The distribution characteristics of three types of diarrheal pathogens in the lakes of Wuhan city
DENG Min1,2, WANG Yu-ren1,2,3, LIU Wen-jing1,2,3, LI Lu2,3, SONG Kang2,3
1. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China; 2. Key Laboratory of Lake and Watershed Science for Water Security, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; 3. University of Chinese Academy of Sciences, Beijing 100049, China
Abstract：Field surveys were conducted in Wuhan city and its surrounding areas to assess the water quality of urban and agricultural lakes during winter and summer. Additionally, fluorescence quantitative PCR technology was employed to analyze the distribution patterns of three diarrheal pathogens. The results revealed that the average abundance of Escherichia coli uidA gene [(1.86±1.15)×109 copies/100mL] and the Shigella dysenteriae ipaH gene [(2.20±1.54)×105 copies/100mL] in urban lakes was approximately 2- and 2.7-times higher, respectively, compared to agricultural lakes (P<0.05). However, no significant regional difference was observed in the abundance of Salmonella spp. between urban and agricultural lakes. During the summer, the abundance of the E. coli uidA gene [(3.75±1.48)×109 copies/100mL] in lake water was significantly higher compared to the winter [(1.45±1.07)×109copies/100mL] (P<0.01). Conversely, no significant seasonal difference was observed in the abundance of Salmonella spp. and S. dysenteriae in the lake water. The abundance of E. coli, an indicator of fecal contamination, showed a significant positive correlation with the presence of S. dysenteriae ipaH gene (P<0.0001). However, no significant linear relationship was found between the abundance of the E. coli uidA gene and the presence of the Salmonella spp. dam gene (P>0.05). In the lake water, the abundance of the E. coli uidA gene and the S. dysenteriae ipaH gene showed significant positive correlations with chlorophyll-a, total phosphorus, and ammonium nitrogen. Overall, sewage discharge and surface runoff have led to nutrient enrichment and a significant increase in the abundance of pathogenic microorganisms in urban lakes. In summer, higher levels of suspended particles, predominantly composed of algae, promote the attachment and growth of pathogenic bacteria like E. coli. To accurately reflect pathogenic bacterial contamination in water bodies and control biological risks, it is necessary to increase the variety of pathogenic bacteria monitored in environmental water.
邓闵, 王昱人, 刘文晶, 李露, 宋康. 武汉市湖泊水体三种致腹泻病原菌的分布特征[J]. 中国环境科学, 2024, 44(10): 5875-5884.
DENG Min, WANG Yu-ren, LIU Wen-jing, LI Lu, SONG Kang. The distribution characteristics of three types of diarrheal pathogens in the lakes of Wuhan city. CHINA ENVIRONMENTAL SCIENCECE, 2024, 44(10): 5875-5884.
[1] 张崇淼,王晓昌,周进宏,等.城市地表水中肠道病原微生物与粪便污染指示菌的关系研究[J]. 环境科学学报, 2012,32(11):2789-2794. Zhang C M, Wang X C, Zhou J H, et al. Comparative study on enteric pathogens and their relations with fecal indicator bacteria in urban surface waters [J]. Acta Scientiae Circumstantiae, 2012,32(11):2789- 2794. [2] Cui Q, Fang T, Huang Y, et al. Evaluation of bacterial pathogen diversity, abundance and health risks in urban recreational water by amplicon next-generation sequencing and quantitative PCR [J]. Journal of Environmental Sciences, 2017,57:137-149. [3] GB 3838-2002地表水环境质量标准[S]. GB3838-2002 Environmental quality standards for surface water [S]. [4] 刘永军,张崇淼,王晓昌,等.