2023,17(12):11492-11506.