侯曉鵬,李春華,葉春,許士洪,鄭向勇
1. 中國(guó)環(huán)境科學(xué)研究院,北京 100012
2. 東華大學(xué)環(huán)境科學(xué)與工程學(xué)院,上海 201620
3. 浙江省水環(huán)境與海洋生物資源保護(hù)重點(diǎn)實(shí)驗(yàn)室,浙江 溫州 325035
不同電子受體作用下微生物降解多環(huán)芳烴研究進(jìn)展
侯曉鵬1,2,李春華1*,葉春1,許士洪2,鄭向勇3
1. 中國(guó)環(huán)境科學(xué)研究院,北京 100012
2. 東華大學(xué)環(huán)境科學(xué)與工程學(xué)院,上海 201620
3. 浙江省水環(huán)境與海洋生物資源保護(hù)重點(diǎn)實(shí)驗(yàn)室,浙江 溫州 325035
電子受體作為微生物代謝過程中的必需物質(zhì),對(duì)不同類型微生物的數(shù)量及其代謝能力有重要影響。分析了不同電子受體對(duì)微生物降解多環(huán)芳烴的影響。對(duì)好氧降解(氧氣為電子受體)多環(huán)芳烴微生物種類及降解途徑進(jìn)行了總結(jié);厭氧降解方面,概述了硝酸鹽、硫酸鹽、金屬離子〔Fe(Ⅲ)或Mn(Ⅳ)〕和碳酸鹽為電子受體微生物降解多環(huán)芳烴的研究進(jìn)展。此外,對(duì)微生物降解多環(huán)芳烴的研究存在的問題以及未來的發(fā)展方向進(jìn)行了簡(jiǎn)述與展望。
多環(huán)芳烴;電子受體;微生物降解;降解效率;降解途徑
多環(huán)芳烴(polycyclic aromatic hydrocarbons)是由2個(gè)及以上苯環(huán)以線狀、角狀或簇狀排列而成的芳香族化合物[1-2]。由于其廣泛分布于大氣、水體、植被和土壤中[3],且具有潛在的“三致”效應(yīng)以及生物富集性,多環(huán)芳烴對(duì)農(nóng)產(chǎn)品安全和人類健康構(gòu)成了嚴(yán)重威脅[4-5]。多環(huán)芳烴可能的轉(zhuǎn)化或去除方式有吸收吸附、揮發(fā)、化學(xué)降解、光分解和微生物降解等[6],其中微生物降解被認(rèn)為是最主要和最有效的方法。盡管研究表明大多數(shù)的多環(huán)芳烴均能被微生物降解,但在實(shí)際環(huán)境中其降解速率較慢,主要有2方面原因:1)多環(huán)芳烴的憎水親脂性限制了其傳質(zhì)過程,導(dǎo)致生物利用率降低;2)現(xiàn)有環(huán)境影響因子無法為微生物降解多環(huán)芳烴創(chuàng)造適宜的外部條件。一般認(rèn)為添加表面活性劑〔如十二烷基磺酸鈉(SDS)[7-8]〕能改善多環(huán)芳烴的水溶性,從而使其生物利用率增大。影響多環(huán)芳烴降解的環(huán)境因子(如溫度、pH、營(yíng)養(yǎng)鹽、含氧量、濕度)已被廣泛總結(jié),研究表明:溫度為24~30 ℃,pH為7.0~7.8,C∶N∶P為100∶10∶1,含氧量為10%~40%,濕度為30%~90%時(shí),有利于微生物降解多環(huán)芳烴[9]。然而,從電子受體角度去考察微生物對(duì)多環(huán)芳烴的降解卻鮮有報(bào)道。
氧化還原電位可反映在某一反應(yīng)體系中電子受體得電子的能力,生物體內(nèi)的電子傳遞一般是從氧化還原電位低的物質(zhì)到高的物質(zhì),例如NAD→黃素酶→細(xì)胞色素C系→O2。不同電子受體還原反應(yīng)的氧化還原電位和釋放能量見表1[16-17]。在有氧條件下氧氣優(yōu)先獲得電子;在無氧條件下,硝酸鹽、硫酸鹽、碳酸鹽或CO2、Mn(Ⅳ)、Fe(Ⅲ)等可作為微生物降解多環(huán)芳烴的電子受體[18-22]。在活細(xì)胞中,好氧性細(xì)胞的氧化還原電位高于厭氧性細(xì)胞,氧化還原電位還會(huì)影響酶的活性、細(xì)胞同化能力和微生物的生長(zhǎng)發(fā)育等。