四环素对污泥蚯蚓粪中微生物种群和抗性基因的影响
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摘要
城市污泥中高含量的四环素可能会致使污泥蚯蚓堆肥产物中携带高丰度的抗性基因,降低其利用价值.本实验采用赤子爱胜蚓处理添加不同含量四环素(100、500和1 000 mg·kg-1)的新鲜污泥,以不添加为对照组,分析微生物种群和四环素抗性基因(tet C、tet G、tet M、tet W和tet X)及整合子基因(int I1)在不同四环素选择性压力下的变化,揭示四环素含量对污泥蚯蚓堆肥中微生物种群和抗性基因的影响.结果表明,添加四环素降低了污泥蚯蚓堆肥产物中变形菌门的丰度但增加了拟杆菌门的丰度,且四环素的含量与细菌的Shannon和Pielou指数有明显的负相关关系.同时,添加四环素致使int I1增加了4. 25倍;四环素类抗性基因增加了4. 7～186. 9倍,其中tet M基因丰度与四环素含量呈现出显著的正相关关系.因此初始污泥中较高含量的四环素会改变污泥蚯蚓粪的微生物种群结构,增加抗生素抗性基因的丰度和传播风险.
The high content of tetracycline in municipal sludge may result in vermicomposting products carrying a high abundance of antibiotic resistance genes,thus lowering the utilization value of the vermicompost. Hence,this study aimed to reveal the underlying effects of tetracycline concentrations on the resistance genes involved in vermicomposting systems for sludge recycling. For this purpose,fresh sludge substrates with different concentrations of tetracycline( 100,500,and 1000 mg·kg-1) were vermicomposted for60 days using Eisenia foetida. In parallel,sludge treatment without the addition of the tetracycline was used as a control. During the experiment,changes in bacterial communities,tetracycline resistance genes( tet C,tet G,tet M,tet W,and tet X),and class 1 integron( int I1) were detected using high-throughput sequencing and qualitative PCR,respectively. The results showed that the addition of tetracycline reduced the abundance of Proteobacteria but increased the abundance of Bacteroidetes in the sludge vermicompost.Furthermore,the concentrations of tetracycline had a significant negative correlation with Shannon and Pielou indexes of bacterial diversity. In addition,tetracycline increased int I1 genes and tetracycline resistance genes in the sludge by 4. 25 times and 4. 7-186. 9 times,respectively. Moreover,there was a significantly positive correlation between the abundance of tet M genes and tetracycline concentration. This study suggests that higher concentration of tetracycline in sludge can modify the microbial community structure of vermicompost,enhancing the abundance of antibiotic resistance genes and their associated dissemination risks.
The high content of tetracycline in municipal sludge may result in vermicomposting products carrying a high abundance of antibiotic resistance genes,thus lowering the utilization value of the vermicompost. Hence,this study aimed to reveal the underlying effects of tetracycline concentrations on the resistance genes involved in vermicomposting systems for sludge recycling. For this purpose,fresh sludge substrates with different concentrations of tetracycline( 100,500,and 1000 mg·kg-1) were vermicomposted for60 days using Eisenia foetida. In parallel,sludge treatment without the addition of the tetracycline was used as a control. During the experiment,changes in bacterial communities,tetracycline resistance genes( tet C,tet G,tet M,tet W,and tet X),and class 1 integron( int I1) were detected using high-throughput sequencing and qualitative PCR,respectively. The results showed that the addition of tetracycline reduced the abundance of Proteobacteria but increased the abundance of Bacteroidetes in the sludge vermicompost.Furthermore,the concentrations of tetracycline had a significant negative correlation with Shannon and Pielou indexes of bacterial diversity. In addition,tetracycline increased int I1 genes and tetracycline resistance genes in the sludge by 4. 25 times and 4. 7-186. 9 times,respectively. Moreover,there was a significantly positive correlation between the abundance of tet M genes and tetracycline concentration. This study suggests that higher concentration of tetracycline in sludge can modify the microbial community structure of vermicompost,enhancing the abundance of antibiotic resistance genes and their associated dissemination risks.
