生物阴极强化氯霉素还原降解及电极微生物功能机制解析
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摘要
抗生素进入环境可以诱发进化新的抗生素抗性基因和抗性细菌，对人类健康产生巨大威胁，因此抗生素的抗性问题已引起全球关注。氯代硝基芳香类抗生素氯霉素对人类可导致再生障碍性贫血且具有潜在的遗传毒性和致癌性。环境中频繁检测出低浓度的氯霉素和氯霉素抗性基因存在，因此在废水处理过程中消除氯霉素抗细菌活性至关重要。生物电化学系统（BES）生物阴极可以还原降解多种污染物，重要地是微生物作为阴极催化剂具有可自我更新和环境友好等特性，发展颇具潜力。硝基基团对于决定氯霉素抗细菌活性非常重要，本研究采用生物阴极还原降解氯霉素为脱氯芳香胺产物，对应的硝基还原和脱氯反应解除了氯霉素抗细菌活性；揭示了加速阴极电子传递还原氯霉素的核心微生物群落与关键功能基因组成；发现了低温启动生物阴极更能应激环境温度变化维持稳定的催化活性，为开发抗生素废水高效降解生物技术提供了重要依据。
生物阴极（阴极电位为-0.7V和提供500mg/L葡萄糖）还原氯霉素速率比非生物阴极和单纯厌氧生物膜还原分别快10倍和1.6倍，证明了生物阴极强化还原氯霉素为芳香胺产物AMCl2，并进一步依赖脱卤素酶脱氯生成AMCl产物。非生物阴极还原氯霉素明显积累毒性较大的亚硝基和羟基胺基中间产物，并通过加氢脱氯机制脱氯AMCl2生成AMCl。微生物催化氯霉素短暂积累独特的氯霉素乙酰化产物。阴极还原氯霉素过程解除了其抗细菌活性。电化学分析表明生物阴极明显降低了氯霉素还原反应过电位（正移400mV），暗示了阴极微生物促进阴极电子传递。生物阴极中多个占优势菌属具有硝基芳香烃还原能力（Salmonella、Enterobacter、Clavibacter和Pseudomonas）和阴极电化学活性（Enterobacter、Pseudomonas和Dechloromonas），说明了这些功能微生物参与强化氯霉素还原降解过程。
生物阴极还原氯霉素效率显著高于单纯厌氧生物膜。基于高通量功能基因芯片（GeoChip）和16S rRNA基因Illumina测序结果表明阴极给电子刺激具有选择性，显著改变了阴极生物膜的群落结构与功能基因组成，并明显降低了阴极生物膜群落多样性。生物阴极显著富集了具有电化学活性革兰氏阳性Lactococcus（P=0.004；51.50±24.60%），Lactococcus能够分泌电子传递中介体这与生物阴极检测到显著低水平的典型电子传递蛋白细胞色素c基因丰度（P=0.023）相一致，重要地是Lactococcus具有硝基芳香烃还原能力；而厌氧生物膜显著富集了葡萄糖发酵细菌Escherichia（P=0.002；10.64±4.49%）和Dysgonomonas（P=0.015；25.25±13.17%），其中Escherichia具有氯霉素还原能力。生物膜中占优势其它菌属比如Desulfovibrio、Geobacter、Pseudomonas和Klebsiella均具有还原硝基芳香化合物到对应的芳香胺产物的能力。生物阴极显著高的氯霉素还原效率与生物膜中占优势的Lactococcus丰度成显著正相关（r=0.7769；P=0.003），而与细胞色素c基因丰度成显著负相关（r=-0.5857；P=0.045），暗示了生物阴极主要通过电子传递中介体捕获电子加速还原降解氯霉素。
北方寒冷地区环境温度变化大，启动能够应激温度变化的生物阴极来稳定还原氯霉素至关重要。对比常温25℃和低温10℃启动生物阴极，并分别降低或升高15℃后，发现10℃比25℃启动生物阴极更能应激温度变化来稳定还原降解氯霉素，而且常温下产物AMCl形成效率与低温运行时无显著差异。基于GeoChip和16S rRNA基因Illumina测序结果，温度提升15℃显著改变阴极生物膜群落结构与功能基因组成。在菌门水平上温度变化前后阴极生物膜没有显著差别，主要富集变形菌门（＞60%）和厚壁菌门（＞20%）细菌，但占优势菌属差异非常显著。10℃和25℃阴极生物膜分别富集1067和2113个独特功能基因，其中各富集了9个独特的电子传递有关基因。进一步分析发现了维持生物阴极催化功能的关键功能基因及优势菌属。低温运行显著富集适低温环境的Aeromonas和Vagococcus细菌，而温度提升显著富集具有硝基芳香烃还原能力细菌Raoultella和硝基还原酶基因丰度。参与热激响应的基因在阴极生物膜环境温度提高后显著富集，而细胞色素c和氢化酶等重要电子传递基因丰度均未显著改变。这些重要功能基因类群和生物膜占优势菌属参与应激环境温度变化，对于维持生物阴极稳定还原降解氯霉素具有重要作用。
Antibiotics entering into the environments can result in evolution of novel antibiotic resistant genes and bacteria, and then has enormous ramifications for human health. Thus antibiotic resistance problem has attracted global attentions. For humans, chlorinated nitroaromatic antibiotic, chloramphenicol (CAP) can lead to aplastic anemia and have potential genotoxicity and carcinogenicity. Trace CAP and the CAP-resistant genes were frequently detected in diverse environments, thus elimination of the antibacterial