徐永剛， 宇萬太， 馬 強(qiáng)， 周 樺， 姜春明

中國科學(xué)院沈陽應(yīng)用生態(tài)研究所，沈陽 110016

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環(huán)境中抗生素及其生態(tài)毒性效應(yīng)研究進(jìn)展

徐永剛， 宇萬太*， 馬 強(qiáng)， 周 樺， 姜春明

中國科學(xué)院沈陽應(yīng)用生態(tài)研究所，沈陽 110016

近年來，越來越多的抗生素類藥物用于在醫(yī)療、畜禽和水產(chǎn)養(yǎng)殖業(yè)。由于其機(jī)體代謝率低，大部分以原藥或代謝物的形式經(jīng)由尿液和糞便排出體外進(jìn)入環(huán)境中，造成抗生素在水體和土壤等環(huán)境介質(zhì)中的殘留。這些殘留的抗生素會導(dǎo)致潛在的環(huán)境風(fēng)險，其中最嚴(yán)重的是會誘發(fā)和傳播各類抗生素抗性基因(antibiotic resistance genes, ARGs)，進(jìn)而對人類健康產(chǎn)生威脅。本文介紹了環(huán)境中抗生素的來源，歸趨和殘留狀況，并且對其所引起的生態(tài)毒性效應(yīng)以及ARGs進(jìn)行總結(jié)，最后指出了目前研究中存在的問題，并對未來研究進(jìn)行了展望。

抗生素；生態(tài)毒性效應(yīng)；抗性基因

抗生素類藥物(以下簡稱抗生素)是由微生物(包括細(xì)菌、真菌、放線菌屬)或高等動植物在生活過程中所產(chǎn)生的具有抗病原體或其它活性的一類次級代謝產(chǎn)物，能干擾其他生活細(xì)胞發(fā)育功能的化學(xué)物質(zhì)?，F(xiàn)常用的抗生素除了包括β-內(nèi)酰胺類，氨基糖苷類，氯霉素類，大環(huán)內(nèi)脂類和四環(huán)素類抗生素等微生物培養(yǎng)液中提取物的抗生素，還包括磺胺類和喹諾酮類等用化學(xué)方法合成或半合成的藥物。抗生素除了用于人類和動物感染性疾病的治療，也被作為促長劑添加于飼料中在養(yǎng)殖業(yè)中大量應(yīng)用。據(jù)統(tǒng)計，美國1999年抗生素的使用量為2.68萬t，其中60%用于人類的疾病治療和預(yù)防，32%用作養(yǎng)殖業(yè)生長促進(jìn)劑，另8%用作治療劑[1]。1999年，歐盟和瑞士共消耗抗生素1.33萬t，其中65%是醫(yī)用，29%是動物養(yǎng)殖獸藥，6%是動物生長促進(jìn)劑[2]。中國是抗生素使用大國，也是抗生素生產(chǎn)大國。根據(jù)化學(xué)工業(yè)制藥工業(yè)協(xié)會2005年統(tǒng)計數(shù)據(jù)，我國每年抗生素原料生產(chǎn)量約為21萬t，其中有9.7萬t(占年總產(chǎn)量的46.1%)的抗生素用于養(yǎng)殖業(yè)。

大部分抗生素具有水溶性，人類和動物服用的抗生素有30%～90%將隨糞尿排出體外[3]。大量未被代謝的抗生素經(jīng)不同途徑進(jìn)入環(huán)境，雖然抗生素的半衰期不長，但由于頻繁使用并進(jìn)入環(huán)境，導(dǎo)致水體、沉積物和土壤等環(huán)境介質(zhì)抗生素及其代謝活性產(chǎn)物濃度逐漸提高[3]。環(huán)境殘留的抗生素不僅可抑制微生物的生長和活性，也可對動植物產(chǎn)生毒性效應(yīng)，進(jìn)而干擾其生態(tài)功能，對維持生態(tài)系統(tǒng)的穩(wěn)定構(gòu)成潛在風(fēng)險[4]。另外，抗生素還可誘導(dǎo)微生物產(chǎn)生抗性基因，其可在水、土壤和空氣等環(huán)境介質(zhì)中以及動植物體內(nèi)傳播擴(kuò)散，從而對人類健康構(gòu)成巨大威脅[5,6]。

1 環(huán)境抗生素的來源和和歸趨

1.1 環(huán)境中抗生素的來源

自然界存在于土壤中的一些細(xì)菌種類本身可以合成抗生素，如鏈霉菌等放線菌類，但是抗生素的環(huán)境本底值總體是非常微量的。目前，環(huán)境中抗生素主要來源于抗生素工業(yè)廢水、醫(yī)用抗生素和農(nóng)用抗生素。圖1列舉了環(huán)境中抗生素的來源及其遷移途徑。

