Nitrogen-Fixing Anabaena sp. Mediated As(Ⅲ) Oxidation and Its Response to Ammonium Input
-
摘要: 铵氮在砷的生物地球化学循环过程中发挥着重要作用,但铵氮输入对藻类介导的As(Ⅲ)生物氧化机理尚不清楚.以固氮蓝藻鱼腥藻(Anabaena sp.)为研究对象,通过室内模拟实验,研究在不同浓度As(Ⅲ)条件下,鱼腥藻对As(Ⅲ)的毒性响应和氧化作用,并研究了外源铵氮输入对鱼腥藻的生长以及氧化As(Ⅲ)的影响.结果表明,鱼腥藻的半抑制浓度(IC50)值为15.59 mg/L,当As(Ⅲ)的浓度为0.1 mg/L、1 mg/L和10 mg/L时,分别在1 d、2 d和7 d内被完全氧化为As(Ⅴ),并且随着As(Ⅲ)浓度增加,鱼腥藻的固氮作用增强.NH4+浓度在234 mg/L以内时,对鱼腥藻(Anabaena sp.)的生长有促进作用,随着NH4+浓度从0 mg/L增加至1 mg/L、45 mg/L和234 mg/L,1 mg/L As(Ⅲ)分别在48 h、36 h、24 h和12 h被完全氧化.随着NH4+浓度增加,鱼腥藻对砷的吸附量增加,As(Ⅲ)的氧化加速.研究结果有助于阐释天然水体中铵氮在砷生物转化过程中的作用.Abstract: Ammonium plays an important role in the biogeochemical cycle of arsenic, but the mechanism of ammonium input on algae-mediated As(Ⅲ) bio-oxidation remains unexplored. The arsenic-resistant cyanobacteria Anabaena sp. was used in this study. Through laboratory simulation experiments, the toxicity, oxidation of different As(Ⅲ)concentrations mediated by Anabaena sp. was investigated. The influences of the input of exogenous ammonium on the growth of Anabaena sp. and the oxidation of As(Ⅲ) were also explored. The results show that the IC50 value of Anabaena sp. was 15.59 mg/L, and 0.1 mg/L, 1 mg/L and 10 mg/L As(Ⅲ) were completely oxidized to As(Ⅴ) within 1 d, 2 d and 7 d, respectively, after inoculating Anabaena sp., With the concentration of As(Ⅲ) increased, the nitrogen fixation effect of Anabaena sp. is enhanced. Furthermore, the growth of Anabaena sp. was promoted within 234 mg/L NH4+. With the increase of NH4+ concentration from 0 mg/L to 1 mg/L, 45 mg/L and 234 mg/L, 1 mg/L As(Ⅲ) was completely oxidized at 48 h, 36 h, 24 h and 12 h, respectively, as the concentration of NH4+ increases, the adsorption of Anabaena sp. to arsenic increases, and the oxidation of As(Ⅲ) accelerates. The research results help to interpret the role of ammonium nitrogen in the process of arsenic biotransformation in natural waters.
-
Key words:
- anabaena sp /
- arsenite /
- ammonium /
- toxicity /
- oxidation /
- adsorption /
- geochemistry
-
图 1 不同浓度As(Ⅲ)对鱼腥藻生长的影响(*表示不同As(Ⅲ)浓度处理组中鱼腥藻在第10 d的生长与对照组相比存在显著差异,p < 0.05)
Fig. 1. The effect of different As(Ⅲ) concentrations on the growth of Anabaena sp. (*Indicates that there is a significant difference in the growth of Anabaena sp. on the 10 d in the treatments with different As(Ⅲ) concentrations compared with the control group, p < 0.05)
图 2 不同浓度As(Ⅲ)对鱼腥藻的叶绿素a和类胡萝卜素合成的影响(*表示不同As(Ⅲ)浓度处理组中鱼腥藻在第10 d的色素合成与对照组相比存在显著差异,p < 0.05)
Fig. 2. The effect of different As(Ⅲ) concentrations on the chlorophyll a and carotenoids of Anabaena sp. (*Indicates that the pigments synthesis of Anabaena sp. on the 10 d in the treatment groups with different As(Ⅲ) concentrations was significantly different from that in the control group, p < 0.05)
表 1 不同NH4+浓度条件下准一级和准二级动力学方程的动力学参数
Table 1. Kinetic parameters obtained from pseudo-first-order and pseudo-second-order under different NH4+ concentrations
准一级动力学 准二级动力学 NH4+浓度(mg/L) k1(h‒1) R2 k2(g/μg·h) R2 0 0.106 0.998 2.027×10‒4 0.997 234 0.545 0.984 4.103×10‒4 0.995 -