activity of CAP is very important during wastewater treatment. The bioelectrochemical system (BES) with biocathode is an emerging technology that could reductively degrade various pollutants. Importantly, microbes worked as the cathode catalyst has great potential as the characteristic of self-renewal and environmental friendliness. The nitro group of CAP is the essential functional group determining its antibiotic properties. In this study BES biocathode was employed for the reductive degradation of CAP to the corresponding dechlorinated aromatic amine product. Corresponding nitro group reduction and dechlorination reactions eliminated the antibacterial activity of CAP. The key microbial community structure and functional genes composition for the accelerating the cathodic electrons transfer associated with the CAP reduction was revealed. It discovers that the low temperature performed biocathode had stronger stress response to environment temperature changes and keeping the stable catalytic activity. These results provides the important basis for the development of efficient degradation biotechnology for the antibiotics wastewater treatment.
The CAP reduction speed constant of biocathode was10and1.6times higher than an abiotic cathode and opened biocathode (pure anaerobic microbial reduction) experiment, respectively. Biocathode enhanced reduction of CAP to the corresponding aromatic amine product AMCl2, and the AMCl2was further dechlorinated to AMCl with dehalogenase catalysis. Toxic intermediates, hydroxylamino (HOAM), and nitroso (NO), from CAP reduction were obviously accumulated only in the abiotic cathode, and electrochemical hydrodechlorination was responsible for the dechlorination of AMCl2to AMCl in abiotic BES. Acetylation of one hydroxyl of CAP (CAP-acetyl) was briefly accumulated exclusive in the biocatalyzed process. Cathodic CAP reduction lost the antibacterial activity. The electrochemical analysis indicated the obvious decrease of overpotentials (positive shift of400mV) for the CAP reduction at the biocathode compared with abiotic cathode, suggesting that the cathodophilic microbes maybe improve the cathodic electrons transfer. Some dominant genera from biocathode had the nitroaromatics reduction ability (Salmonella, Enterobacter, Stenotrophomonas, Clavibacter and Pseudomonas) and cathodic electrochemical activity (Enterobacter, Pseudomonas and Dechloromonas), indicating that these functional microbes involved in the enhanced reduction of CAP.
