張海涵,王 躍,黃廷林,赫慧艷,王 玥,張夢瑤

沉積物電纜細菌研究進展

張海涵*,王 躍,黃廷林,赫慧艷,王 玥,張夢瑤

(西安建筑科技大學,陜西省環(huán)境工程重點實驗室,西北水資源與環(huán)境生態(tài)教育部重點實驗室,陜西 西安 710055)

目前,在沉積物中發(fā)現(xiàn)一種絲狀多細胞微生物—電纜細菌,該菌屬于變形菌門的脫硫球莖菌科(Desulfobulbaceae).電纜細菌通過遠距離電子傳輸將沉積物表面的氧還原與深處缺氧層的硫化物氧化電耦合進行完整的氧化還原反應,調(diào)節(jié)氧分子和硫化物遷移轉(zhuǎn)化.電纜細菌有3種連接方式,表層存在脊段結構進行電子運輸,并在富含硫酸鹽和季節(jié)性周期變化的自然環(huán)境中廣泛存在.這種新型的多細胞合作方式對沉積物的生物地球化學循環(huán)產(chǎn)生顯著影響,促進沉積物硫化區(qū)鐵錳的溶解,并抑制硫和磷等元素的釋放.此外,電纜細菌參與硫化物和烴類污染物的降解,為污染沉積物生物修復領域提供新的研究方向.本文對電纜細菌的發(fā)現(xiàn)、生理代謝、棲息環(huán)境以及生物地球化學循環(huán)的影響等研究進行了綜述.

電纜細菌；遠距離電子傳輸；氧化還原反應；生物地球化學循環(huán)

多細胞生物是地球生物圈重要組成部分[1-3].其一個基本特征是能有效的利用能量并維持細胞功能[4].他的胞外電子傳輸方式包括:細胞的直接接觸[6-7];利用可溶性氧化還原電子穿梭體[8-11];“納米導線”(鐵氧化菌的菌毛)直接將細胞外電子轉(zhuǎn)移到固體基質(zhì)并有效進行電子長距離的運輸[12-17].這3種方式廣泛存在于土壤、沉積物和活性污泥等環(huán)境中,并應用于微生物修復和重金屬還原等方面[18].然而,最近在海洋沉積物中,發(fā)現(xiàn)一種新型多細胞合作方式,即細胞間通過電流的方式合作以提供能量、發(fā)揮生態(tài)功能[19].

生物地球化學循環(huán)的主要能量由生物體的氧化還原反應直接或間接提供[20].氧化還原作用會導致沉積物表層出現(xiàn)高度氧化的環(huán)境,該環(huán)境中富含的有機質(zhì)、硫化物和甲烷等還原產(chǎn)物可作為電子供體,而微生物體內(nèi)C、N、Mn、Fe、S和P等元素的氧化形式作為電子受體[21-28].傳統(tǒng)的氧化還原反應在同一局部環(huán)境中需要同時提供電子供體和電子受體[29].然而,多細胞合作的長絲狀電纜細菌可在厘米級的距離產(chǎn)生并傳遞電子,在不同空間分別進行氧化半反應和還原半反應[19].電纜細菌參與沉積物中元素的生物地球化學循環(huán),促進沉積物底部鐵錳的溶解,在水-沉積物界面積累鐵錳氧化物,抑制硫和磷的釋放.并對污染物(硫化物和烴類化合物)的遷移降解也發(fā)揮重要作用.此外,電纜細菌棲息環(huán)境廣泛,在海洋、湖泊和紅樹林等自然環(huán)境中均發(fā)現(xiàn)其的存在.電纜細菌不僅為微生物生態(tài)學的研究提供了新方向,并在生物修復、生物電等應用領域有著巨大潛力.因此,本文對沉積物中電纜細菌的生長繁殖、能量傳輸及棲息環(huán)境等研究進行綜述.