醫(yī)用抗生素的使用主要在醫(yī)院和家庭。此類抗生素不能被人體完全吸收或代謝，未吸收的抗生素和代謝產(chǎn)物通過糞尿排出體外進(jìn)入廢水系統(tǒng)。醫(yī)院里抗生素使用較為頻繁且集中，因此醫(yī)院廢水中抗生素種類較少，以喹諾酮類和磺胺類藥物為主，但其濃度較高，含量可達(dá)μg·L-1級別[8-9]。家庭使用的抗生素一部分通過人體排泄進(jìn)入環(huán)境水體，另一部分作為固體垃圾被丟棄，并極有可能因為浸泡、腐蝕而滲入水體環(huán)境。

農(nóng)用抗生素主要在畜禽養(yǎng)殖和水產(chǎn)養(yǎng)殖業(yè)中使用。它們除了被用來預(yù)防和治療動物疾病，還以亞治療劑量長期添加于飼料中作為促生長劑使用。在畜禽養(yǎng)殖業(yè)中，大部分的抗生素都不能被動物體吸收或代謝通過糞尿排泄出體外。目前，高濃度抗生素頻繁發(fā)現(xiàn)于集約化畜禽養(yǎng)殖場廢水和畜禽糞便中，其檢出濃度多在μg·L-1或mg·kg-1級別，且主要以四環(huán)素、喹諾酮和磺胺類等獸藥抗生素為主[10-13]。這些廢棄物無論用作肥料施用于農(nóng)田，還是直接排放，都可能隨著地表徑流匯入江河或淋溶至地下水，并很有可能通過飲用水源和植物吸收積累進(jìn)入食物鏈，威脅人類健康。

圖1 環(huán)境中抗生素的來源與遷移途徑Fig. 1 The sources and migration paths of antibiotics in the environment[7]

水產(chǎn)養(yǎng)殖中抗生素的使用主要以直接投放為主，因此大量未被水產(chǎn)養(yǎng)殖生物吸收及隨糞便排泄的抗生素殘留于水體，或沉降富集于底泥，成為水環(huán)境抗生素的一個重要污染源。盡管各國對水產(chǎn)養(yǎng)殖用藥規(guī)定不同，但磺胺類和喹諾酮類藥物均被頻繁檢出，其濃度高達(dá)幾十mg·L-1或mg·kg-1[14-16]。

醫(yī)藥生產(chǎn)企業(yè)污水廢料也是環(huán)境抗生素的重要來源，但對其抗生素類型和含量的報道不多。僅有的幾篇文獻(xiàn)資料顯示，制藥廠廢水中抗生素種類與其所生產(chǎn)的藥品種類有關(guān)，其含量很高，濃度在mg·L-1級別[17,18]。

醫(yī)院、養(yǎng)殖和制藥廢水通過市政污水收集系統(tǒng)進(jìn)入污水處理廠，經(jīng)過稀釋作用使其抗生素含量降低，濃度多在幾百到幾千ng·L-1范圍。然而現(xiàn)有的常規(guī)水處理技術(shù)很難將其去除，污水處理廠出水中抗生素濃度仍在ng·L-1級別。在污水廠進(jìn)水和出水中，最常被檢出的是大環(huán)內(nèi)酯類、磺胺類和喹諾酮類抗生素(表1)。另外，在污水廠處理流程中抗生素會不斷地吸附在活性污泥上而不容易降解，對抗生素具有一定的蓄積作用。四環(huán)素類、喹諾酮類和磺胺類抗生素已在污泥中被頻繁的檢出，且檢測濃度多在μg·kg-1級別(表1)。污水處理廠尾水直接排放入河流或作為農(nóng)田灌溉用水以及污泥施用于農(nóng)田都成為環(huán)境抗生素污染的一個主要來源。

1.2 抗生素在環(huán)境中的歸趨

和其它有機(jī)污染物一樣，進(jìn)入土壤、水和沉積物等環(huán)境介質(zhì)的抗生素通過吸附、遷移和降解等一系列生化過程在環(huán)境介質(zhì)間發(fā)生再分配，這將直接影響抗生素在環(huán)境中的殘留濃度及其生物學(xué)效應(yīng)。

