#These authors contributed equally to this work.
芳香族化合物是一类具有苯环结构的有机物,它们结构稳定,不易分解,并可通过食物链进行生物富集和生物放大,对生态环境及人类健康造成极大危害。细菌具有超强的分解代谢能力,能降解多环芳烃(polycyclic aromatic hydrocarbons, PAHs)等多种难降解芳香族污染物。吸附和转运是细菌进行芳香族化合物细胞内代谢的前提。虽然芳香族化合物的细菌降解已取得较为显著的研究进展,但吸附和转运机理仍不甚清楚。本文讨论了细菌对芳香族化合物的吸附有积极作用的细胞表面疏水性、生物被膜形成和细菌趋化性等影响因素,总结了FadL家族、TonB依赖性受体蛋白、OmpW家族等外膜转运系统和主要协同转运蛋白超家族(major facilitator superfamily, MFS)转运体、ATP结合盒(ATP-binding cassette, ABC)转运蛋白等内膜转运系统对该类化合物跨膜运输作用,并对跨膜转运机制进行了讨论和阐述,旨在为芳香族污染物的防控和治理提供一定理论参考。
Aromatic compounds are a class of organic compounds with benzene ring(s). Aromatic compounds are hardly decomposed due to its stable structure and can be accumulated in the food cycle, posing a great threat to the ecological environment and human health. Bacteria have a strong catabolic ability to degrade various refractory organic contaminants (e.g., polycyclic aromatic hydrocarbons, PAHs). The adsorption and transportation are prerequisites for the catabolism of aromatic compounds by bacteria. While remarkable progress has been made in understanding the metabolism of aromatic compounds in bacterial degraders, the systems responsible for the uptake and transport of aromatic compounds are poorly understood. Here we summarize the effect of cell-surface hydrophobicity, biofilm formation, and bacterial chemotaxis on the bacterial adsorption of aromatic compounds. Besides, the effects of outer membrane transport systems (such as FadL family, TonB-dependent receptors, and OmpW family), and inner membrane transport systems (such as major facilitator superfamily (MFS) transporter and ATP-binding cassette (ABC) transporter) involved in the membrane transport of these compounds are summarized. Moreover, the mechanism of transmembrane transport is also discussed. This review may serve as a reference for the prevention and remediation of aromatic pollutants.
芳香族化合物是指分子中含有苯环的有机化合物,包括苯、多环芳烃(polycyclic aromatic hydrocarbons, PAHs)等芳香烃及其衍生物。煤、焦油、石油和天然气、烟草或烟熏食品等有机物质等的不完全燃烧,均会导致芳香族化合物的形成;森林大火、火山喷发等自然活动也会产生大量芳香族化合物。芳香族化合物具有较大的致癌、致畸和致突变性,对公众健康造成极大威胁。在芳香族化合物开采、分离、储运及加工过程中导致的土壤及地下水污染已成为全球面临的主要环境问题之一。微生物修复技术因其成本低、可处理各种形式的污染物、无二次污染等优点,得到越来越多的关注。
目前已鉴定出具有芳香族化合物降解能力的细菌主要有不动杆菌属(
近年来,人们对芳烃类化合物的吸附摄取和跨膜转运过程,尤其是膜蛋白在跨膜转运中的作用和传递方式进行了越来越多的研究。本文将以苯、甲苯、萘、菲等芳香族化合物为例,阐述细菌对芳烃类化合物的吸附、吸收和跨膜运输过程,期望为后续相关污染物的高效降解提供一定的借鉴和参考。
细菌对芳香族化合物的降解速率与细菌种类、培养基的pH值等有着显著关系[