環(huán)境中的氧氣是微生物降解多環(huán)芳烴的重要影響因素:1)氧氣的含量決定微生物的群落結(jié)構(gòu);2)由于氧氣的氧化能力強(qiáng),在還原反應(yīng)中釋放的能量多,故好氧微生物對(duì)多環(huán)芳烴的降解效率較高。大多數(shù)厭氧微生物對(duì)電子受體的利用都有單一選擇性,有研究[23]將微生物厭氧降解多環(huán)芳烴的反應(yīng)體系分為反硝化還原反應(yīng)體系(硝酸鹽為電子受體)、硫酸鹽還原反應(yīng)體系(硫酸鹽為電子受體)、金屬還原反應(yīng)體系〔Mn(Ⅳ)和Fe(Ⅲ)等為電子受體〕和產(chǎn)甲烷還原反應(yīng)體系(碳酸鹽或CO2為電子受體)等。無氧條件下微生物降解多環(huán)芳烴對(duì)特定外源電子受體的需求量有最適范圍,電子受體供給量過高或過低都會(huì)對(duì)降解產(chǎn)生抑制作用。此外,不同外源電子受體對(duì)特定微生物厭氧降解多環(huán)芳烴反應(yīng)有不同的促進(jìn)作用[24]。
表1 不同電子受體還原反應(yīng)的氧化還原電位和釋放能量(pH=7)[16-17]
對(duì)好氧條件下微生物降解多環(huán)芳烴已經(jīng)有較廣泛的研究,主要集中在降解菌種的篩選與鑒定、對(duì)多環(huán)芳烴的降解效率及降解條件優(yōu)化、多環(huán)芳烴的降解途徑、多環(huán)芳烴的酶促降解反應(yīng)4個(gè)方面。大量能夠降解多環(huán)芳烴的細(xì)菌、真菌和藻類從土壤和水體底泥中被篩選出,其中發(fā)揮主要作用的是細(xì)菌[25]。常見的好氧微生物有:從毛單胞菌屬(Comamonassp.)[26]、巴氏桿菌屬(Pasteurellasp.)[27]、伯克氏菌屬(Burkholderiasp.)[28]、分枝桿菌屬(Mycobacteriumsp.)[29]、氧化節(jié)桿菌屬(Arthrobacteroxydanssp.)[30]、熱帶根瘤菌屬(Rhizobiumtropicisp.)[31]、克雷伯氏菌屬(Klebsiellasp.)[32]、不動(dòng)桿菌屬(Acinetobactersp.)[6]、假單胞菌屬(Psuedomonassp.)[33]和解環(huán)菌屬(Cycloclasticussp.)[34]等,這些微生物對(duì)不同的多環(huán)芳烴表現(xiàn)出不同的降解效果。一般而言,對(duì)低分子量的多環(huán)芳烴(如萘、蒽、菲、芴等)降解速率較高;對(duì)高分子量的多環(huán)芳烴降解很慢,主要是由于其分子結(jié)構(gòu)復(fù)雜,電子云密度高,很難被氧化,水溶性差,熱穩(wěn)定性強(qiáng)[35]。Guo等[36]從紅樹林底泥中分離出的一株降解菌(PseudomonasSKDOP),7 d內(nèi)對(duì)菲的降解率可達(dá)60%以上,而在14 d的試驗(yàn)期內(nèi)對(duì)芘基本無降解。張杰等[37]在降解菲試驗(yàn)中加入適合濃度的共代謝底物(葡萄糖),發(fā)現(xiàn)混合菌系對(duì)菲的降解速率由67.85%增加到86.34%。
圖1 好氧微生物(真菌和細(xì)菌)降解菲的一般途徑[38]Fig.1 Proposed pathways for phenanthrene degradation by aerobic microorganisms (fungi and bacteria)