1.2.1 吸附和遷移

吸附行為是抗生素在環(huán)境介質(zhì)間的重要物理化學(xué)過程，其直接決定了遷移與降解過程?？股赝ㄟ^范德華力、色散力、誘導(dǎo)力和氫鍵等分子間作用力與環(huán)境介質(zhì)的吸附位點(diǎn)相吸附，或者抗生素的分子功能基團(tuán)(如羧酸、醛、胺類)與環(huán)境介質(zhì)表面發(fā)生化學(xué)反應(yīng)形成絡(luò)合物或螯合物。因此，抗生素的性質(zhì)(如親水性、空間構(gòu)型和官能團(tuán))決定了其在環(huán)境介質(zhì)上的吸附能力[33]。例如，四環(huán)素類和喹諾酮類抗生素具有較多的羧基、羰基和酰胺基等極性官能團(tuán)使其與環(huán)境介質(zhì)有很強(qiáng)的親和力；盡管大環(huán)內(nèi)酯類抗生素含有的極性官能團(tuán)不少，但因分子較大阻礙環(huán)境介質(zhì)對其的吸附；氨基糖苷類和β-內(nèi)酰胺類抗生素極性較強(qiáng)，因此固相介質(zhì)對其吸附能力較弱；磺胺類抗生素僅含有苯胺基和酰胺基兩個離子型官能團(tuán)，與環(huán)境介質(zhì)的吸附作用很弱。其它種類的抗生素與環(huán)境介質(zhì)的吸附研究較少。綜合資料表明[34-36]，抗生素吸附作用強(qiáng)弱順序依次為四環(huán)素類>氟喹諾酮類>大環(huán)內(nèi)酯類>氨基糖苷類>β-內(nèi)酰胺類>磺胺類。

表1 污水處理廠污水和污泥中抗生素含量

環(huán)境介質(zhì)對抗生素的吸附行為也受環(huán)境因子的調(diào)控。研究最多的是pH的影響，它通過改變抗生素和吸附介質(zhì)的電荷狀態(tài)對吸附產(chǎn)生顯著影響。多數(shù)研究顯示抗生素的吸附能力隨土壤或沉積物pH的增加而降低[37-39]。此外，不同形態(tài)的金屬離子對抗生素吸附的影響不同。比如，多價態(tài)金屬離子通過共價鍵連接抗生素帶負(fù)電部分與固體表面的負(fù)吸附位，形成抗生素-金屬離子-吸附介質(zhì)三相絡(luò)合物，進(jìn)而促進(jìn)吸附[40]。然而，Na+、K+等一價金屬離子通過與陽離子態(tài)/0價態(tài)的抗生素競爭吸附位進(jìn)而減少吸附[41]。粘粒礦物和有機(jī)質(zhì)組分是抗生素在土壤和沉積物中的主要吸附位點(diǎn)，因此多數(shù)研究發(fā)現(xiàn)抗生素的Kd值與粘土礦物和有機(jī)質(zhì)含量成正相關(guān)[42,43]。

抗生素在土壤或沉積物剖面內(nèi)的遷移與吸附作用相關(guān)聯(lián)。吸附性能越強(qiáng)的物質(zhì)，與土壤等介質(zhì)的結(jié)合能力越強(qiáng)，則遷移能力越差，因此，多數(shù)研究者通過土柱淋溶實驗發(fā)現(xiàn)磺胺類藥物能淋溶較深土層或地下水[44,45]。

1.2.2 降解

抗生素在環(huán)境中可能發(fā)生水解、光解(統(tǒng)稱非生物降解)和微生物降解等一系列降解反應(yīng)。視環(huán)境條件的不同，抗生素會發(fā)生一種或多種降解反應(yīng)，比如，糞便、土壤和沉積物中主要是微生物降解，而水體中主要以非生物降解方式為主，特別是厭氧條件下[46]。應(yīng)該注意的是，一般降解過程會降低抗生素的藥效，但有些抗生素的代謝物有著抗生素本身的毒性甚至更毒，且可能轉(zhuǎn)化回抗生素原藥[47]。

水解是水體中抗生素降解的重要方式。β-內(nèi)酰胺類、大環(huán)內(nèi)酯類和四環(huán)素類抗生素易溶于水發(fā)生水解。pH是影響抗生素水解的重要環(huán)境因子。例如，大環(huán)內(nèi)酯類抗生素在中性pH條件下水解慢，且活性較低[48]；β-內(nèi)酰胺類在弱酸至強(qiáng)堿條件下水解速度都很快[49]。此外，部分抗生素的水解還受到溫度和離子強(qiáng)度的影響[50,51]。

微生物降解是大部分抗生素在固相環(huán)境中降解的重要途徑，其速率主要受抗生素種類的影響[55,56]。同樣，環(huán)境抗生素微生物降解速率也受眾多環(huán)境因素的影響，尤其是影響降解微生物生存和活性的環(huán)境因子，比如溫度、營養(yǎng)物質(zhì)、供氧狀況、生物量以及環(huán)境中抗生素濃度水平等[57,58]。

2 環(huán)境中抗生素的殘留狀況

2.1 自然水體

環(huán)境中的絕大部分抗生素最終都會進(jìn)入水環(huán)境，因此其對水環(huán)境的影響最為嚴(yán)重，也是最受關(guān)注的環(huán)境污染問題。目前的相關(guān)研究表明，世界各國和地區(qū)的地表水、地下水和飲用水中抗生素殘留現(xiàn)象是比較普遍[59]。與污廢水相比，地表水中抗生素存在的種類較多，但含量較低，其含量在幾十到幾百ng·L-1范圍(表2)。地表水中的抗生素也有很大部分被吸附到沉積物中，但其含量較污泥和養(yǎng)殖場底泥低很多，其抗生素含量多在幾十到幾百μ g·kg-1范圍(表1)。沉積物中以喹諾酮類和四環(huán)素類抗生素為主，這主要是由于喹諾酮類和四環(huán)素類抗生素在固體顆粒上吸附能力較強(qiáng)?？股卦谒统练e物間的遷移轉(zhuǎn)化是一個動態(tài)平衡的過程，即沉積物是抗生素的儲存庫，同時也是水中抗生素潛在的污染源。

表2 地表水和沉積物中抗生素的污染水平

注：nd代表未檢出.