细胞表面疏水性(cell-surface hydrophobicity, CSH)是决定微生物非特异性黏附到各种生物和非生物表面及界面的最重要的因素之一,从而影响微生物对疏水性化合物的吸收和转运[
PAHs等疏水性有机污染物降解的限制步骤源自它们的难溶性,从而降低了降解微生物对其的摄取效率和降解速率。通过向生长培养基中添加表面活性剂,或者通过生物自身产生生物表面活性剂可使碳氢化合物更具水溶性,提高碳氢化合物的降解效率和速率[
表面活性剂可以显著降低物质的表面张力。生物表面活性剂通过提高CSH,提高PAHs等难溶性有机化合物的生物利用度。一些芳香族化合物降解微生物通过产生表面活性化合物以及改变细胞表面特性(如细胞表面疏水性)来响应这些不可难溶性碳源[
苯并芘(benzo[α]pyrene, BaP)因其难降解且常与各种碳源的共代谢而闻名[
在添加表面活性剂后,细胞的表面疏水性、膜通透性等发生变化,促进了细胞对疏水性碳氢化合物的吸收。Liu等不仅关注表面活性剂对细菌表面特性的影响,还通过转录组测序,在以菲为唯一碳源培养条件下,分析比较了添加/不添加Tween 80对鞘氨醇单胞菌GY2B菌株(
作为地球上最成功和分布最广泛的生物生活方式之一,生物被膜可以保护微生物群落免受环境胁迫,提高微生物的存活率[
研究发现,低毒性芳香族化合物可以促进生物被膜的成熟。Hu等测试了有毒芳香胺对厌氧生物被膜发育的影响,并确定了不同浓度有毒芳香胺对EPS产生和细菌群落的动态影响。在培养48 h后,发现添加了低毒性芳香胺的系统中生物附着率高于不添加有毒芳香胺的系统。此外还发现有毒芳香族物质能刺激微生物分泌更多的EPS,EPS的分泌增强可以形成致密的保护层,这可以减轻添加到体系中的芳烃的毒性,致密的保护层可以让微生物适应有毒的环境,并逐渐降解有毒化合物[
细菌的生物被膜提高了疏水性芳香族化合物的生物修复效率。Mangwani等[
生物被膜还可以扩大细菌和疏水碳基质之间的界面面积,从而提高生物利用度,进一步加速生物被膜中芳香族化合物的生物降解。疏水性高分子量多糖分布于细菌表面[
细菌的趋化性是指细菌通过感知化学效应物的梯度,向更高浓度的引诱剂或更低浓度的驱离剂定向迁移的生理特性[
目前对大肠杆菌(
在化学效应因子中,芳香族化合物作为引诱剂可被特定的MCPs感知,随后触发细菌对芳香族化合物的趋化性[
在革兰氏阴性菌中,外膜(outer membrane, OM)的脂多糖层形成了一个非常有效的屏障,阻止亲水性化合物和疏水化合物的渗透[
目前关于亲水性物质外膜转运通道研究较多,但PAHs等芳香族化合物如何跨越这一屏障还需要进一步探索。了解此类疏水分子如何穿过外膜不仅具有基本的重要性,而且可以指导产生更有效的细菌生物降解菌株,并有望应用于设计新的疏水药物等。目前已报道可转运芳香族化合物的外膜蛋白包括FadL家族、TonB依赖性受体蛋白、OmpW家族等(
运输芳香族化合物的外膜通道蛋白
Outer membrane transporters for transport of aromatic compounds
Aromatic compound | Transporter | Protein family | Energy dependence | Strains | References |
MAHs | TodX | FadL | No | [ |
|
MAHs | CymD | FadL | No | [ |
|
MAHs | TbuX | FadL | No | [ |
|
Benzo[α]pyrene (BaP) |
TBDT-11 | TBDT | Yes | [ |
|
5, 5′-dehydrodivanillate | DDVT | TBDT | Yes | [ |
|
Naphthalene | OmpW | OmpW | Yes | [ |
FadL家族通道蛋白的成员广泛存在于革兰氏阴性菌中,是迄今为止唯一在外膜吸收疏水分子中起确定作用的蛋白。FadL最先发现于大肠杆菌中,作为该家族成员的原型,其EcFadL主要负责长链脂肪酸(long-chain fatty acids, LCFA)摄取和转运[
FadL家族成员转运机制[
The proposed transport mechanism for FadL family members[
Somboon等[
FadL家族通道蛋白在革兰氏阴性菌中非常普遍,尽管如此,但很少有FadL直系同源物被研究过,该家族很可能介导革兰氏阴性细菌中的许多重要过程。除了LCFA,MAH等分子量小的疏水性分子也可以作为FadL通道的底物。FadL家族成员侧向开口大小的不同可能是其具有底物特异性的因素之一[
TBDT由跨越外膜的22股β-折叠链组成的桶状结构域和折叠到桶内部的球状插头结构域组成。插头结构域在N末端包含一个共有序列TonB-box。栓结构域在外膜的细胞外侧结合底物,其周质区域(特别是TonB-box)与TonB-ExbB-ExbD复合物相互作用,以利用质子动力穿过内膜产生的能量,进行物质的主动运输。周质空间中的底物随后通过内膜中的ABC转运蛋白转移到细胞质中(
TBDT对芳香族化合物的运输示意图[
Schematic model for transport of aromatic compounds by TonB-dependent transporter (TBDT)[
TBDT具有底物特异性,它们在细胞膜外侧具有高亲和力底物结合口袋[
Liang等[
与14股β-折叠的FadL家族成员相比,TBDT形成的孔腔更大,因此可以转运由于分子量太大而无法通过外膜孔扩散的物质。但TBDT对亲水底物的亲和力更高,且依赖TonB-ExbB-ExbD复合物形成的质子动力势,因此是否可以直接转运疏水性芳香族化合物还存在疑问。