1 電纜細菌的長距離電子傳輸

1.1 長距離電子傳輸(LDET)

Nielsen等[19]將奧爾胡斯海岸沉積物與上覆水培養(yǎng).揭示沉積物表面存在一個較窄的有氧區(qū).隨后是1.5cm的次氧區(qū),最后是黑色硫化物沉淀形成低硫化區(qū).此外,實驗中觀察到pH值垂向變化顯著,其在沉積物表面的有氧區(qū)達到峰值,在次氧區(qū)和硫化區(qū)急劇下降.按照常規(guī)的好氧沉積過程,與氧分子發(fā)生的反應是在中性或者pH值下降的環(huán)境中,所以對于實驗中pH值異常變化,只能由電化學氧化還原解釋(圖1).陰極位于表層有氧區(qū),氧氣的還原半反應消耗H+;陽極位于硫化區(qū),游離硫化氫(H2S)通過氧化半反應被消耗,為了使這種空間分離的半反應發(fā)生,電纜細菌將陽極硫化物氧化產(chǎn)生的電子運輸?shù)疥帢O進行還原反應,相隔很遠的細胞能協(xié)同進行氧化還原反應,這是由LDET驅(qū)動的好氧硫化物參與的電氧化反應(e-SO)[30].

圖1 電纜細菌的LDET

1.2 電纜細菌的發(fā)現(xiàn)

LDET被發(fā)現(xiàn)時,一些學者推測其是通過細菌納米導電線、腐殖質(zhì)顆粒和半導電礦物傳遞電子[8,11,14].然而,在2012年,Pfeffer等[30]證明電流是由生物介導的:一種絲狀多細胞的e-SO與LDET密切相關,間隙水中O2、H2S和pH值垂向偏移現(xiàn)象表明氧分子還原反應和硫化物氧化反應在空間上是分離的.e-SO在沉積物中傳遞電子時,會產(chǎn)生相應的電場,從而驅(qū)動間隙水中的離子移動以維持電荷平衡,這揭示了沉積物可以提供電活性環(huán)境[31-32].

實驗進一步表明,電子傳遞是在電纜細菌內(nèi)部發(fā)生的,而不是通過分子擴散或者可溶性電子穿梭體的偶然接觸.實驗中在有氧-缺氧界面下1~2mm處水平穿過一根鎢絲(直徑50mm),有氧區(qū)pH值峰值在1h后變得不明顯,同時氧氣和硫化物的消耗量顯著下降[30].Nielsen等[19]也通過改變上覆水中氧分子濃度發(fā)現(xiàn)沉積物中硫化氫濃度在有氧區(qū)以下迅速變化(1h內(nèi)),這遠快于分子擴散的速度.將孔徑2μm的過濾器插入沉積物中心,沉積物中出現(xiàn)明顯的LDET特征,而0.8μm孔徑中的沉積物則未發(fā)現(xiàn)該現(xiàn)象,表明電子傳遞需要細菌大小的物質(zhì)介導.最后當非導電玻璃微球?qū)哟?mm厚的沉積物層時也發(fā)生了LDET,表明沉積物顆粒不是電子運輸?shù)闹匾橘|(zhì).這些實驗均間接的為LDET是由電纜細菌內(nèi)部介導的觀點提供了科學支撐.

然而,電纜細菌通過菌絲傳輸電子的現(xiàn)象仍然缺乏直接證據(jù)證明.直到Bjerg等[33]檢測單個絲狀體細胞色素氧化還原電位梯度.當在缺氧或激光切割絲狀菌體時該梯度立即消失,電子受體失效,細胞色素明顯減少,所以細胞色素氧化還原狀態(tài)的迅速變化必須依賴于從硫化物區(qū)到有氧區(qū)的電子傳輸.這為電纜細菌遠距離電子傳遞提供了直接證據(jù).

1.3 電纜細菌電子傳遞結構

確定電纜細菌的導電結構和機理不僅加深對電纜細菌的認識,還可以進一步擴展生物電的應用.在掃描電鏡下觀察,電纜細胞外表面結構獨特,沿著電纜細菌的軸存在均勻的脊狀結構[30].絲狀體相鄰的細胞被200nm寬的間隙隔開,間隙由脊狀物填充橋接而成,并被外膜緊緊包裹,一般有15~58個標記脊(圖2),外觀上類似于電纜,脊段結構表面存在弦(strings)充當“導電線”,電子在其內(nèi)部的周質(zhì)空間傳遞,并具有顯著的極化性或電荷存儲能力,并且是連接多個細胞的關鍵結構.這些弦引導電子穿過細胞間交界處,加強了節(jié)點的連接.弦與弦之間相互纏繞呈二聚體結構,提高電纜細菌穩(wěn)定性,也是電纜細菌抵抗外界壓力和保持厘米長度的必要結構[34].