Awoyemi, O. M., Subbiah, S., Velazquez, A., et al., 2020. Nitrate-N-Mediated Toxicological Responses of Scenedesmus Acutus and Daphnia Pulex to Cadmium, Arsenic and Their Binary Mixture (Cd/Asmix) at Environmentally Relevant Concentrations. Journal of Hazardous Materials, 400: 123189. https://doi.org/10.1016/j.jhazmat.2020.123189 Bahar, M. M., Megharaj, M., Naidu, R., 2013. Toxicity, Transformation and Accumulation of Inorganic Arsenic Species in a Microalga Scenedesmus sp. Isolated from Soil. Journal of Applied Phycology, 25(3): 913-917. https://doi.org/10.1007/s10811-012-9923-0 Berman-Frank, I., Lundgren, P., Falkowski, P., 2003. Nitrogen Fixation and Photosynthetic Oxygen Evolution in Cyanobacteria. Research in Microbiology, 154(3): 157-164. https://doi.org/10.1016/S0923-2508(03)00029-9 Böhme, H., 1998. Regulation of Nitrogen Fixation in Heterocyst-Forming Cyanobacteria. Trends in Plant Science, 3(9): 346-351. https://doi.org/10.1016/s1360-1385(98)01290-4 Chakraborty, A., Aziz Chowdhury, A., Bhakat, K., et al., 2019. Elevated Level of Arsenic Negatively Influences nifH Gene Expression of Isolated Soil Bacteria in Culture Condition as Well as Soil System. Environmental Geochemistry and Health, 41(5): 1953-1966. https://doi.org/10.1007/s10653-019-00261-2 Che, F. F., Du, M. M., Yan, C. Z., 2018. Arsenate Biotransformation by Microcystis Aeruginosa under Different Nitrogen and Phosphorus Levels. Journal of Environmental Sciences (China), 66: 41-49. https://doi.org/10.1016/j.jes.2017.05.041 Collos, Y., Harrison, P. J., 2014. Acclimation and Toxicity of High Ammonium Concentrations to Unicellular Algae. Marine Pollution Bulletin, 80(1/2): 8-23. https://doi.org/10.1016/j.marpolbul.2014.01.006 Dawodu, M. O., Akpomie, K. G., 2016. Evaluating the Potential of a Nigerian Soil as an Adsorbent for Tartrazine Dye: Isotherm, Kinetic and Thermodynamic Studies. Alexandria Engineering Journal, 55(4): 3211-3218. https://doi.org/10.1016/j.aej.2016.08.008 Fang, J. H., Xie, Z. M., Wang, J., et al., 2021. Bacterially Mediated Release and Mobilization of As/Fe Coupled to Nitrate Reduction in a Sediment Environment. Ecotoxicology and Environmental Safety, 208: 111478. https://doi.org/10.1016/j.ecoenv.2020.111478 Hussain, M. M., Wang, J. X., Bibi, I., et al., 2021. Arsenic Speciation and Biotransformation Pathways in the Aquatic Ecosystem: The Significance of Algae. Journal of Hazardous Materials, 403: 124027. https://doi.org/10.1016/j.jhazmat.2020.124027 Jana, A., Bhattacharya, P., Swarnakar, S., et al., 2015. Anabaena sp. Mediated Bio-Oxidation of Arsenite to Arsenate in Synthetic Arsenic (Ⅲ) Solution: Process Optimization by Response Surface Methodology. Chemosphere, 138: 682-690. https://doi.org/10.1016/j.chemosphere.2015.07.055 Jiamali, J., Maimaiti, G., Tumier, A., 2019. Study on Characteristics of Tolerance and Absorption of Four Heavy Metals by Three Photobionts. Acta Botanica Boreali-Occidentalia Sinica, 39(7): 1230-1240 (in Chinese with English abstract). Kumar, A., Bera, S., 2020. Revisiting Nitrogen Utilization in Algae: A Review on the Process of Regulation and Assimilation. Bioresource Technology Reports, 12: 100584. https://doi.org/10.1016/j.biteb.2020.100584 Levy, J. L., Stauber, J. L., Adams, M. S., et al., 2005. Toxicity, Biotransformation, and Mode of Action of Arsenic in Two Freshwater Microalgae (Chlorella sp. and Monoraphidium Arcuatum). Environmental Toxicology and Chemistry, 24(10): 2630-2639. https://doi.org/10.1897/04-580r.1 Li, X. T., Li, W., Zhai, J., et al., 2019. Effect of Ammonium Nitrogen on Microalgal Growth, Biochemical Composition and Photosynthetic Performance in Mixotrophic Cultivation. Bioresource Technology, 273: 368-376. https://doi.org/10.1016/j.biortech.2018.11.042 Lichtenthaler, H. K., 1987. Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods in Enzymology. Elsevier, Amsterdam, 350-382. https://doi.org/10.1016/0076-6879(87)48036-1 Liu, J. Q., Sun, Z. Q., Lavoie, M., et al., 2015. Ammonium Reduces Chromium Toxicity in the Freshwater Alga Chlorella Vulgaris. Applied Microbiology and Biotechnology, 99(7): 3249-3258. https://doi.org/10.1007/s00253-014-6218-1 Ministry of Environmental Protection of the People's Republic of China, 2010. Water Quality Determination of Ammonia Nitrogen Determination by Nessler's Reagent Dectrophotometry (HJ 535-2009). China Environmental Science Press, Beijing (in Chinese). Miyashita, S. I., Murota, C., Kondo, K., et al., 2016. Arsenic Metabolism in Cyanobacteria. Environmental Chemistry, 13(4): 577. https://doi.org/10.1071/en15071 Ospina-Betancourth, C., Acharya, K., Sanabria, J., et al., 2021. Low Inhibitory Effect of Ammonia on the Nitrogen-Fixing Activity of a Sludge Enriched with Nitrogen-Fixing Bacteria. Bioresource Technology Reports, 14: 100655. https://doi.org/10.1016/j.biteb.2021.100655 Patel, A., Tiwari, S., Prasad, S. M., 2018. Toxicity Assessment of Arsenate and Arsenite on Growth, Chlorophyll a Fluorescence and Antioxidant Machinery in Nostoc Muscorum. Ecotoxicology and Environmental Safety, 157: 369-379. https://doi.org/10.1016/j.ecoenv.2018.03.056 Patel, A., Tiwari, S., Prasad, S. M., 2021. Effect of Time Interval on Arsenic Toxicity to Paddy Field Cyanobacteria as Evident by Nitrogen Metabolism, Biochemical Constituent, and Exopolysaccharide Content. Biological Trace Element Research, 199(5): 2031-2046. https://doi.org/10.1007/s12011-020-02289-3 Pokhrel, D., Viraraghavan, T., 2008. Arsenic Removal from an Aqueous Solution by Modified A. Niger Biomass: Batch Kinetic and Isotherm Studies. Journal of Hazardous Materials, 150(3): 818-825. https://doi.org/10.1016/j.jhazmat.2007.05.041 Qu, G. Y., Li, M. J., Zheng, J. H., et al., 2022. The Promoting Effect and Mechanism of Nitrogen Conversion in the Sediments of Polluted Lake on the Degradation of Organic Pollutants. Earth Science, 47(2): 652-661 (in Chinese with English abstract). Ruan, Y. H., Fang, X., Guo, T. Y., et al., 2022. Metabolic Reprogramming in the Arsenic Carcinogenesis. Ecotoxicology and Environmental Safety, 229: 113098. https://doi.org/10.1016/j.ecoenv.2021.113098 Tabaraki, R., Heidarizadi, E., 2018. Simultaneous Biosorption of Arsenic (Ⅲ) and Arsenic (Ⅴ): Application of Multiple Response Optimizations. Ecotoxicology and Environmental Safety, 166: 35-41. https://doi.org/10.1016/j.ecoenv.2018.09.063 Wang, J., Xie, Z. M., Wang, J., et al., 2021. Influence of Bioreduction of Arsenic-Bearing Goethite by Bacteria under Sulfur Mediation on