引文
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[25]王桂珍,李兆君,张树清,等.土霉素在鸡粪好氧堆肥过程中的降解及其对相关参数的影响[J].环境科学,2013,34(2):795-803.Wang G Z, Li Z J, Zhang S Q, et al. Degradation of oxytetracycline in chicken feces aerobic-composting and its effects on their related parameters[J]. Environmental Science,2013,34(2):795-803.
[26]郭梦婷,邓友华,冯小晏,等.土霉素残留对猪粪堆肥过程中理化性质的影响[J].环境污染与防治,2012,34(2):50-54.Guo M T,Deng Y H,Feng X Y,et al. Effects of residual oxytetracycline on the physical and chemical properties of pig manure during composting[J]. Environmental Pollution and Control,2012,34(2):50-54.
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[32] Gutierrez T,Rhodes G,Mishamandani S,et al. Polycyclic aromatic hydrocarbon degradation of phytoplankton-associated Arenibacter spp. and description of Arenibacter algicola sp. nov.,an aromatic hydrocarbon-degrading bacterium[J]. Applied and Environmental Microbiology,2014,80(2):618-628.
[33] Agamennone V, Roelofs D, Van Straalen N M, et al.Antimicrobial activity in culturable gut microbial communities of springtails[J]. Journal of Applied Microbiology,2018,125(3):740-752.
[34]段佳丽,薛泉宏,舒志明,等.放线菌Act12与腐植酸钾配施对丹参生长及其根域微生态的影响[J].生态学报,2015,35(6):1807-1819.Duan J L,Xue Q H,Shu Z M,et al. Effects of combined application of actinomycetes Act12 bio-control agents and potassium humate on growth and microbial flora in rooting zone of Salvia miltiorrhiza Bge[J]. Acta Ecologica Sinica,2015,35(6):1807-1819.
[35] Smith M S,Yang R K,Knapp C W,et al. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR[J]. Applied and Environmental Microbiology,2004,70(12):7372-7377.
[36] Cui G Y,Li F S,Li S L,et al. Changes of quinolone resistance genes and their relations with microbial profiles during vermicomposting of municipal excess sludge[J]. Science of the Total Environment,2018,644:494-502.
[37]韦蓓,黄福义,苏建强.堆肥对污泥中四环素类抗生素及抗性基因的影响[J].环境工程学报,2014,8(12):5431-5438.Wei B, Huang F Y, Su J Q. Effect of composting on tetracyclines and tetracycline resistance genes in sewage sludge[J]. Chinese Journal of Environmental Engineering,2014,8(12):5431-5438.
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[2] Hvistendahl M. China takes aim at rampant antibiotic resistance[J]. Science,2012,336(6083):795.
[3] Zhang Q Q,Ying G G, Pan C G, et al. Comprehensive evaluation of antibiotics emission and fate in the river basins of China:source analysis,multimedia modeling,and linkage to bacterial resistance[J]. Environmental Science&Technology,2015,49(11):6772-6782.
[4] Chee-Sanford J C,Mackie R I,Koike S,et al. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste[J]. Journal of Environmental Quality,2009,38(3):1086-1108.
[5]罗义,周启星.抗生素抗性基因(ARGs)———一种新型环境污染物[J].环境科学学报,2008,28(8):1499-1505.Luo Y,Zhou Q X. Antibiotic resistance genes(ARGs)as emerging pollutants[J]. Acta Scientiae Circumstantiae,2008,28(8):1499-1505.
[6]窦春玲,郭雪萍,尹大强.污水处理厂抗生素抗性基因分布和去除研究进展[J].环境化学,2013,32(10):1885-1893.Dou C L,Guo X P,Yin D Q. Review on distribution and removal of antibiotic resistance genes(ARGs)in wastewater treatment plants(WWTPs)[J]. Environmental Chemistry,2013,32(10):1885-1893.