圖2 電纜細菌形態(tài)示意

2 電纜細菌的生理特性

2.1 電纜細菌的代謝

Schauer等[35]基于熒光原位雜交(FISH)監(jiān)測電纜細菌密度以探究電纜細菌的代謝途徑和增殖速率,結果表明絲狀菌生長過程中的菌直徑在垂向無明顯變化,在所有時間點和不同的沉積物層中均可以觀察到沿整個細絲的細胞分裂的不同階段,細菌是連續(xù)分裂的.在21d絲狀菌密度達到最大(2km/cm2),間隙水的化學特征完全顯現(xiàn).隨著時間的變化(21~53d),電纜細菌的密度和活性大幅度下降,可能是由于次氧區(qū)的FeS耗盡[36].Jiang等[34]提出了一個模型來表示細胞分裂的不同階段(圖3)也是絲狀菌不同類型的連接方式(J1、J2和J3).J2出現(xiàn)在細胞復制時期,分裂的細胞從中間開始膨脹,形成一個新的連接J2,隨著細胞分裂,當兩個細胞之間形成細胞膜時,過渡型的連接J3出現(xiàn),在分裂將要結束時,兩個新的細胞形成,菌絲伸長,J2收縮形成J1連接,J1和J2交替出現(xiàn).根據(jù)細胞分裂模型,所有細胞的分裂是均勻連續(xù)的.

電纜細菌能夠在幾天內(nèi)大量繁殖,這意味著它有高效的碳固定方式.Vasquez-Cardena等[37]通過納米級次級離子質(zhì)譜法(NanoSIMS)和磷脂衍生脂肪酸穩(wěn)定同位素探針法(PLFA-SIP)用13C標記丙酸和碳酸氫鹽結合細菌脂肪酸來研究電纜細菌的代謝方式,表明電纜細菌與化能無機自養(yǎng)生物密切相關,e-SO是由化能有機型電纜細菌、化能自養(yǎng)型ε-變形菌和丙型變形菌共同完成.然而,對這兩組代謝類型之間的聯(lián)系還有待進一步研究.

圖3 電纜細菌的3種連接方式

2.2 電纜細菌的能動性

電纜細菌的演替通常是快速增長到種群密度峰值,根據(jù)電纜細菌生長及增殖表明,細胞分裂并具有能動性才能使菌絲向下延伸.Malkin等[38]研究電纜細菌與光合藻類生物膜的關系時,發(fā)現(xiàn)在明暗交替的狀態(tài)下培育沉積物,深部硫化物濃度隨光/暗周期的變化呈規(guī)律性循環(huán).所以Malkin假設電纜細菌是運動的,并且隨氧化還原梯度的變化進行移動.Bjerg[39]等利用時差顯微成像技術觀察到電纜細菌通常是沿著菌絲的軸線滑行運動,但是部分電纜細菌有時會反向運動.當電纜細菌的末端滑動遇到障礙停留,菌絲繼續(xù)移動從而成環(huán),或者不同的菌絲反向運動,形成環(huán)狀凸起.電纜細菌群體中有3種運動狀態(tài):不運動(22%),末端直線滑動(35%)和環(huán)狀滑動(43%).通過了解電纜細菌的運動不僅揭示了其在環(huán)境中的作用,還加深了對電纜細菌生態(tài)作用的理解.

2.3 電纜細菌的系統(tǒng)發(fā)育分析

目前發(fā)現(xiàn)的所有電纜細菌均屬于脫硫球莖菌(Desulfobulbaceae),它們確切的系統(tǒng)發(fā)育分類尚不明確,因為大多數(shù)研究只通過16S rRNA序列測序,依靠絲狀形態(tài)鑒定或利用Desulfobulbaceae探針熒光原位雜交進行鑒定[32].Trojan等[40]從淡水和海洋沉積物中獲取電纜細菌,對16S rRNA和AB基因序列進行全基因組擴增、測序,并構建電纜細菌16S rRNA基因序列的環(huán)境分布.電纜細菌16S rRNA基因序列可按相似性分為2個屬水平,6個不同的種水平.2個新增的屬分別為(來自海洋)和Candidatus(來自淡水). Candidatus附屬4個種,分別為:,,,和; Candidatus附屬2個種,分別為:,和.對含有分離亞硫酸鹽還原酶的全部或部分AB基因的系統(tǒng)發(fā)育分析也得到了相同分組.目前,對于LDET是否局限于電纜細菌,會不會存在于不同種類的微生物中,如光合菌,化能自養(yǎng)菌等還有待進一步深入探究.