Note: nd=not detected

國內(nèi)外許多文獻(xiàn)報道了地下水中抗生素的存在，但由于土壤層的天然凈化作用，地下水受抗生素污染程度較低，一般檢測到的含量在幾十ng·L-1，且主要以遷移能力強(qiáng)的磺胺類藥物為主(表3)。應(yīng)該引起重視的是世界多地飲用水中也檢測到抗生素的殘留(表3)。盡管飲用水中抗生素含量不高(一般在幾個ng·L-1范圍)，但其中的抗生素殘留仍然對人類健康有著不容忽視的影響。

2.2 土壤中抗生素的殘留狀況

抗生素隨污水灌溉、畜禽糞便和污泥施肥等途徑進(jìn)入土壤環(huán)境。不同國家和地區(qū)土壤中抗生素殘留水平有所差異，但總體看來土壤中抗生素含量一般在μg·kg-1級，如表4。醫(yī)用和農(nóng)用抗生素在土壤中可被大量檢出，包括四環(huán)素、喹諾酮類、磺胺類和大環(huán)內(nèi)脂類抗生素等。綜合資料表明[94]，人為干擾的土壤中抗生素總量容易超過歐盟醫(yī)藥產(chǎn)品排放基準(zhǔn)值(100 μg·kg-1)。

以上研究表面，目前有關(guān)抗生素在各種環(huán)境中的存在和污染水平的報道日漸增多，但是仍然缺乏合適的且具有可比性的分析測定方法。世界各國或地區(qū)報道的抗生素污染水平的差異部分源于此。

3 環(huán)境中抗生素的生態(tài)毒性效應(yīng)

抗生素在藥物設(shè)計時主要是針對人體和動物體內(nèi)的病原性致病菌，因此，環(huán)境中殘留的抗生素也會對環(huán)境中其他有機(jī)體產(chǎn)生不同程度的潛在的生態(tài)毒性效應(yīng)。

3.1 對土壤生物的生態(tài)毒性效應(yīng)

3.1.1 微生物

由于抗生素本身設(shè)計為抗菌藥物，能直接殺死或抑制土壤中相關(guān)微生物的生長，從而影響微生物活性或功能。與其它污染物相似，抗生素的微生物毒性作用呈現(xiàn)劑量效應(yīng)[95-97]。多數(shù)研究顯示低濃度的抗生素?zé)o顯著毒性效應(yīng)，這可能與土壤吸附有很大關(guān)系[98]。有意思的是，部分研究顯示添加低劑量的抗生素甚至可以對土壤微生物產(chǎn)生刺激作用，其原因可能在于這些抗生素可以作為某些微生物的碳源促進(jìn)其生長[99]。但也有學(xué)著研究發(fā)現(xiàn)，在低濃度抗生素條件下微生物活性也會受到顯著影響。例如，Toth等[100]研究發(fā)現(xiàn)磺胺二甲嘧啶和莫能菌素在環(huán)境濃度條件下(≤200 μg·kg-1)對土壤鐵還原和硝化作用產(chǎn)生顯著影響。

表3 地下水和飲用水中抗生素的污染水平

表4 土壤中抗生素殘留狀況

抗生素類藥物有其靶標(biāo)的微生物，因此，靶標(biāo)微生物受到抑制后，環(huán)境中的其它微生物可以獲得大量的資源，從而刺激其快速生長繁殖，對整個環(huán)境微生物群落結(jié)構(gòu)產(chǎn)生影響。多位研究者采用分子指紋技術(shù)(如DGGE、T-RFLP等)研究了抗生素對土壤微生物群落結(jié)構(gòu)的影響[101-103]，結(jié)果顯示，抗生素處理土壤后，代表不同微生物種類的條帶會出現(xiàn)或消失，這說明抗生素對土壤微生物群落結(jié)構(gòu)產(chǎn)生了顯著影響。多數(shù)抗生素為抑細(xì)菌或滅細(xì)菌藥物，因此此類抗生素的添加能降低土壤細(xì)菌數(shù)量，進(jìn)而增加土壤真菌/細(xì)菌比例[104,105]。部分抗生素對革蘭氏陽性菌(G+)和革蘭氏陰性菌(G-)也具有選擇性，因此G+/G-比例也會受到影響[106,107]。應(yīng)該注意的是，抗生素也會直接作用于非靶標(biāo)微生物。例如，Mohamed等[108]研究顯示，游霉素(一種真菌抑制劑)在較高濃度下也會對細(xì)菌數(shù)量和群落結(jié)構(gòu)產(chǎn)生影響。