好氧降解多環(huán)芳烴的途徑已有較多研究,普遍認(rèn)為是細(xì)菌在雙加氧酶作用下或真菌在單加氧酶作用下,使芳香環(huán)羥基化后,再使之開環(huán)進(jìn)行下一步降解,一般會(huì)形成中間產(chǎn)物——鄰苯二酚或取代鄰苯二酚,然后通過1,2-雙加氧酶催化的鄰裂途徑或者2,3-雙加氧酶催化的間裂途徑裂解開環(huán)進(jìn)入三羧酸循環(huán)(TCA),實(shí)現(xiàn)最終降解。以菲為例[38],真菌對(duì)菲的降解途徑仍不清楚,而細(xì)菌對(duì)菲的降解途徑已有研究。首先在菲雙加氧酶作用下形成順式-3,4-二羥基-3,4-二氫菲,在脫氫酶作用下形成順式-3,4-二羥基菲,隨后在一系列酶作用下轉(zhuǎn)化為1-羥基-2-萘甲酸,不同的菌種會(huì)通過不同的途徑進(jìn)行下一步降解,主要是水楊酸代謝途徑或鄰苯二甲酸代謝途徑或二者都有,最后進(jìn)入TCA循環(huán)降解為CO2和H2O(圖1),降解過程中羥基化碳的初始位置可以不同。好氧降解過程會(huì)產(chǎn)生有毒中間產(chǎn)物,很難被生物利用。Luan等[39]使用紅樹林濕地中富集到的多環(huán)芳烴降解菌群好氧降解芴時(shí),共檢測(cè)到4種單羥基化中間產(chǎn)物(1-羥基芴,2-羥基芴,3-羥基芴及9-羥基芴),但只有9-羥基芴得到較完全降解,最終轉(zhuǎn)化為鄰苯二甲酸,而其他3種中間產(chǎn)物濃度逐漸升高,且無進(jìn)一步降解趨勢(shì)。 在微生物降解多環(huán)芳烴過程中有多種酶參與,目前研究較多的酶有3種,反應(yīng)過程見表2[40]。一些加氧酶作用下產(chǎn)生的中間產(chǎn)物分子量比母體多環(huán)芳烴大,只有部分能被完全轉(zhuǎn)化為無毒、低分子產(chǎn)物,其他大部分仍滯留在環(huán)境中,造成更大的危害。如芘在雙加氧酶作用后形成的二氫二醇芘會(huì)轉(zhuǎn)化成一種更有毒的中間體二醇芘,并造成毒性累積[41]。
表2 3種雙加氧酶反應(yīng)過程
厭氧降解多環(huán)芳烴研究中,以硝酸鹽或硫酸鹽為電子受體的研究相對(duì)較多。Mihelcic等[42]于1988年首次發(fā)現(xiàn)反硝化還原反應(yīng)體系對(duì)萘的降解現(xiàn)象,隨后越來越多能降解多環(huán)芳烴的反硝化菌株或菌群逐漸被分離。Dou等[24]從土壤中分離得到萘降解菌,在厭氧條件下純培養(yǎng)試驗(yàn)發(fā)現(xiàn),合理控制硝酸鹽的投入量能在一定程度上提高對(duì)萘的降解率和降解速率。然而,反硝化還原反應(yīng)體系對(duì)多環(huán)芳烴的降解效率一直有很大爭(zhēng)議。Mihelcic等[42-43]的研究表明多環(huán)芳烴或多或少都有被降解;Lei等[8,44]的研究表明多環(huán)芳烴完全沒有被降解。以硝酸鹽為電子受體的微生物降解多環(huán)芳烴研究主要集中在低分子多環(huán)芳烴,對(duì)4環(huán)以上的高分子多環(huán)芳烴的降解鮮有報(bào)道。Mcnally等[45]以硝酸鹽為電子受體在嚴(yán)格的厭氧純培養(yǎng)條件下發(fā)現(xiàn),不同多環(huán)芳烴的降解速率依次為蒽>菲>芘,說明厭氧條件下多環(huán)芳烴的降解難易程度與好氧條件下一致。
由于硫酸鹽廣泛存在于各類自然環(huán)境中,以硫酸鹽為電子受體的還原反應(yīng)體系對(duì)多環(huán)芳烴的降解更普遍。研究發(fā)現(xiàn)[20,46]添加硫酸鹽可以加強(qiáng)環(huán)境中微生物對(duì)多環(huán)芳烴的去除效果,并且相較其他電子受體,硫酸鹽為電子受體時(shí)微生物對(duì)多環(huán)芳烴的降解效率最高。Hayes等[47]在研究硫酸鹽還原反應(yīng)體系對(duì)多環(huán)芳烴的降解時(shí),添加硫酸鹽抑制劑導(dǎo)致多環(huán)芳烴不再被降解,從而說明硫酸鹽是降解的關(guān)鍵因素。硫酸鈣是硫酸鹽還原反應(yīng)體系中最佳的電子受體,主要因?yàn)榱蛩徕}水溶性低,在環(huán)境中不會(huì)形成較高的鹽度而抑制細(xì)菌的活性。