3 電纜細菌棲息環(huán)境

電纜細菌在各種自然環(huán)境的沉積物中被發(fā)現(xiàn),其中以富含硫酸鹽、季節(jié)性周期變化和缺少生物強烈擾動等特征的海岸地區(qū)為主[41,49].目前發(fā)現(xiàn)的棲息地包括鹽沼[41-43]、紅樹林[44]、海岸潮間帶[45]、海岸淤泥堆積地[46]和季節(jié)性缺氧湖泊[47-48].此外,最近在淡水湖,半咸水水域沉積物中也發(fā)現(xiàn)電纜細菌的存在[50-51](表1),有關水源水庫沉積物電纜細菌的研究未見報道.

表1 電纜細菌棲息環(huán)境

4 電纜細菌對生物地球化學循環(huán)的影響

4.1 電纜細菌對沉積物中鐵錳鈣元素影響

e-SO對水體-沉積物生物地球化學循環(huán)有顯著影響,電纜細菌通過調(diào)控硫循環(huán)[46,49]、磷循環(huán)[52]、錳循環(huán)和鐵循環(huán)[47,53],從而影響季節(jié)性缺氧環(huán)境的生態(tài)系統(tǒng)功能.主要機理為e-SO生成硫酸鹽同時生成質(zhì)子H+,導致沉積物缺氧層中硫化鐵和碳酸鈣溶解,Ca2+、Fe2+和SO42-向孔隙水流動,由于沉積物中40%以上的氧分子參與質(zhì)子H+的電化學反應,陰極部分有氧區(qū)呈堿性,所以Fe2+向上擴散到有氧區(qū)形成FeOOH,Ca2+在氧區(qū)沉淀為CaMg(1-x)CO3[60]. e-SO導致溶解的Mn2+和Fe2+在深處釋放,而錳和鐵的氧化物富集在沉積物表面附近.電纜細菌的代謝造成表層沉積物中形成FeOOH,隨后作為夏季沉積物中游離硫化物的緩沖物,延遲euxinia在水底的發(fā)生,類似“防火墻”的作用[54].電纜細菌的種群動態(tài)變化,也會誘導沉積物鐵?磷的季節(jié)性變化.春季,在電纜細菌的作用下鐵氧結合磷大量存在,夏季缺氧,氧化鐵耦聯(lián)的磷被釋放出來,水中磷含量大大增加[52].

4.2 電纜細菌對沉積物中微量元素循環(huán)的影響

e-SO導致孔隙水中pH值偏移,從而影響對pH值敏感的礦物質(zhì)(硫化物和碳酸鹽)循環(huán)[60].此外, e-SO對沿海沉積物中微量金屬的早期成巖作用也有影響.微量元素砷和鈷可吸附在硫化物沉淀上,當e-SO使孔隙水酸化后,硫化鐵的溶解使微量元素釋放出來向上擴散,在上覆水富集[61].沉積物中的鉬主要來源有:鐵氧化物和氫氧化物顆粒表面富集攜帶;上覆水中在硫化物作用下形成的硫代鉬酸鹽的釋放[62-64].電纜細菌的代謝引起錳碳酸鹽和FeS的溶解,從而間接影響鉬動力學,擴大了鉬的季節(jié)性變化[62].

4.3 電纜細菌對污染物遷移轉(zhuǎn)化的影響

電纜細菌不僅改變水-沉積物的生物地球化學特征,參加元素循環(huán),在微生物修復和污染物遷移轉(zhuǎn)化方面也值得深入研究.Malkin等[45]證明藍貝、牡蠣等生物依靠微生物e-SO來阻止硫化物在鰓表面的吸收擴散,因此,電纜細菌可能是雙殼類礁沉積物解毒的關鍵.硫酸鹽是沉積物中重要氧化劑,石油烴類在硫酸鹽還原作用下降解.在受污染的海洋沉積物缺氧區(qū),通過電纜細菌的作用硫化物氧化形成硫酸鹽促進石油烴類氧化生物降解[57].綜上,電纜細菌對生物地球化學循環(huán)的影響與硫化物的溶解、沉淀有密切聯(lián)系.