許多研究者發(fā)現(xiàn)抗生素對土壤微生物群落功能多樣性的影響[109,110]。但是直到現(xiàn)在，抗生素對參與生態(tài)系統(tǒng)過程的功能微生物群落的研究仍然很少。僅有Schauss等[111]和Kleineidam等[112]分別研究了豬糞配施磺胺嘧啶對氨氧化和反硝化微生物群落的影響。

3.1.2 動物

土壤動物(如蚯蚓，線蟲，變形蟲和輪蟲等)不但對土壤起著天然的“過濾”和“凈化”作用，而且在環(huán)境監(jiān)測和生態(tài)毒性診斷研究中等方面也起著重要的作用?，F(xiàn)有研究顯示，只有在極高濃度條件下(效應(yīng)濃度已遠(yuǎn)超過實際環(huán)境濃度)，抗生素才會對土壤動物產(chǎn)生毒副作用[113,114]。Baguer等[115]研究了不同濃度土霉素和泰樂菌素對土壤無脊椎動物蚯蚓、跳蟲和線蚓的影響，結(jié)果發(fā)現(xiàn)這兩種藥物對所測定的三種土壤動物的毒性較低，其ECl0達(dá)到150 mg·kg-1。陳海剛等[116]也發(fā)現(xiàn)喹乙醇、阿散酸和土霉素只有在高濃度條件下(500、500和125 mg·L-1)才會顯著影響赤子愛勝蚓(Eisenia foetida )體中的纖維素酶和超氧化物歧化酶(SOD酶)活力。盡管抗生素對土壤動物的急性毒性低，但并不能就此忽略。因為它們及代謝物在環(huán)境中可發(fā)生遷移，并可在環(huán)境生物中蓄積并造成蓄積毒性。因而有必要進(jìn)一步進(jìn)行抗生素及其降解產(chǎn)物對土壤動物的慢性毒性或蓄積毒性試驗。

3.1.3 植物

抗生素對植物生長發(fā)育的影響除與其自身的性質(zhì)和使用劑量，還與培養(yǎng)介質(zhì)和植物品種等有關(guān)。Boxall等[117]研究發(fā)現(xiàn)，土培條件下1 mg·kg-1濃度土霉素、保泰松和恩諾沙星能顯著抑制胡蘿卜和萵苣生長，而相同濃度的阿莫西林、磺胺嘧啶、泰樂素、甲氧芐啶和氟苯尼考等對這兩種蔬菜生長沒有影響。與其它污染物相似，抗生素在低濃度下可促進(jìn)植物生長，高濃度則抑制植物生長[118,119]。同種抗生素對不同植物的生態(tài)毒性差異非常大。Eggen等[120]研究表明，當(dāng)環(huán)丙沙星添加濃度為10 mg·kg-1時對大麥和胡蘿卜的生長產(chǎn)生抑制作用，其中胡蘿卜對環(huán)丙沙星的毒性效應(yīng)更為敏感。

3.2 對水生生物的生態(tài)毒性效應(yīng)

目前開展的相關(guān)研究較多針對水體的微生物、藻類、枝角類(或稱“溞類”)及魚類等，且多集中在急性毒害研究。一般來講，抗生素對微生物和藻類產(chǎn)生毒性效應(yīng)的濃度與高營養(yǎng)級生物相比要低2-3個數(shù)量級。研究表明，抗生素對低等水生生物(藻類和微生物)的半數(shù)效應(yīng)濃度(EC50)多在μg·L-1級別[121,122]。例如，Robinson等[123]研究七種喹諾酮類藥物對五種水生生物的影響發(fā)現(xiàn)，其中對藍(lán)細(xì)菌(Microcystis aeruginosa )、浮萍(Lemna minor )和月牙藻(Pseudokirchneriella subcapitata )的EC50分別為49、106和7400 μg·L-1，而在10 mg·L-1范圍內(nèi)對大型溞(Daphnia magna )和黑頭呆魚(Pimephales promelas )無顯著影響。其它研究也顯示，環(huán)境相關(guān)濃度的抗生素對高等水生生物無明顯影響[124,125]。但是也有研究顯示，魚類對大環(huán)內(nèi)酯類藥物比較敏感，其EC50都在100 μg·L-1以下[126,127]。顯然，不同種類的抗生素對同種生物的毒性效應(yīng)差異很大。

