Roles of cyanobacterial-derived dissolved organic matter in mediating biodegradation of 17β-estradiol in water column
HUA Ke1, JIANG Yu2, WU Yuan-qiang1, YANG Nan1, LIU Xin1
1. College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China; 2. Jiangsu Provincial Ecological Assessment Center (Jiangsu Provincial Management Center for Emissions Registration and Exchange), Nanjing 210036, China
Abstract:The effects of cyanobacterial-derived dissolved organic matter (COM) and its microbial processing on the biodegradation of 17β-estradiol (E2) in lake water column were investigated in this study. Through the simulated microbial ageing within a four-stage plug-flow bioreactor, five COM fractions with a gradient of decreasing bioreactivity were separated: S0 (78%) > S1 (67%) > S0 (36%) > S0 (13%) > S0 (1%). Within the 60 hours of batch incubation at dark, the addition of COM fractions at 8mgC/L exhibited strong acceleration on E2biodegradation, increasing the first-order kinetic rate with the order of S0 > S4 > S3 > S1 > S2. Microbial analysis further showed that the highly labile compounds in COM not only promoted the bacterial growth but also maintained the diverse microbial community in the S0-amended group. In comparsion, the bacterial concentration and E2biodegradation rate in the S1- and S2-amended groups was remarkably lower, meaning that the semilabile and recalcitrant compounds were unable to serve as effective carbon sources. However, the enriched aromatic, humic structure in the S3- and S4-amended groups significantly increased the biomass-normalized E2biodegradation rate, possibly due to the selection of potentially E2-degrading bacteria and the activation of catabolic enzymes under carbon-limited conditions. The environmental behavior and fate of estrogens in eutrophic waters are closely related to the bioreactivity of COM.
化柯, 蒋豫, 吴元强, 杨楠, 刘新. 藻源可溶有机质对17β-雌二醇生物降解的影响[J]. 中国环境科学, 2022, 42(4): 1829-1836.
HUA Ke, JIANG Yu, WU Yuan-qiang, YANG Nan, LIU Xin. Roles of cyanobacterial-derived dissolved organic matter in mediating biodegradation of 17β-estradiol in water column. CHINA ENVIRONMENTAL SCIENCECE, 2022, 42(4): 1829-1836.
Zhang C, Li Y, Wang C, et al. Occurrence of endocrine disrupting compounds in aqueous environment and their bacterial degradation:A review[J]. Critical Reviews in Environmental Science and Technology, 2016,46(1):1-59.
[2]
Martinz R, Herrero-Nogareda L, Van A M, et al. Morphometric signatures of exposure to endocrine disrupting chemicals in zebrafish eleutheroembryos[J]. Aquatic Toxicology, 2019,214:105232.
[3]
Van Den Belt K, Berckmans P, Vangenechten C, et al. Comparative study on the in vitro in vivo estrogenic potencies of 17beta-estradiol, estrone, 17alpha-ethynylestradiol and nonylphenol[J]. Aquatic Toxicology, 2004,66(2):183-195.
[4]
Xie Z, Lu G, Liu J, et al. Occurrence, bioaccumulation, and trophic magnification of pharmaceutically active compounds in Taihu Lake, China[J]. Chemosphere, 2015,138:140-147.
[5]
Huang B, Wang B, Ren D, et al. Occurrence, removal and bioaccumulation of steroid estrogens in Dianchi Lake catchment, China[J]. Environment International, 2013,59:262-273.
[6]
宋晓明,杨悦锁,温玉娟,等.雌激素在地下环境中的归宿及其生态调控[J]. 中国环境科学, 2016,36(9):2828-2840. Song X M, Yang Y S, Wen Y J, et al. Fate and ecological regulation of steroidal estrogens in subsurface environment[J]. China Environmental Science, 2016,36(9):2828-2840.
[7]
师博颖,王智源,刘俊杰,等.长江江苏段饮用水源地3种雌激素污染特征[J]. 环境科学学报, 2018,38(3):875-883. Shi B Y, Wang Z Y, Liu J J, et al. Pollution characteristics of three estrogens in drinking water sources in Jiangsu reach of the Yangtze River[J]. Acta Scientiae Circumstantiae, 2018,38(3):875-883.
[8]
Zhou L J, Zhang B B, Zhao Y G, et al. Occurrence, spatiotemporal distribution, and ecological risks of steroids in a large shallow Chinese lake, Lake Taihu[J]. Science of the Total Environment, 2016,557:68-79.
[9]
Wear E K, Carlson C A, James A K, et al. Synchronous shifts in dissolved organic carbon bioavailability and bacterial community responses over the course of an upwelling-driven phytoplankton bloom[J]. Limnology and Oceanography, 2015,60(2):657-677.
[10]
Zhang Y L, Liu X H, Wang M Z, et al. Compositional differences of chromophoric dissolved organic matter derived from phytoplankton and macrophytes[J]. Organic Geochemistry, 2013,55:26-37.
[11]
Cory R M, Davis T W, Dick G J, et al. Seasonal dynamics in dissolved organic matter, hydrogen peroxide, and cyanobacterial blooms in lake erie[J]. Frontiers in Marine Science, 2016,3:54.
[12]
Hoikkala L, Tammert H, Lignell R, et al. Autochthonous dissolved organic matter drives bacterial community composition during a bloom of filamentous cyanobacteria[J]. Frontiers in Marine Science, 2016,3:111.
[13]
Lee J H, Zhou J L, Kim S D. Effects of biodegradation and sorption by humic acid on the estrogenicity of 17beta-estradiol[J]. Chemosphere, 2011,85(8):1383-1389.