环境水体中肠道病原细菌定量PCR检测与膜过滤分析方法的比较[J]. 环境科学学报, 2008,28(7):1482- 1488. Liu Y J, Zhang C M, Wang X C, et al. Comparison of enteric pathogenic bacteria measurements in surface waters by quantitative polymerase chain reaction and membrane filter culture analysis [J]. Acta Scientiae Circumstantiae, 2008,28(7):1482-1488. [5] 董柏青,龚健,林玫,等.广西壮族自治区2001~2005年伤寒、副伤寒疫情暴发原因分析及控制对策[J]. 中华流行病学杂志, 2006, 27(8):734-735. Dong B Q, Gong J, Lin M, et al. Strategies on epidemiological surveillance and control of typhoid and paratyphoid in 2001~2005[J]. Chinese Journal of Epidemiology, 2006,27(8):734-735. [6] 张杨,郑前兴,吴仁人,等.有氧和厌氧环境下指示菌微生物的稳定性特征[J]. 中国环境科学, 2022,42(3):1327-1334. Zhang Y, Zheng Q X, Wu R R, et al. The stability of microbiological indicators in aerobic and anaerobic environment [J]. China Environmental Science, 2022,42(3):1327-1334. [7] 蒋娟,龙云川,胡菁,等.垃圾堆周边土壤微塑料及潜在病原微生物特征[J]. 中国环境科学, 2023,43(7):3592-3603. Jiang J, Long Y C, Hu J, et al. Characteristics of microplastics and potential pathogenic microorganisms in the soil surrounding a rural garbage dump [J]. China Environmental Science, 2023,43(7):3592- 3603. [8] 施玮,宋伟民,卢纯惠,等. MUCAP试验检测环境水样中沙门氏菌[J]. 中国卫生检验杂志, 1999,9(3):188-190. Shi W, Song W M, Lu C H, et al. MUCAP test to detect Salmonella in environmental water samples [J]. Chinese Journal of Health Laboratory Technology, 1999,9(3):188-190. [9] 张振兴,王江权,郑祥.水体病原微生物定量风险评价:历史、现状与发展趋势[J]. 环境科学学报, 2016,36(1):2-15. Zhang Z X, Wang J Q, Zheng X, et al. Quantitative microbial risk assessment of waterborne pathogens: History and progress [J]. Acta Scientiae Circumstantiae, 2016,36(1):2-15. [10] Kong R Y C, Lee S K Y, Law T W F, et al. Rapid detection of six types of bacterial pathogens in marine waters by multiplex PCR [J]. Water Research, 2002,36(11):2802-2812. [11] Brinkman N E, Francisco R, Nichols T L, et al. Detection of multiple waterborne pathogens using microsequencing arrays [J]. Journal of Applied Microbiology, 2013,114(2):564-573. [12] 李珂,张洪勋,余志晟,等.中国水环境微生物污染研究进展[J]. 科技导报, 2021,39(15):110-116. Li K, Zhang H X, Yu Z S, et al. Research status of microbial pollution in Chinese water environment [J]. Science and Technology Review, 2021,39(15):110-116. [13] 张蕊,丁美月,李慧儒,等.冻融循环下大肠杆菌O157:H7在长春市南湖岸边水中的存活行为研究[J]. 科学技术与工程, 2017,17(21): 150-155. Zhang R, Ding M Y, Li H R, et al. Suivival of Escherichia coli 0157: H7 in Changchun south lake water under freezing and thawing cycle condition [J]. Science Technology and Engineering, 2017,17(21):150- 155. [14] 徐晓璇,康丽娟,叶建锋,等.景观河道病原微生物分布特征及其与环境因子的关系[J]. 水生态学杂志, 2019,40(3):65-70. Xu X X, Kang L J, Ye J F, et al. Distributions of coliform and fecal coliform in three urban rivers and the influence of environmental factors [J]. Journal of Hydroecology, 2019,40(3):65-70. [15] Jjemba P K, Weinrich L A, Cheng W, et al. Regrowth of potential opportunistic pathogens and algae in reclaimed-water distribution systems [J]. Appl Environ Microbiol, 2010,76(13):4169-4178. [16] 毛怡心,郑萍,孙宗科.北京某地水源水及末梢水痢疾志贺菌污染状况[J]. 