不同濃度的硫酸鹽對(duì)降解多環(huán)芳烴也有影響,一般最佳濃度為10~50 mmolL,目前普遍采用的濃度為20 mmolL。Rothermich等[48]在研究海洋沉積物中的多環(huán)芳烴降解時(shí),用14C標(biāo)記法首次發(fā)現(xiàn)硫酸鹽還原反應(yīng)體系下對(duì)苯并[a]芘的降解,同時(shí)發(fā)現(xiàn)高分子多環(huán)芳烴的降解速率低于低分子多環(huán)芳烴。以硫酸鹽為電子受體時(shí)降解多環(huán)芳烴產(chǎn)生的中間產(chǎn)物比氧氣為電子受體時(shí)更簡(jiǎn)單、毒性更小且分解更完全[49-50]。Tsai[51]對(duì)芴的降解產(chǎn)物研究中沒有發(fā)現(xiàn)高分子中間產(chǎn)物,而是大量低分子苯酚,且很快完全轉(zhuǎn)化為CO2和H2O(圖2)。Zhang等[52]在產(chǎn)硫菌群對(duì)萘和菲的厭氧降解研究中提出,羧基化可能是該系統(tǒng)降解反應(yīng)的第一步,并用14C標(biāo)記法證明萘和菲最終被降解為CO2。
圖2 硫酸鹽為電子受體下微生物對(duì)芴的降解途徑[51]Fig.2 Biodegradation pathways of fluorene with amendment of sulfate
目前對(duì)于金屬離子作為電子受體的微生物降解多環(huán)芳烴的研究較少,主要集中在Fe(Ⅲ)和Mn(Ⅳ)的研究上。研究表明[43,53],添加高濃度Fe(Ⅲ)有利于降解多環(huán)芳烴,特別是5環(huán)和6環(huán)的多環(huán)芳烴。Fe(Ⅲ)的形式對(duì)降解多環(huán)芳烴也有影響,Kraig[53]研究表明,磷酸鐵(FePO4)對(duì)大多數(shù)微生物降解多環(huán)芳烴有抑制作用,而檸檬酸鐵則沒有。Li等[18]的研究發(fā)現(xiàn),在硫酸鹽非常豐富時(shí),添加Fe(Ⅲ)對(duì)微生物厭氧降解4種多環(huán)芳烴(芴、菲、熒蒽和芘)并無顯著影響,這或許是因?yàn)樵摥h(huán)境下硫酸鹽的得電子能力高于Fe(Ⅲ)。
對(duì)于Mn(Ⅳ)為電子受體的微生物降解多環(huán)芳烴鮮有報(bào)道,可能是由于Mn(Ⅳ)容易被多種自然存在的有機(jī)污染物所利用,而不是被Mn還原菌利用[12]。僅有的研究結(jié)果也不統(tǒng)一:有研究表明[12],Mn(Ⅳ)對(duì)微生物厭氧降解萘有一定作用,而對(duì)芘沒有顯著影響;也有研究表明[54],Mn(Ⅳ)對(duì)微生物降解芴、菲、熒蒽和芘有顯著的抑制作用。這可能是由于降解菌種的不同所致,有的菌種能利用Mn(Ⅳ)促進(jìn)自我生長(zhǎng),而有的菌種會(huì)受到Mn(Ⅳ)的毒害而被抑制生長(zhǎng)。
某些產(chǎn)甲烷菌在厭氧還原體系中具有一定降解或者促進(jìn)其他厭氧微生物降解多環(huán)芳烴的能力。由于產(chǎn)甲烷菌廣泛分布于高有機(jī)碳負(fù)荷的還原環(huán)境中(氧化還原電位為-600~-200 mV),其在多環(huán)芳烴的生物修復(fù)中起著重要作用。產(chǎn)甲烷還原反應(yīng)體系下降解多環(huán)芳烴的研究并不深入細(xì)致,大多集中在對(duì)低分子多環(huán)芳烴的研究[14,55],該反應(yīng)體系中高分子多環(huán)芳烴沒有減少或消失[46,53]。Chang等[56]以萘和菲為降解對(duì)象研究產(chǎn)甲烷和厭氧降解之間的聯(lián)系時(shí),通過添加產(chǎn)甲烷抑制劑發(fā)現(xiàn)多環(huán)芳烴降解被部分抑制,從而證明產(chǎn)甲烷在厭氧降解多環(huán)芳烴過程中發(fā)揮重要作用。