The cathode biofilm showed significant higher CAP reduction efficiency than that of the pure anaerobic biofilm. The cathode providing electrons stimulation had the selectivity, which significantly altered the community structure and functional genes composition of cathode biofilm, and obviously lowered the microbial diversity based on the highthroughput functional gene array (GeoChip) and Illumina16S rRNA gene sequencing analysis. The electrochemically active Gram-positive Lactococcus (P=0.004;51.50±24.60%) was significantly enriched in the biocathode community. Lactococcus could self-excrete electrons transfer mediator was consistent with that the cathode biofilm detected significantly lower cytochrome c gene abundances (P=0.023). Importantly, Lactococcus was capable of reducing nitroaromatics to the corresponding aromatic amines. While anaerobic glucose fermentative bacteria Escherichia (P=0.002;10.64±4.49%) and Dysgonomonas (P=0.015;25.25±13.17%) were significantly enriched in the anaerobic biofilm, among them Escherichia was capable of reducing CAP. Some other dominant genera such as Desulfovibrio, Geobacter, Pseudomonas and Klebsiella all were capable of reducing nitroaromatics to corresponding aromatic amines. The significant higher CAP reduction efficiency in the biocathode community, which significantly positively (r=0.78; P=0.003) correlated with the dominant Lactococcus, while significantly negatively correlated with the significantly lower cytochrome c genes (r=-0.5802; P=0.048), suggested that electrons transfer mediator was mainly employed to capture cathodic electrons for accelerated reduction of CAP within biocathode communities.
Environment temperature changes greatly in northern cold regions, it is crucial for the enrichment of cathode biofilm that have stress responses ability to stably reduce CAP upon temperature changes. Comparing with the room temperature25°C, low temperature10°C performed biocathode and the corresponding15°C decrement and increment for the performed biocathode BES reactors respectively, the results showed that the10°C performed biocathode had more stress response ability to stably reduce CAP upon temperature changes, and the formation efficiency of reduced product AMCl under room temperature was not significant different from that of the low temperature performed biocathode. Based on the GeoChip and Illumina16S rRNA gene sequencing analysis, the results indicated that the15°C increment significantly altered the microbial phylogenetic community structure and functional genes composition. Before and after of temperature changes, the cathode biofilm was not obviously differed at the phylum level (enriched>60%Proteobacteria and>20%Firmicutes) but at the genus level showed the significant differences. The10°C and25°C performed biocathode enriched1067and2113unique functional genes respectively, thereinto both enriched9unique genes that related to electrons transfer. Further analysis revealed that the key functional genes and dominant genera were employed for the maintaining the biocathode catalytic function. Cold-adapting Aeromonas and Vagococcus dominated in the10°C performed biocathode, while the25°C performed biocathode had higher abundance of nitroaromatics-reducing Raoultella and nitroreductase genes. Genes related to heat shock protein were significantly enriched in the25°C performed biocathode, however the abundances of important electrons transfer genes such as cytochrome c and hydrogenase was not significantly differed. These important functional gene categories and dominant genera in the cathode biofilms involved in the stress response to environment temperature changes, which played the key role for the maintaining the stability of CAP reduction.