[7] Auerbach E A,Seyfried E E,Mc Mahon K D. Tetracycline resistance genes in activated sludge wastewater treatment plants[J]. Water Research,2007,41(5):1143-1151.
[8] Munir M,Wong K,Xagoraraki I. Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan[J]. Water Research,2011,45(2):681-693.
[9] Zhang X X,Zhang T. Occurrence,abundance,and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations[J]. Environmental Science&Technology,2011,45(7):2598-2604.
[10] Pruden A,Pei R T,Storteboom H,et al. Antibiotic resistance genes as emerging contaminants:studies in northern colorado[J]. Environmental Science&Technology,2006,40(23):7445-7450.
[11] Su J Q,Wei B,Ouyang W Y,et al. Antibiotic resistome and its association with bacterial communities during sewage sludge composting[J]. Environmental Science&Technology,2015,49(12):7356-7363.
[12] Yang Y,Li B,Zou S C,et al. Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach[J].Water Research,2014,62:97-106.
[13]任佳,姚宏,刘苗苗,等.厌氧和好氧处理过程中四环素抗药基因的丰度[J].中国环境科学,2016,36(1):268-275.Ren J,Yao H,Liu M M,et al. Characteristics of tetracycline resistance genes in the anaerobic and aerobic treatment of tetracycline production wastewater[J]. China Environmental Science,2016,36(1):268-275.
[14] Domínguez J,Aira M,Gómez-Brandón M. Vermicomposting:earthworms enhance the work of microbes[A]. In:Insam H,Franke-Whittle I,Goberna M(Eds.). Microbes at Work[M].Berlin,Heidelberg:Springer,2010. 93-114.
[15]张志剑,刘萌,朱军.蚯蚓堆肥及蝇蛆生物转化技术在有机废弃物处理应用中的研究进展[J].环境科学,2013,34(5):1679-1686.Zhang Z J,Liu M,Zhu J. Organic waste treatment by earthworm vermicomposting and larvae bioconversion:review and perspective[J]. Environmental Science,2013,34(5):1679-1686.
[16] Pathma J,Sakthivel N. Molecular and functional characterization of bacteria isolated from straw and goat manure based vermicompost[J]. Applied Soil Ecology,2013,70:33-47.
[17] Huang K,Xia H,Cui G Y,et al. Effects of earthworms on nitrification and ammonia oxidizers in vermicomposting systems for recycling of fruit and vegetable wastes[J]. Science of the Total Environment,2017,578:337-345.
[18]黄魁,夏慧,陈景阳,等.蚯蚓对城市污泥蚯蚓堆肥过程中微生物特征变化的影响[J].环境科学学报,2018,38(8):3146-3152.Huang K,Xia H,Chen J Y,et al. Effects of earthworms on changes of microbial characteristics during vermicomposting of municipal sludge[J]. Acta Scientiae Circumstantiae,2018,38(8):3146-3152.
[19] Yasir M,Aslam Z,Kim S W,et al. Bacterial community composition and chitinase gene diversity of vermicompost with antifungal activity[J]. Bioresource Technology, 2009, 100(19):4396-4403.
[20] Qian X,Sun W,Gu J,et al. Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure[J]. Journal of Hazardous Materials,2016,315:61-69.
[21] Selvam A,Xu D L,Zhao Z Y,et al. Fate of tetracycline,sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure[J].Bioresource Technology,2012,126:383-390.
[22]曾萍,刘诗月,张俊珂,等.芬顿法深度处理生物处理排水中的四环素抗性基因[J].中国环境科学,2017,37(9):3315-3323.Zeng P,Liu S Y,Zhang J K,et al. Advanced Fenton oxidation treatment of tetracycline resistance genes in effluent discharged from biological wastewater treatment[J]. China Environmental Science,2017,37(9):3315-3323.