盡管抗生素在沉積物和活性污泥中廣泛存在，但是相對于土壤環(huán)境，抗生素對這些環(huán)境中微生物的影響研究較少。由于沉積物和污泥對抗生素有強(qiáng)烈的吸附作用，抗生素可能降低甚至失去其抗菌活性。因此，多數(shù)研究顯示抗生素對沉積物和活性污泥中微生物數(shù)量、活性及群落結(jié)構(gòu)的效應(yīng)濃度較高，都在mg·kg-1或mg·L-1級別[128-131]。

4 環(huán)境中的抗生素抗性基因問題

進(jìn)入環(huán)境中的抗生素除了會造成化學(xué)污染外，還可能會誘導(dǎo)抗性微生物和抗性基因(antibiotics resistance genes，ARGs)的產(chǎn)生，并加速抗生素抗性的傳播和擴(kuò)散。這些抗性微生物可能會通過直接或者間接接觸(如食物鏈)等途徑進(jìn)入人體，增加人體的耐藥性，從而給人類公共健康帶來威脅。自Piuden等[132]首次提出將ARGs作為一種環(huán)境污染物后，對其來源、分布和傳播的研究開始受到人們的重視。

4.1 環(huán)境中ARGs的來源

環(huán)境中ARGs的來源主要有以下兩種：

(1)內(nèi)在抗性 內(nèi)在抗性是指存在于細(xì)菌的基因組上的抗性基因的原型、準(zhǔn)抗性基因或平時沒有表達(dá)的抗性基因[133]。土壤中一些土著微生物本身就能夠產(chǎn)生低濃度的抗生素，這些低濃度抗生素均可作為微生物種群間或種群內(nèi)的信號分子，使微生物可通過隨機(jī)突變或表達(dá)潛在抗性基因而獲得抗性，因此土壤中必然存在著相應(yīng)的ARGs。人類多次從千年凍土篩選到多種ARGs[134-136]，足以證明ARGs早就存在于自然界中，而并非是由于現(xiàn)代臨床治療過程中抗生素的使用而造成。另外，環(huán)境中殘留的抗生素構(gòu)成篩選抗性細(xì)菌的環(huán)境選擇壓力，從而促進(jìn)環(huán)境中ARGs的產(chǎn)生，加速內(nèi)在ARGs突變和水平轉(zhuǎn)移。目前許多研究發(fā)現(xiàn)環(huán)境中的抗生素殘留與抗性基因之間有很好的相關(guān)性[137-138]。

(2) 外源輸入 抗生素主要用于人類醫(yī)療業(yè)和養(yǎng)殖業(yè)，在其腸道內(nèi)誘導(dǎo)出抗藥菌株。從基因水平上看，抗藥菌株都是由于其體內(nèi)基因發(fā)生變異產(chǎn)生ARGs而表現(xiàn)出抗藥性，這些抗性菌株隨糞便排泄進(jìn)入環(huán)境，使其成為環(huán)境中ARGs的重要來源。

醫(yī)用抗生素首先在人體內(nèi)誘導(dǎo)出ARGs，這些ARGs隨糞便菌群排出體外，進(jìn)入醫(yī)療廢水。因此，醫(yī)療廢水中ARGs的檢出率較高，且以人用抗生素對應(yīng)的ARGs種類為主，例如，β-內(nèi)酰胺類[139]、氨基糖苷類[140]和大環(huán)內(nèi)酯類[141]等。

在養(yǎng)殖業(yè)中，抗生素的使用極大地刺激了動物腸道內(nèi)ARGs的發(fā)展。一些研究人員從畜禽糞便中分離出抗性菌株(如糞腸球菌、大腸桿菌等)，并檢測到多種ARGs[142-144]。畜禽糞便施肥是ARGs進(jìn)入土壤環(huán)境的主要途徑。另外，多位研究人員對美國不同地區(qū)養(yǎng)殖場廢水的研究發(fā)現(xiàn)，四環(huán)素和磺胺類抗性基因等廣泛存在于養(yǎng)殖廢水中[138,145,146]。最近，Li等[147]在北京3個地區(qū)的養(yǎng)豬場廢水中檢測出五種喹諾酮類抗性基因(qnrD、qnrS、qepA、oqxA和oqxB)，其絕對濃度在1.66×107～4.06×108copies·mL-1之間。以上研究也發(fā)現(xiàn)，養(yǎng)殖廢水的排放已經(jīng)對周邊納污水體構(gòu)成污染。水產(chǎn)養(yǎng)殖業(yè)中，養(yǎng)殖生物糞便直接排放到水環(huán)境中，使得全球不同地區(qū)水產(chǎn)養(yǎng)殖區(qū)域水體和底泥中均檢測到多種ARGs，且以磺胺類和四環(huán)素類ARGs為主[148-150]。