环境与健康杂志, 2020,37(4):291-293. Mao Y X, Zheng P, Sun Z K. Contamination of source water and tap water by Shigella dysenteriae in an area of Beijing [J]. Journal of Environment and Health, 2020,37(4):291-293. [17] Demeter K, Linke R, Balleste E, et al. Have genetic targets for faecal pollution diagnostics and source tracking revolutionized water quality analysis yet? [J]. FEMS Microbiol Rev, 2023,47(4):1-36. [18] 孙丽华,王春芳,朱珺瑶,等.慢滤对污水厂二级出水中条件致病菌的去除[J]. 中国环境科学, 2023,43(8):3946-3955. Sun L H, Wang C F, Zhu J Y, et al. Removal of opportunistic pathogens in secondary effluent from sewage plants by slow filtration [J]. China Environmental Science, 2023,43(8):3946-3955. [19] APHA, 2012. Standard methods for the examination of water and wastewater [M]. 22th ed. Washington, D.C.: American Public Health Association, American Water Works Association, Water Environment Federation, 2012. [20] 林怡雯,李丹,吴舒旭,等.基于RT-qPCR选择性检测水中活性病原菌[J]. 环境科学, 2012,33(11):4040-4045. Lin Y W, Li D, Wu S X, et al. Selective detection of viable pathogenic bacteria in water using reverse transcription quantitative PCR [J]. Environmental Science, 2012,33(11):4040-4045. [21] Parker A M, Mohler V L, Gunn A A, et al. Development of a qPCR for the detection and quantification of Salmonella spp. in sheep feces and tissues [J]. Journal of Veterinary Diagnostic Investigation, 2020,32(6): 835-843. [22] 毛怡心,孙宗科,郑萍,等.环境水体中痢疾志贺菌荧光定量PCR检测方法研究[J]. 环境与健康杂志, 2016,33(2):145-148. Mao Y X, Sun Z K, Zheng P, et al. Fluorescent quantitative PCR detection method of Shigella dysenteriae in environmental waters [J]. Journal of Environment and Health, 2016,33(2):145-148. [23] 邓闵,李露,宋康.水环境中致病菌快速检测技术及应用研究进展[J]. 环境科学研究, 2023,36(10):1835-1844. Deng M, Li L, Song K. Rapid molecular biology detection and risk assessment of waterborne pathogens: a review [J]. Research of Environmental Sciences, 2023,36(10):1835-1844. [24] Cui Q, Huang Y, Wang H, et al. Diversity and abundance of bacterial pathogens in urban rivers impacted by domestic sewage [J]. Environmental Pollution, 2019,249:24-35. [25] 陈胜蓝,尹红果,陈梦清,等.环境水体中病原微生物与指示微生物的相关性研究[J]. 浙江农业科学, 2015,56(4):448-452,537. Chen S L, Yin H G, Chen M Q, et al. Study on the correlation between pathogenic microorganism and indicator microorganism in environmental water [J]. Journal of Zhejiang Agricultural Sciences, 2015,56(4):448-452,537. [26] 杨梦瑶,张明珠,汪颖,等.迪沟采煤沉陷区水体中人体肠道病原菌致病基因丰度变化及其影响因素[J]. 西南农业学报, 2021,34(12): 2757-2764. Yang M Y, Zhang M Z, Wang Y, et al. Human intestinal pathogenic bacteria in waterbody of Digou coal mining subsidence area changes in abundance of pathogenic genes and their influencing elements [J]. Southwest China Journal of Agricultural Sciences, 2021,34(12):2757- 2764. [27] 赵彩霞,安新丽,苏建强.高通量定量PCR研究环境中的微生物污染特征[J]. 环境化学, 2022,41(10):3144-3158. Zhao C X, An X L, Su J Q. Tracking microbial contaminants in environments by high-throughput quantitative PCR [J]. Environmental Chemistry, 2022,41(10):3144-3158. [28] 姜勇.城市空间拓展对湖泊水质影响及对策研究——以武汉市为例[J]. 城市规划, 2018,42(6):95-99,116. Jiang Y. Impact of urban expansion on lake water quality and countermeasures: a case study of Wuhan [J]. City Planning Review, 2018,42(6):95-99,116. [29] Kelsey H, Porter D E, Scott G, et al. Using geographic information systems and regression analysis to evaluate relationships between land use and fecal coliform bacterial pollution [J]. Journal of Experimental Marine Biology and Ecology, 2004,298(2):197-209. [30] 张千千,李向全,王效科,等.城市路面降雨径流污染特征及源解析的研究进展[J]. 