[23] Huang K,Xia H,Wu Y,et al. Effects of earthworms on the fate of tetracycline and fluoroquinolone resistance genes of sewage sludge during vermicomposting[J]. Bioresource Technology,2018,259:32-39.
[24]吴安驰,邓湘雯,任小丽,等.中国典型森林生态系统乔木层群落物种多样性的空间分布格局及其影响因素[J].生态学报,2018,38(21):7727-7738.Wu A C,Deng X W,Ren X L,et al. Biogeographic patterns and influencing factors of the species diversity of tree layer community in typical forest ecosystems in China[J]. Acta Ecologica Sinica,2018,38(21):7727-7738.
[25]王桂珍,李兆君,张树清,等.土霉素在鸡粪好氧堆肥过程中的降解及其对相关参数的影响[J].环境科学,2013,34(2):795-803.Wang G Z, Li Z J, Zhang S Q, et al. Degradation of oxytetracycline in chicken feces aerobic-composting and its effects on their related parameters[J]. Environmental Science,2013,34(2):795-803.
[26]郭梦婷,邓友华,冯小晏,等.土霉素残留对猪粪堆肥过程中理化性质的影响[J].环境污染与防治,2012,34(2):50-54.Guo M T,Deng Y H,Feng X Y,et al. Effects of residual oxytetracycline on the physical and chemical properties of pig manure during composting[J]. Environmental Pollution and Control,2012,34(2):50-54.
[27] CAFA(Commission on Antimicrobial Feed Additives).Antimicrobial feed additives[R]. Stockholm,Sweden:Ministry of Agriculture,1997. 132.
[28]时红蕾,王晓昌,李倩,等.四环素对人粪便好氧堆肥过程及微生物群落演替的影响[J].环境科学,2018,39(6):2810-2818.Shi H L,Wang X C,Li Q,et al. Effects of elevated tetracycline concentrations on aerobic composting of human feces:composting behavior and microbial community succession[J]. Environmental Science,2018,39(6):2810-2818.
[29] De Gannes V,Eudoxie G,Hickey W J. Prokaryotic successions and diversity in composts as revealed by 454-pyrosequencing[J].Bioresource Technology,2013,133:573-580.
[30] Knapp B A,Podmirseg S M,Seeber J,et al. Diet-related composition of the gut microbiota of Lumbricus rubellus as revealed by a molecular fingerprinting technique and cloning[J]. Soil Biology and Biochemistry,2009,41(11):2299-2307.
[31] Huang K,Xia H,Li F S,et al. Optimal growth condition of earthworms and their vermicompost features during recycling of five different fresh fruit and vegetable wastes[J]. Environmental Science and Pollution Research,2016,23(13):13569-13575.
[32] Gutierrez T,Rhodes G,Mishamandani S,et al. Polycyclic aromatic hydrocarbon degradation of phytoplankton-associated Arenibacter spp. and description of Arenibacter algicola sp. nov.,an aromatic hydrocarbon-degrading bacterium[J]. Applied and Environmental Microbiology,2014,80(2):618-628.
[33] Agamennone V, Roelofs D, Van Straalen N M, et al.Antimicrobial activity in culturable gut microbial communities of springtails[J]. Journal of Applied Microbiology,2018,125(3):740-752.
[34]段佳丽,薛泉宏,舒志明,等.放线菌Act12与腐植酸钾配施对丹参生长及其根域微生态的影响[J].生态学报,2015,35(6):1807-1819.Duan J L,Xue Q H,Shu Z M,et al. Effects of combined application of actinomycetes Act12 bio-control agents and potassium humate on growth and microbial flora in rooting zone of Salvia miltiorrhiza Bge[J]. Acta Ecologica Sinica,2015,35(6):1807-1819.
[35] Smith M S,Yang R K,Knapp C W,et al. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR[J]. Applied and Environmental Microbiology,2004,70(12):7372-7377.
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