[14]
吕伟伟,姚昕,张保华.太湖北部湖区春、冬季节天然有机质的荧光特征及环境意义[J]. 环境科学, 2018,39(8):3601-3613. Lu W W, Yao X, Zhang B H. Fluorescence characteristics and environmental significance of organic matter in the northern part of Lake Taihu in spring and winter[J]. Environmental Science, 2018,39(8):3601-3613.
[15]
Ma L, Yates S R. Dissolved organic matter and estrogen interactions regulate estrogen removal in the aqueous environment:A review[J]. Science of the Total Environment, 2018,640:529-542.
[16]
Tan D T, Temme H R, Arnold W A, et al. Estrone degradation:does organic matter (quality), matter?[J]. Environmental Science and Technology, 2015,49(1):498-503.
[17]
Lim M H, Snyder S A, Sedlak D L. Use of biodegradable dissolved organic carbon (BDOC) to assess the potential for transformation of wastewater-derived contaminants in surface waters[J]. Water Research, 2008,42(12):2943-2952.
[18]
Muller M, Rabenoelina F, Balaguer P, et al. Chemical and biological analysis of endocrine-disrupting hormones and estrogenic activity in an advanced sewage treatment plant[J]. Environmental Toxicology and Chemistry, 2008,27(8):1649-1658.
[19]
Shi L, Huang Y, Lu Y, et al. Stocks and dynamics of particulate and dissolved organic matter in a large, shallow eutrophic lake (Taihu, China) with dense cyanobacterial blooms[J]. Journal of Oceanology and Limnology, 2018,36(3):738-749.
[20]
Wang Y, Wang Q, Hu L, et al. Occurrence of estrogens in water, sediment and biota and their ecological risk in Northern Taihu Lake in China[J]. Environmental Geochemistry and Health, 2015,37(1):147- 156.
[21]
Han C, Geng J, Xie X, et al. Determination of phosphite in a eutrophic freshwater lake by suppressed conductivity ion chromatography[J]. Environmental Science and Technology, 2012,46(19):10667-10674.
[22]
Bai L, Cao C, Wang C, et al. Toward quantitative understanding of the bioavailability of dissolved organic matter in freshwater lake during cyanobacteria blooming[J]. Environmental Science and Technology, 2017,51(11):6018-6026.
[23]
Westrich J T, Berner R A. The role of sedimentary organic matter in bacterial sulfate reduction:The G model tested[J]. Limnology and Oceanography, 1984,29(2):236-249.
[24]
Matilainen A, Gjessing E T, Lahtinen T, et al. An overview of the methods used in the characterisation of natural organic matter (NOM) in relation to drinking water treatment[J]. Chemosphere, 2011,83(11):1431-1442.
[25]
Murphy K R, Stedmon C A, Graeber D, et al. Fluorescence spectroscopy and multi-way techniques. PARAFAC[J]. Analytical Methods, 2013,5(23):6557-6566.
[26]
Danhiez F P, Vantrepotte V, Cauvin A, et al. Optical properties of chromophoric dissolved organic matter during a phytoplankton bloom. Implication for DOC estimates from CDOM absorption[J]. Limnology and Oceanography, 2017,62(4):1409-1425.
[27]
Helms J R, Stubbins A, Ritchie J D, et al. Absorption spectral slopes and slope ratios as indicators of molecular weight, source, and photobleaching of chromophoric dissolved organic matter[J]. Limnology and Oceanography, 2008,53(3):955-969.
[28]
Phong D D, Hur J. Using two-dimensional correlation size exclusion chromatography (2D-CoSEC) and EEM-PARAFAC to explore the heterogeneous adsorption behavior of humic substances on nanoparticles with respect to molecular sizes[J]. Environmental Science and Technology, 2018,52(2):427-435.
[29]
Weishaar J L, Aiken G R, Bergamaschi B A, et al. Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon[J]. Environmental Science and Technology, 2003,37(20):4702-4708.
[30]
Fellman J B, Hood E, Spencer R G M. Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems:A review[J]. Limnology and Oceanography, 2010,55(6):2452-2462.
[31]
Banihashemi B, Droste R L. Sorption-desorption and biosorption of bisphenol A, triclosan, and 17alpha-ethinylestradiol to sewage sludge[J]. Science of the Total Environment, 2014,487:813-821.
[32]
Rentz J A, Alvarez P J J, Schnoor J L. Repression of pseudomonas putida phenanthrene-degrading activity by plant root extracts and exudates[J]. Environmental Microbiology, 2004,6(6):574-583.
[33]
Ren Y X, Nakano K, Nomura M, et al. Effects of bacterial activity on estrogen removal in nitrifying activated sludge[J]. Water Research, 2007,41(14):3089-3096.
[34]
Horemans B, Vandermaesen J, Breugelmans P, et al. The quantity and quality of dissolved organic matter as supplementary carbon source impacts the pesticide-degrading activity of a triple-species bacterial biofilm[J]. Applied Microbiology and Biotechnology, 2014,98(2):931-943.
[35]
Egli T. How to live at very low substrate concentration[J]. Water Research, 2010,44(17):4826-4837.
[36]
Muller M, Patureau D, Godon J-J, et al. Molecular and kinetic characterization of mixed cultures degrading natural and synthetic estrogens[J]. Applied Microbiology and Biotechnology, 2010,85(3):691-701.
[37]
Li Z, Nandakumar R, Madayiputhiya N, et al. Proteomic analysis of 17beta-estradiol degradation by stenotrophomonas maltophilia[J]. Environmental Science and Technology, 2012,46(11):5947-5955.