另一类常见的β-桶状跨膜蛋白是OmpW家族,它是广泛存在于革兰氏阴性菌中的一个小外膜孔蛋白家族。孔蛋白一般不支持疏水化合物的转运,但OmpW可以介导小分子疏水物质的跨膜运输。OmpW结构最显著的特征是β-桶内部的疏水特性,以大肠杆菌OmpW为例,其桶壁62个向内的残基中,只有20个是亲水残基,其余全为疏水残基。其中S3链上的Leu56和S7链上的Trp155形成了一个“疏水门”,控制通道关闭。与其他大多数OM蛋白相比,位于“疏水门”周质侧的桶体内部具有更强的亲水特性(
OmpW家族成员转运机制[
The proposed transport mechanism for OmpW family members[
来自恶臭假单胞菌GPoⅠ菌株(
主要协同转运蛋白超家族(major facilitator superfamily, MFS)是目前已知最大的二级主动转运蛋白超家族。MFS通过利用质子动力势(proton motive force, PMF,也称为质子电化学梯度,由质子浓度差ΔpH和膜电位Δψ组成)促进转运。如果净转运导致跨膜的电荷差异,则转运蛋白被认为是“电动的”;如果净电荷差为零,则传输是“电中性的”,并且仅由ΔpH驱动。MFS通常具有12个跨膜α-螺旋(transmembrane segments, TMS)单位,偶尔具有14或24次TMS。无论能量来源如何,当进行分子的跨膜转运时,MFS必须经历多种构象状态变化,将底物结合位点交替地仅暴露于膜的一侧,该种转运方式被称为“交替访问模式”。到目前为止,交替访问机制通常可以用“摇杆开关”、“摇杆”或“电梯”机制3种模型来描述(
MFS三种不同的转运机制模型[
Three transport mechanism models for MFS[
目前已有89个MFS家族和1 244个注释蛋白成员被报道(TCDB数据库,
运输芳香族化合物的MFS家族转运蛋白
MFS family transporters for transport of aromatic compounds
Aromatic compound | Structural formula | Transporter | MFS family | Strains | References |
5, 5′-dehydrodivanillate | DdvK | AAHS | [ |
||
Protocatechuic acid | PmdK | AAHS | [ |
||
Vanillate & protocatechuic acid | VanK | AAHS | [ |
||
Benzoate | BenK | AAHS | [ |
||
Benzalkonium bromide | EmrD | DHA1 | [ |
||
Chloramphenicol | YajR | DHA1 | [ |
||
Chloramphenicol | MdfA | DHA1 | [ |
||
Tetraphenylphosphonium chloride | LmrS | DHA2 | [ |
||
Ferulate | PcaT | MHS | [ |
||
Phthalic acid & 4-methylphthalate | MopB | MHS | [ |
||
Phthalic acid | OphD | ACS | [ |
不同生物体中MFS转运蛋白的多样性使得该家族转运底物多样,如AAHS家族的GenK、DdvK、MhpT、HppK、PacK、MhbT、TsaS和HcnK等主要参与芳香族化合物和木质素衍生的苯丙类化合物的摄取,其中MhpT和MhbT分别参与3-(3-羟基苯基)丙酸盐的分解代谢和3-羟基苯甲酸盐的摄取[
值得注意的是,一些芳香族化合物可以被细菌识别为非优势碳源或毒性物质,被外排至胞外。MFS-多药外排(multidrug resistance, MDR)转运体便可利用离子沿电化学梯度通量释放的自由能,从细胞中识别并排出芳香族化合物[
ABC转运蛋白广泛分布于各种生物体中,能够利用ATP水解产生的能量进而将与其结合的各种物质进行跨膜转运[
目前已通过遗传和生化分析对参与摄取芳香族化合物的多个ABC家族转运蛋白进行了鉴定和功能表征。鞘脂单胞杆(
尽管关于细菌对芳香族化合物的吸附和转运得到了越来越多的关注,但目前的研究仍存在局限性。比如在关于转运PAHs是否依赖能量这一问题,Bugg等[
微生物修复作为一种低耗能和环境友好的生物修复技术,近年来在芳香族化合物等的污染治理方面发挥重要作用。细菌对芳香族化合物的吸附和转运是对其进行胞内降解的基础和前提。大部分芳香族化合物具有较强的疏水性,这极大限制了细菌对该类化合物的高效摄取。细菌可以通过改变细胞表面疏水性,提高对疏水化合物溶解度;通过形成生物被膜增加和该类化合物的接触,并进一步通过细菌的趋化性向目标“食物”进军,加速对芳香族化合物的吸附。吸附至表面的化合物在内膜通道蛋白(主要为MFS超家族和ABC转运蛋白超家族)和外膜通道蛋白(主要介绍了FadL家族、TBDT家族和OmpW家族)的协助下进入胞内,进入生物降解过程。本文概述了影响细菌摄取和转运芳香族化合物主要因素。我们期待,有关芳香族化合物吸附和摄取的研究能为微生物更好地应用于环境污染物高效治理提供新思路和新视野。
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