5 電纜細菌在污染沉積物修復中的應用

沉積物中的污染物可作為電纜細菌的代謝過程中的電子供受體,從而降解污染物,驅(qū)動沉積物生物修復[65-66].電纜細菌利用氧分子和硝酸鹽作為電子受體,硫化物是e-SO過程中的電子供體.有毒硫化物損害植物根系,在電纜細菌的代謝活動下硫化物濃度降低,改善海洋沉積物植物根系的環(huán)境[58];在季節(jié)性缺氧環(huán)境中,電纜細菌參與鐵錳循環(huán),在沉積物表層形成”保護殼”,延緩硫化物的釋放,增強化學自養(yǎng)菌群活性[37],此外,鐵錳氧化物形成減少沉積物向水中鐵錳磷的釋放通量[55];電纜細菌調(diào)控硫循環(huán)參與烴類污染物(甲苯、石油)的降解[57].微生物利用電子受體大量繁殖,電纜細菌也可以將硝酸鹽的還原與硫化物的氧化耦合[56],可通過生物刺激方式激活電纜細菌,促進污染物的降解速率.

目前,由于電纜細菌研究尚在探索階段,沉積物電纜細菌還未成功富集分離純培養(yǎng);硝酸鹽循環(huán)機制未明確;電纜細菌與其他微生物是否存在促進或競爭關系等問題,均限制了電纜細菌在污染沉積物生物修復工程中的應用.

6 展望

目前,對水環(huán)境沉積物電纜細菌的研究尚在初期階段,還有頗多未知問題有待深入探索:(1)有關沉積物電纜細菌菌株基因組的測定;(2)電纜細菌如何在運動中協(xié)調(diào)氧分子和硫化物代謝轉(zhuǎn)化;(3)上覆水中氧分子濃度的準確閾值與菌株豐度的關系;(4)電纜細菌在深水型(高靜水壓)貧營養(yǎng)水源水庫沉積物中是否存在,及其在水源水庫水質(zhì)演變過程中的代謝調(diào)控機制尚不明確(尤其是季節(jié)性物理熱分層的作用機制);(5)人工外源增氧(如揚水曝氣技術)調(diào)控水源水庫“沉積物-水”界面驅(qū)動表層沉積物中電纜細菌豐富、組成代謝活性機制尚需探索.綜上,在水環(huán)境微生物生態(tài)研究和污染生態(tài)修復工程領域,對特殊生境沉積物中電纜細菌的深度研究,將驅(qū)動沉積物微生物生態(tài)學發(fā)展,并且為污染沉積物微生物菌劑修復領域提供嶄新的方向.

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Research progress of cable bacteria in sediment.

ZHANG Hai-han*, WANG Yue, HUANG Ting-lin, HE Hui-yan, WANG Yue, ZHANG Meng-yao

(Key Laboratory of Northwest Water Resources and Environment, Ministry of Education, Shaanxi Key Laboratory of Environmental Engineering, Xi’an University of Architecture and Technology, Xi’an 710055, China)., 2019,39(7)：3048~3055

Recently, a novel multicellular filamentous microbe named as cable bacteria was observed in sediments, which belong to Desulfobulbaceae of proteobacteria. Cable bacteria conducedted complete redox reaction by coupling oxygen reduction on sediment surface with sulfide oxidation in deep anoxic layer through long-distance electron transport. Cable bacteria had three connection modes and surface ridge structure for electronic transport. It existed widely in natural environment rich in sulfate and seasonal periodic variation. This new multicellular cooperation mode had a significant impact on the biogeochemical cycle of sediments, which promoted the dissolution of iron and manganese in sulphide areas of sediments, and inhibited the release of sulfur and phosphorus. Moreover, cable bacteria was involved in the degradation of sulfide and hydrocarbon pollutants, and providing a new research direction in the field of bioremediation of contaminated sediments. Here, the discovery, physiological metabolism, habitat environmental conditions and biogeochemical cycle of cable bacteria were reviewed systematically.

cable bacteria；long-distance electron transport；redox reaction；biogeochemical cycles

X524

A

1000-6923(2019)07-3048-08

張海涵(1981-),男,陜西西安人,副教授,博士,主要研究方向為水環(huán)境微生物群落結構.發(fā)表論文50余篇.

2018-12-16

國家重點研發(fā)計劃(2016YFC0400706);陜西省國際科技合作計劃項目(2018KW-011);國家級大學生創(chuàng)新創(chuàng)業(yè)項目(201809023)

* 責任作者, 副教授,zhanghaihan@xauat.edu.cn