生物阴极（阴极电位为-0.7V和提供500mg/L葡萄糖）还原氯霉素速率比非生物阴极和单纯厌氧生物膜还原分别快10倍和1.6倍，证明了生物阴极强化还原氯霉素为芳香胺产物AMCl2，并进一步依赖脱卤素酶脱氯生成AMCl产物。非生物阴极还原氯霉素明显积累毒性较大的亚硝基和羟基胺基中间产物，并通过加氢脱氯机制脱氯AMCl2生成AMCl。微生物催化氯霉素短暂积累独特的氯霉素乙酰化产物。阴极还原氯霉素过程解除了其抗细菌活性。电化学分析表明生物阴极明显降低了氯霉素还原反应过电位（正移400mV），暗示了阴极微生物促进阴极电子传递。生物阴极中多个占优势菌属具有硝基芳香烃还原能力（Salmonella、Enterobacter、Clavibacter和Pseudomonas）和阴极电化学活性（Enterobacter、Pseudomonas和Dechloromonas），说明了这些功能微生物参与强化氯霉素还原降解过程。
生物阴极还原氯霉素效率显著高于单纯厌氧生物膜。基于高通量功能基因芯片（GeoChip）和16S rRNA基因Illumina测序结果表明阴极给电子刺激具有选择性，显著改变了阴极生物膜的群落结构与功能基因组成，并明显降低了阴极生物膜群落多样性。生物阴极显著富集了具有电化学活性革兰氏阳性Lactococcus（P=0.004；51.50±24.60%），Lactococcus能够分泌电子传递中介体这与生物阴极检测到显著低水平的典型电子传递蛋白细胞色素c基因丰度（P=0.023）相一致，重要地是Lactococcus具有硝基芳香烃还原能力；而厌氧生物膜显著富集了葡萄糖发酵细菌Escherichia（P=0.002；10.64±4.49%）和Dysgonomonas（P=0.015；25.25±13.17%），其中Escherichia具有氯霉素还原能力。生物膜中占优势其它菌属比如Desulfovibrio、Geobacter、Pseudomonas和Klebsiella均具有还原硝基芳香化合物到对应的芳香胺产物的能力。生物阴极显著高的氯霉素还原效率与生物膜中占优势的Lactococcus丰度成显著正相关（r=0.7769；P=0.003），而与细胞色素c基因丰度成显著负相关（r=-0.5857；P=0.045），暗示了生物阴极主要通过电子传递中介体捕获电子加速还原降解氯霉素。
北方寒冷地区环境温度变化大，启动能够应激温度变化的生物阴极来稳定还原氯霉素至关重要。对比常温25℃和低温10℃启动生物阴极，并分别降低或升高15℃后，发现10℃比25℃启动生物阴极更能应激温度变化来稳定还原降解氯霉素，而且常温下产物AMCl形成效率与低温运行时无显著差异。基于GeoChip和16S rRNA基因Illumina测序结果，温度提升15℃显著改变阴极生物膜群落结构与功能基因组成。在菌门水平上温度变化前后阴极生物膜没有显著差别，主要富集变形菌门（＞60%）和厚壁菌门（＞20%）细菌，但占优势菌属差异非常显著。10℃和25℃阴极生物膜分别富集1067和2113个独特功能基因，其中各富集了9个独特的电子传递有关基因。进一步分析发现了维持生物阴极催化功能的关键功能基因及优势菌属。低温运行显著富集适低温环境的Aeromonas和Vagococcus细菌，而温度提升显著富集具有硝基芳香烃还原能力细菌Raoultella和硝基还原酶基因丰度。参与热激响应的基因在阴极生物膜环境温度提高后显著富集，而细胞色素c和氢化酶等重要电子传递基因丰度均未显著改变。这些重要功能基因类群和生物膜占优势菌属参与应激环境温度变化，对于维持生物阴极稳定还原降解氯霉素具有重要作用。
Antibiotics entering into the environments can result in evolution of novel antibiotic resistant genes and bacteria, and then has enormous ramifications for human health. Thus antibiotic resistance problem has attracted global attentions. For humans, chlorinated nitroaromatic antibiotic, chloramphenicol (CAP) can lead to aplastic anemia and have potential genotoxicity and carcinogenicity. Trace CAP and the CAP-resistant genes were frequently detected in diverse environments, thus elimination of the antibacterial activity of CAP is very important during wastewater treatment. The bioelectrochemical system (BES) with biocathode is an emerging technology that could reductively degrade various pollutants. Importantly, microbes worked as the cathode catalyst has great potential as the characteristic of self-renewal and environmental friendliness. The nitro group of CAP is the essential functional group determining its antibiotic properties. In this study BES biocathode was employed for the reductive degradation of CAP to the corresponding dechlorinated aromatic amine product. Corresponding nitro group reduction and dechlorination reactions eliminated the antibacterial activity of CAP. The key microbial community structure and functional genes composition for the accelerating the cathodic electrons transfer associated with the CAP reduction was revealed. It discovers that the low temperature performed biocathode had stronger stress response to environment temperature changes and keeping the stable catalytic activity. These results provides the important basis for the development of efficient degradation biotechnology for the antibiotics wastewater treatment.