ARGs可以隨醫(yī)療廢水和動物養(yǎng)殖場污水等進(jìn)入市政污水處理系統(tǒng)，使其成為ARGs聚集的“匯”。然而由于現(xiàn)有的水處理技術(shù)對ARGs沒有明顯的去除效果，國內(nèi)外研究發(fā)現(xiàn)污水出水中仍有相當(dāng)濃度的ARGs存在(表5)。由于處理廠污水與活性污泥間接觸緊密，造成活性污泥中也可檢出多種ARGs(表5)。市政污水處理系統(tǒng)中ARGs通過出水排放及污泥施肥進(jìn)入到水體和土壤環(huán)境，造成受納環(huán)境ARGs污染。

4.2 環(huán)境中AGRs的污染狀況

各類污廢水可通過不同途徑進(jìn)入地表水(海洋、湖泊、河流等)，故在地表水和沉積物已普遍檢測到ARGs。Stoll等[157]研究了24種抗性基因在德國和澳大利亞河流表層水中的分布，他們發(fā)現(xiàn)磺胺類和甲氧芐氨嘧啶抗性基因是最普遍的。Luo等[158]在海河(中國天津)河水和沉積物中檢測出4種磺胺抗性基因(sul1、sul2、sul3、sulA)和7種四環(huán)素抗性基因(tetB、tetM、tetO、tetQ、tetS、tetT、tetW)，沉積物中的抗性基因是水樣中的120～2,000倍。Pei等[159]美國科羅拉多州北部沉積物多處點(diǎn)位檢測到2種抗四環(huán)素基因(tetW，tetO)和兩種磺胺抗性基因(sul1，sul2)。這些研究表明，地表水和沉積物已成為ARGs的庫，并可能加速了ARGs的傳播。

ARGs能夠通過滲透、泄漏等途徑從農(nóng)田或沉積物進(jìn)入地下水。目前，多人從養(yǎng)豬場附近的地下水中檢測到多種四環(huán)素抗性基因[160,161]。如果地下水作為飲用水并很可能將ARGs通過飲水與食物帶入食物鏈，在各個環(huán)境介質(zhì)中傳播轉(zhuǎn)化，可能導(dǎo)致ARGs的全球性污染。

相對于水環(huán)境而言，目前有關(guān)ARGs在土壤環(huán)境中的研究還不系統(tǒng)，但已有研究表明ARGs可通過污水灌溉、施用畜禽糞便或污泥傳播給土壤土著微生物。例如，Dalkmann等[162]墨西哥中部污水灌溉區(qū)域的土壤中ARGs的積累，僅在污水灌溉土壤中發(fā)現(xiàn)qnrS和qnrB，而非灌溉土壤沒有發(fā)現(xiàn)；Schmitt等[163]檢測了豬糞中，以及施用豬糞前后的土壤中的四環(huán)素類抗性基因，通過對比發(fā)現(xiàn)有一部分抗性基因是施肥前的土壤中所沒有的，而是豬糞中特有的，因此可以推斷這部分抗性基因是由豬糞帶入土壤中的。此外，多項研究發(fā)現(xiàn)畜禽養(yǎng)殖場周邊的土壤存在多種ARGs[129,164]，這些研究表明畜禽糞便中的ARGs作為污染源能夠遷移到土壤土著微生物。

目前在醫(yī)院室內(nèi)和養(yǎng)殖場附近的空氣環(huán)境中已分離到多種攜帶ARGs的細(xì)菌。例如，Gilbert等[165]在加拿大一家醫(yī)院的空氣中分離的細(xì)菌中檢測出多種ARGs，其中erm(X)、tet(G)和erm(F)具有較高的檢出率。Sapkota等[166]在大型養(yǎng)豬場室內(nèi)發(fā)現(xiàn)空氣中氣生革蘭氏陽性細(xì)菌具有高水平的多藥物抗性，所有受試菌(腸球菌和鏈球菌)均含有多重對大環(huán)內(nèi)脂類、林可胺類、紅霉素及四環(huán)素的抗性基因，50%的腸球菌和44%的鏈狀球菌含有多重四環(huán)素抗性基因。以上研究表明，空氣中的抗性菌可能是ARGs的儲存庫，吸入這些環(huán)境的空氣是ARGs向人體傳播的一個暴露途徑。

表5 污水處理廠污水和污泥中抗生素抗性基因含量

注：-代表未檢測

Note: -non-detection

5 研究展望

綜上所述，雖然抗生素在環(huán)境中的濃度較低，但其對生態(tài)環(huán)境以及人類健康的潛在危害不容忽視。在過去10年間，隨著各種環(huán)境中ARGs的不斷發(fā)現(xiàn)，ARGs可以在各個環(huán)境介質(zhì)中遷移、轉(zhuǎn)化，并很可能將ARGs帶入食物鏈傳播，最終使ARGs污染具全球性。盡管人們對環(huán)境中的抗生素殘留及其生態(tài)毒性效應(yīng)和ARGs污染情況進(jìn)行了大量的研究，但是仍然存在很多問題需要進(jìn)一步研究：