生态环境学报, 2014,23(2):352-358. Zhang Q Q, Li X Q, Wang X K, et al. Research advance in the characterization and source apportionment of pollutants in urban roadway runoff [J]. Ecology and Environmental Sciences, 2014,23(2): 352-358. [31] Gu G, Strawn L K, Ottesen A R, et al. Correlation of Salmonella enterica and Listeria monocytogenes in irrigation water to environmental factors, fecal indicators, and bacterial communities [J]. Front Microbiol, 2020,11:557289. [32] Toro M, Weller D, Ramos R, et al. Environmental and anthropogenic factors associated with the likelihood of detecting Salmonella in agricultural watersheds [J]. Environ. Pollut., 2022,306:119298. [33] Deaven A M, FerreirA C M, Reed E A, et al. Salmonella genomics and population analyses reveal high inter- and intraserovar diversity in freshwater [J]. Appl. Environ. Microbiol., 2021,87(6):e02594-20. [34] Tazehabadi M H, Algburia, Popov I V, et al. Probiotic Bacilli inhibit Salmonella biofilm formation without killing planktonic cells [J]. Front Microbiol, 2021,12:615328. [35] 应鹏聪,周俊,全蓓蓓,等.嘉兴市城市水体微生物污染状况的调查[J]. 嘉兴学院学报, 2005,17(6):78-80. Ying P C, Zhou J, Quan B B, et al. An investigation about the microbiological pollution of the water body in Jiaxing City [J]. Journal of Jiaxing University, 2005,17(6):78-80. [36] 张利华.福州市城市生活饮用水水源地水质状况及大肠杆菌生长影响因素的研究[J]. 科技资讯, 2009,18:138-139. Zhang L H. Study on the water quality of urban drinking water source and the influencing factors of Escherichia coli growth in Fuzhou City [J]. Science and Technology Information, 2009,18:138-139. [37] Fang T, Cui Q, Huang Y, et al. Distribution comparison and risk assessment of free-floating and particle-attached bacterial pathogens in urban recreational water: Implications for water quality management [J]. Science of the Total Environment, 2018,613-614: 428-438. [38] 陈新蕾,许均华,华中,等.东湖水体的微生物污染状况初步调查[J]. 氨基酸和生物资源, 2004,26(1):16-19. Chen X L, Xu J H, Hua Z, et al. Elementary investigation of East Lake on its microbial contamination [J]. Amino Acids and Biotic Resources, 2004,26(1):16-19. [39] Roy P K, Ha A J, Mizan M F R, et al. Effects of environmental conditions (temperature, pH, and glucose) on biofilm formation of Salmonella enterica serotype Kentucky and virulence gene expression [J]. Poult. Sci., 2021,100(7):101209. [40] Huang K H, Hsu B M, Chou M Y, et al. Application of molecular biological techniques to analyze Salmonella seasonal distribution in stream water [J]. FEMS Microbiology Letters, 2014,352(1):87-96. [41] Yuan Y, Zheng G, Lin M, et al. Detection of viable Escherichia coli in environmental water using combined propidium monoazide staining and quantitative PCR [J]. Water Res., 2018,145:398-407. [42] Liu Y, Wang C, Fung C, et al. Quantification of viable but nonculturable Escherichia coli O157: H7 by targeting the rpoS mRNA [J]. Anal. Chem., 2010,82(7):2612-2615. [43] 吴效晋,刘刚,胡洪营,等.环介导等温扩增(LAMP)技术检测水源病原菌[J]. 环境工程, 2021,39(12):10-17,37. Wu X J, Liu G, Hu H Y, et al. Detection of waterborne pathogens by loop-mediated isothermal amplification (LAMP) [J]. Environmental Engineering, 2021,39(12):10-17,37. [44] 孙傅,沙婧,张一帆,等.城市景观娱乐水体微生物风险评价[J]. 环境科学, 2013,34(3):933-942. Sun F, Sha J, Zhang Y F, et al. Microbial risk assessment of urban water bodies for aesthetical and recreational uses [J]. Environmental Science, 2013,34(3):933-942.