Genthner等[55]在研究被木溜油污染的底泥中的多環(huán)芳烴時(shí),添加CO2碳酸氫鹽緩沖作為電子受體,發(fā)現(xiàn)有甲烷產(chǎn)生并且多環(huán)芳烴有一定程度的去除,但4環(huán)和5環(huán)的多環(huán)芳烴沒有被降解。產(chǎn)甲烷還原反應(yīng)體系降解萘的途徑(圖3)[57]與單環(huán)烴相似。Chang等[20,58]對(duì)5種多環(huán)芳烴在不同厭氧還原反應(yīng)體系下研究表明:對(duì)多環(huán)芳烴降解效果的促進(jìn)作用由強(qiáng)到弱依次為硫酸鹽還原反應(yīng)體系>產(chǎn)甲烷還原反應(yīng)體系>硝酸鹽還原反應(yīng)體系;微生物對(duì)多環(huán)芳烴的降解速率常數(shù)由高到低依次為菲>芘>蒽>芴>苊。然而,Li等[59]研究表明,添加NaHCO3對(duì)紅樹林底泥中微生物降解多環(huán)芳烴無促進(jìn)作用,這可能是由于紅樹林底泥中其他電子受體濃度較高所致。
圖3 產(chǎn)甲烷還原反應(yīng)體系降解萘的途徑[57]Fig.3 Methane-producing degradation pathways of naphthalene
近年來,以氧氣為電子受體對(duì)多環(huán)芳烴的微生物降解(即好氧降解)研究廣泛,主要集中在好氧菌種的篩選、多環(huán)芳烴的降解速率及影響因素、降解途徑和降解的酶系4個(gè)方面。而無氧條件下的微生物降解多環(huán)芳烴研究相對(duì)薄弱,主要是以硝酸鹽和硫酸鹽為電子受體的厭氧降解,以Fe(Ⅲ)和Mn(Ⅳ)為電子受體的研究較少。不同外源電子受體對(duì)多環(huán)芳烴降解促進(jìn)效果不同,無氧條件下對(duì)不同多環(huán)芳烴降解的難易程度與好氧條件下一致。多環(huán)芳烴的好氧降解速率較厭氧降解高,二者的降解途徑也不同,好氧降解產(chǎn)生有毒大分子中間產(chǎn)物,并滯留在環(huán)境中,而厭氧降解多生成小分子低毒易降解中間產(chǎn)物。
對(duì)多環(huán)芳烴的微生物降解存在以下關(guān)鍵問題,需進(jìn)一步研究。
(1)不同電子受體下的多環(huán)芳烴厭氧降解菌較少,降解途徑目前還不十分清楚,故需加大對(duì)厭氧高效降解菌種的篩選,系統(tǒng)研究和總結(jié)不同電子受體下微生物厭氧降解多環(huán)芳烴的途徑。
(2)厭氧條件廣泛存在于水體底泥和土壤深處,深入研究厭氧環(huán)境下的多環(huán)芳烴降解影響因素從而優(yōu)化降解條件,對(duì)采用工程方法去除環(huán)境中多環(huán)芳烴有重要意義。
(3)多環(huán)芳烴好氧降解會(huì)產(chǎn)生有毒、難降解的中間產(chǎn)物,其滯留在環(huán)境中可能造成更大的危害,對(duì)該類中間產(chǎn)物的研究將成為關(guān)注的熱點(diǎn)。
(4)合理構(gòu)建內(nèi)部厭氧降解菌種與外部好氧降解菌種共存的菌膠團(tuán)結(jié)構(gòu),將好氧降解的高效率與厭氧降解終產(chǎn)物的低毒易分解相結(jié)合,為實(shí)際工程中多環(huán)芳烴的高效生物修復(fù)應(yīng)用奠定理論基礎(chǔ)。
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Research Progress of Biodegradation of Polycyclic Aromatic Hydrocarbons with Amendment of Different Electron Acceptors
HOU Xiaopeng1,2, LI Chunhua1, YE Chun1, XU Shihong2, ZHENG Xiangyong3