環(huán)境中抗生素常與其它多種抗菌藥物及有機(jī)無機(jī)污染物(如重金屬、殺蟲劑和多環(huán)芳烴等)共存，但缺乏對以上兩者或三者在環(huán)境介質(zhì)(主要是土壤)中的吸附-解吸、遷移和降解等行為或過程進(jìn)行研究以及其復(fù)合污染的環(huán)境效應(yīng)研究。

盡管現(xiàn)有研究已明確環(huán)境中的抗生素殘留能產(chǎn)生一定的生態(tài)毒性效應(yīng)，但是對它們的效應(yīng)評價缺乏必要的研究，特別是長時間暴露在低劑量的生態(tài)毒性效應(yīng)研究；另外尚缺乏環(huán)境因素對其生態(tài)毒性效應(yīng)影響及其調(diào)控機(jī)理方面的研究。

在不同的環(huán)境介質(zhì)中均發(fā)現(xiàn)多種ARGs，但是應(yīng)該存在更多的ARGs，應(yīng)加強(qiáng)對ARGs檢測方法的研究，并對其ARGs的起源、轉(zhuǎn)化和傳播等研究領(lǐng)域進(jìn)行積極探索。

ARGs作為一種環(huán)境中的新型污染物，對環(huán)境和人類健康的危害日趨明顯，因此我們應(yīng)該積極地尋找措施以降低其危害，例如，在養(yǎng)殖業(yè)中合理使用抗生素，避免經(jīng)驗用藥；研究消除環(huán)境中抗生素及其抗性基因的方法與技術(shù)。

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◆

基金項目：國家自然科學(xué)基金(No. 41173102；31200396)；天津市科技計劃項目(No.12ZCZDSF01400)；天津理工大學(xué)教學(xué)改革項目(YB11-26)；天津市自然科學(xué)基金(No. 14JCQNJC08500)；海洋公益性項目(201005026-05)

作者簡介：葛興彬(1990-)，男，碩士研究生，研究方向為納米毒理學(xué)，E-mail: gexingbin0504@163.com；

*通訊作者(Corresponding author)， E-mail: litielong@nankai.edu.cn

DOI: 10.7524/AJE.1673-5897-20140227004

葛興彬，王振虹，郭楚奇, 等. 納米零價鐵的生態(tài)毒性效應(yīng)研究進(jìn)展[J]. 生態(tài)毒理學(xué)報，2015, 10(3): 28-37

Ge X B, Wang Z H, Guo C Q, et al. Review of the ecotoxicity of nanoscale zero-valent iron [J]. Asian Journal of Ecotoxicology, 2015, 10(3): 28-37

(in Chinese)

The Antibiotic in Environment and Its Ecotoxicity: A Review

Xu Yonggang, Yu Wantai*, Ma Qiang, Zhou Hua, Jiang Chunming

Institute of Applied Ecology, Chinese Academy of Sciences, Shanyang, 110016, China

Received 11 August 2014 accepted 23 October 2014

In recent years, more and more antibiotic drugs were used in the medical treatment, livestock breeding and aquaculture. Since antibiotic drugs could not be completely absorbed by the body of humans and animals, their parent compounds or related metabolites would be returned back to the aquatic and soil environment via urine or faece, causing their residue in environment. Residual antibiotics drugs could lead to the potential environmental risks, of which the most serious one is to induce and spread antibiotic resistance genes (ARGs), subsequently producing threat to human health. This paper mainly described the source, fate and occurrence of antibiotic drugs in the environment, and then we reviewed the ecotoxicity and ARGs caused by antibiotic. In addition, we also pointed out the problems existing in the present studies and prospected the future research work.

antibiotics; ecotoxicity; ARGs

國家科技部支撐計劃項目(2012BAD05B01)和國家自然科學(xué)基金(31100465)

徐永剛(1984-)，男，博士，研究方向為微生物生態(tài)學(xué)，E-mail：xuyonggang1228@163.com；

*通訊作者(Corresponding author)， E-mail: wtyu@iae.ac.cn

10.7524/AJE.1673-5897-20140811001

2014-08-11 錄用日期：2014-10-23

1673-5897(2015)3-011-17

X171.5

A

宇萬太(1965-)，男，研究員，博士生導(dǎo)師，主要研究方向為土壤養(yǎng)分循環(huán)及農(nóng)業(yè)環(huán)境。

徐永剛，宇萬太，馬強(qiáng), 等. 環(huán)境中抗生素及其生態(tài)毒性效應(yīng)研究進(jìn)展[J]. 生態(tài)毒理學(xué)報，2015, 10(3): 11-27

Xu Y G, Yu W T, Ma Q, et al. The antibiotic in environment and its ecotoxicity: a review [J]. Asian Journal of Ecotoxicology, 2015, 10(3): 11-27 (in Chinese)