The CAP reduction speed constant of biocathode was10and1.6times higher than an abiotic cathode and opened biocathode (pure anaerobic microbial reduction) experiment, respectively. Biocathode enhanced reduction of CAP to the corresponding aromatic amine product AMCl2, and the AMCl2was further dechlorinated to AMCl with dehalogenase catalysis. Toxic intermediates, hydroxylamino (HOAM), and nitroso (NO), from CAP reduction were obviously accumulated only in the abiotic cathode, and electrochemical hydrodechlorination was responsible for the dechlorination of AMCl2to AMCl in abiotic BES. Acetylation of one hydroxyl of CAP (CAP-acetyl) was briefly accumulated exclusive in the biocatalyzed process. Cathodic CAP reduction lost the antibacterial activity. The electrochemical analysis indicated the obvious decrease of overpotentials (positive shift of400mV) for the CAP reduction at the biocathode compared with abiotic cathode, suggesting that the cathodophilic microbes maybe improve the cathodic electrons transfer. Some dominant genera from biocathode had the nitroaromatics reduction ability (Salmonella, Enterobacter, Stenotrophomonas, Clavibacter and Pseudomonas) and cathodic electrochemical activity (Enterobacter, Pseudomonas and Dechloromonas), indicating that these functional microbes involved in the enhanced reduction of CAP.
The cathode biofilm showed significant higher CAP reduction efficiency than that of the pure anaerobic biofilm. The cathode providing electrons stimulation had the selectivity, which significantly altered the community structure and functional genes composition of cathode biofilm, and obviously lowered the microbial diversity based on the highthroughput functional gene array (GeoChip) and Illumina16S rRNA gene sequencing analysis. The electrochemically active Gram-positive Lactococcus (P=0.004;51.50±24.60%) was significantly enriched in the biocathode community. Lactococcus could self-excrete electrons transfer mediator was consistent with that the cathode biofilm detected significantly lower cytochrome c gene abundances (P=0.023). Importantly, Lactococcus was capable of reducing nitroaromatics to the corresponding aromatic amines. While anaerobic glucose fermentative bacteria Escherichia (P=0.002;10.64±4.49%) and Dysgonomonas (P=0.015;25.25±13.17%) were significantly enriched in the anaerobic biofilm, among them Escherichia was capable of reducing CAP. Some other dominant genera such as Desulfovibrio, Geobacter, Pseudomonas and Klebsiella all were capable of reducing nitroaromatics to corresponding aromatic amines. The significant higher CAP reduction efficiency in the biocathode community, which significantly positively (r=0.78; P=0.003) correlated with the dominant Lactococcus, while significantly negatively correlated with the significantly lower cytochrome c genes (r=-0.5802; P=0.048), suggested that electrons transfer mediator was mainly employed to capture cathodic electrons for accelerated reduction of CAP within biocathode communities.
Environment temperature changes greatly in northern cold regions, it is crucial for the enrichment of cathode biofilm that have stress responses ability to stably reduce CAP upon temperature changes. Comparing with the room temperature25°C, low temperature10°C performed biocathode and the corresponding15°C decrement and increment for the performed biocathode BES reactors respectively, the results showed that the10°C performed biocathode had more stress response ability to stably reduce CAP upon temperature changes, and the formation efficiency of reduced product AMCl under room temperature was not significant different from that of the low temperature performed biocathode. Based on the GeoChip and Illumina16S rRNA gene sequencing analysis, the results indicated that the15°C increment significantly altered the microbial phylogenetic community structure and functional genes composition. Before and after of temperature changes, the cathode biofilm was not obviously differed at the phylum level (enriched>60%Proteobacteria and>20%Firmicutes) but at the genus level showed the significant differences. The10°C and25°C performed biocathode enriched1067and2113unique functional genes respectively, thereinto both enriched9unique genes that related to electrons transfer. Further analysis revealed that the key functional genes and dominant genera were employed for the maintaining the biocathode catalytic function. Cold-adapting Aeromonas and Vagococcus dominated in the10°C performed biocathode, while the25°C performed biocathode had higher abundance of nitroaromatics-reducing Raoultella and nitroreductase genes. Genes related to heat shock protein were significantly enriched in the25°C performed biocathode, however the abundances of important electrons transfer genes such as cytochrome c and hydrogenase was not significantly differed. These important functional gene categories and dominant genera in the cathode biofilms involved in the stress response to environment temperature changes, which played the key role for the maintaining the stability of CAP reduction.
引文
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