1.Chinese Research Academy of Environmental Sciences, Beijing 100012, China 2.School of Environmental Science and Engineering, Donghua University, Shanghai 201620, China 3.Zhejiang Provincial Key Lab for Water Environment and Marine Biological Resources Protection, Wenzhou 325035, China
As an essential material in microbial metabolism, the electron acceptors have a very important impact on the number of microorganisms of various types and their ability to biodegrade polycyclic aromatic hydrocarbons (PAHs). The impact of different electron acceptors on the microbial degradation of PAHs was analyzed. The microorganism types and degradation approaches of aerobic biodegradation, with oxygen as electron acceptor, were summarized. In terms of anaerobic biodegradation, a review of research progress was provided for different electron acceptors such as nitrate, sulfate, Fe(Ⅲ) or Mn(Ⅳ) and carbonate. The existing problems in the research on microbial degradation of PAHs were briefed and the prospects of future development provided.
polycyclic aromatic hydrocarbon; electron acceptor; biodegradation; degradation efficiency; degradation pathway
侯曉鵬,李春華,葉春,等.不同電子受體作用下微生物降解多環(huán)芳烴研究進(jìn)展[J].環(huán)境工程技術(shù)學(xué)報(bào),2016,6(1):78-84.
HOU X P, LI C H, YE C, et al.Research progress of biodegradation of polycyclic aromatic hydrocarbons with amendment of different electron acceptors [J].Journal of Environmental Engineering Technology,2016,6(1):78-84.
2015-07-09
國(guó)家自然科學(xué)基金項(xiàng)目(41101487);浙江省亞熱帶水環(huán)境與海洋生物資源保護(hù)重點(diǎn)實(shí)驗(yàn)室開放基金項(xiàng)目
侯曉鵬(1990—),男,碩士,主要從事水環(huán)境污染化學(xué)研究,hxp103@sina.cn
李春華(1977—),女,副研究員,博士,主要從事環(huán)境微生物、生態(tài)健康評(píng)價(jià)、水體生態(tài)修復(fù)研究,lich@craes.org.cn
X172
1674-991X(2016)01-0078-07
10.3969j.issn.1674-991X.2016.01.012