Migration and Transformation of Arsenic. Journal of Earth Science, 46(2): 642-651 (in Chinese with English abstract). Wang, N. X., Huang, B., Xu, S., et al., 2014. Effects of Nitrogen and Phosphorus on Arsenite Accumulation, Oxidation, and Toxicity in Chlamydomonas Reinhardtii. Aquatic Toxicology, 157: 167-174. https://doi.org/10.1016/j.aquatox.2014.10.012 Wang, N. X., Li, Y., Deng, X. H., et al., 2013a. Toxicity and Bioaccumulation Kinetics of Arsenate in Two Freshwater Green Algae under Different Phosphate Regimes. Water Research, 47(7): 2497-2506. https://doi.org/10.1016/j.watres.2013.02.034 Wang, Z. H., Luo, Z. X., Yan, C. Z., 2013b. Accumulation, Transformation, and Release of Inorganic Arsenic by the Freshwater Cyanobacterium Microcystis Aeruginosa. Environmental Science and Pollution Research, 20(10): 7286-7295. https://doi.org/10.1007/s11356-013-1741-7 Wang, S. Z., Zhang, D. Y., Pan, X. L., 2012. Effects of Arsenic on Growth and Photosystem Ⅱ (PSII) Activity of Microcystis Aeruginosa. Ecotoxicology and Environmental Safety, 84: 104-111. https://doi.org/10.1016/j.ecoenv.2012.06.028 Wang, Y., Wang, S., Xu, P. P., et al., 2015. Review of Arsenic Speciation, Toxicity and Metabolism in Microalgae. Reviews in Environmental Science and Bio/Technology, 14(3): 427-451. https://doi.org/10.1007/s11157-015-9371-9 Wang, Z. H., Fu, Y., Wang, L. L., 2021. Abiotic Oxidation of Arsenite in Natural and Engineered Systems: Mechanisms and Related Controversies over the Last Two Decades (1999-2020). Journal of Hazardous Materials, 414: 125488. https://doi.org/10.1016/j.jhazmat.2021.125488 Xue, X. M., Yan, Y., Xiong, C., et al., 2017. Arsenic Biotransformation by a Cyanobacterium Nostoc sp. PCC 7120. Environmental Pollution, 228: 111-117. https://doi.org/10.1016/j.envpol.2017.05.005 Zhang, S. Y., Rensing, C., Zhu, Y. G., 2014. Cyanobacteria-Mediated Arsenic Redox Dynamics is Regulated by Phosphate in Aquatic Environments. Environmental Science & Technology, 48(2): 994-1000. https://doi.org/10.1021/es403836g Zhao, X. C., Tan, X. B., Yang, L. B., et al., 2019. Cultivation of Chlorella Pyrenoidosa in Anaerobic Wastewater: The Coupled Effects of Ammonium, Temperature and pH Conditions on Lipids Compositions. Bioresource Technology, 284: 90-97. https://doi.org/10.1016/j.biortech.2019.03.117 Zhao, X. X., Li, Y. L., Li, Y. W., et al., 2020. Effects of Increased Nitrogen Deposition and Anthropogenic Perturbation on Soil Respiration in a Semiarid Grassland. Transactions of the Chinese Society of Agricultural Engineering (Transactions of the CSAE), 36(15): 120-127 (in Chinese with English abstract). 吉米拉木·加马力, 古海尼沙·买买提, 艾尼瓦尔·吐米尔, 2019.3种地衣体内藻类对4种重金属离子的耐受能力及其吸附特性研究. 西北植物学报, 39(7): 1230-1240. https://www.cnki.com.cn/Article/CJFDTOTAL-DNYX201907012.htm 中华人民共和国环境保护部, 2010. 水质 氨氮的测定 纳氏试剂分光光度法: HJ 535—2009. 北京: 中国环境科学出版社. 屈国颖, 李民敬, 郑剑涵, 等, 2022. 受污染湖泊沉积物中氮素转化对有机污染物降解的促进效应与机制. 地球科学, 47(2): 652-661. doi: 10.3799/dqkx.2021.095 王晶, 谢作明, 王佳, 等, 2021. 硫介导细菌还原载砷铁矿对砷迁移转化的影响. 地球科学, 46(2): 642-651. doi: 10.3799/dqkx.2020.054 赵欣鑫, 李玉霖, 李有文, 等, 2020. 氮沉降增加和人类干扰对半干旱草地土壤呼吸的影响. 农业工程学报, 36(15): 120-127. https://www.cnki.com.cn/Article/CJFDTOTAL-NYGU202015016.htm -