摘要
细菌耐药性的扩散是一个严重威胁全球公共卫生安全的重要问题,尤其是2010年,在南亚和我国发现新的“超级细菌”后,人们更加关注细菌耐药性问题。细菌获得抗生素抗性基因,一方面是由于抗生素过度使用和滥用产生的抗生素选择压力造成细菌产生抗生素抗性突变；另一方面是细菌通过水平转移的方式获得抗生素抗性基因。后者是细菌获得耐药性的主要方式。细菌抗生素抗性基因往往编码在可移动质粒上,通过质粒接合转移在细菌间进行传播。质粒介导的细菌耐药基因接合转移对细菌耐药性快速扩散起到了至关重要作用。许多环境因素都能够影响质粒的接合转移过程。
纳米材料由于具有新颖的物理、化学和生物学特性,已经被应用于多个领域,尤其是作为高效吸附剂和氧化剂,正用于水处理行业。然而,纳米材料在环境中的残留对环境、生物以及人体的负面影响正在引起人们重视。纳米材料也正在成为一种新的环境污染物。大量研究表明,纳米材料可产生大量活性氧,破坏细菌细胞膜,影响蛋白质和基因,载带DNA或RNA分子进入动物和植物细胞。现在,水环境中存在着大量耐药菌和纳米材料,纳米材料是否促进耐药基因在细菌间传播还不清楚。
本研究基于以上事实提出,水中纳米材料可作用于细菌细胞膜和/或调控基因表达,促进细菌耐药基因接合转移的假说,并建立质粒介导的接合转移模型,研究水中常见纳米材料对细菌耐药基因接合转移的影响及规律,分析纳米材料作用过程中各种因素的影响规律,利用正交实验的方法分析其中的主要因素,从生物化学、细胞生物学和分子生物学多个角度探讨了纳米材料促进细菌耐药基因接合转移机制。主要研究结果如下：
利用RP4质粒建立了四个接合转移模型,包括耐药基因在大肠杆菌种属内、大肠杆菌到沙门氏菌、大肠杆菌到粪肠球菌、粪肠球菌到粪肠球菌的转移；利用RK2质粒建立了耐药基因在大肠杆菌内的转移模型；利用pCF10建立了耐药基因在粪肠球菌内的转移模型。建立的6个耐药基因接合转移模型,既包括了耐药基因在种属内的接合转移,又包括了耐药基因的跨种属转移。研究结果表明,建立的6个耐药基因接合转移模型比较稳定,可以用来评价纳米材料对耐药基因接合转移的影响。
纳米TiO2、纳米SiO2、纳米Fe2O3和纳米Al2O3都能促进RP4质粒从大肠杆菌到沙门菌的转移。纳米材料浓度为5mmol/L时,与空白对照和大颗粒材料相比,可使RP4接合转移分别提高89倍、10倍、20倍和142倍,纳米Al2O3的促进作用最强。不同接合转移体系中,纳米材料都有促进作用。5mmol/L纳米Al2O3可使RP4从大肠杆菌到大肠杆菌、革兰阴性菌到革兰阳性菌、粪肠球菌到粪肠球菌的接合频率转移分别增加200倍、50倍和100倍。纳米Al_2O_3对RK2和pCF10接合转移的促进作用可分别达到170倍和120倍。这些数据说明,纳米材料对接合质粒介导的耐药基因转移的促进作用可能是一个普遍现象。而且相同成分的大颗粒材料对耐药基因的接合转移无明显的促进作用,也说明对接合转移的促进作用来自纳米材料的纳米结构。
以纳米Al_2O_3作为代表材料研究了接合转移中的影响因素。结果表明,随着浓度升高,纳米Al_2O_3对RP4接合转移促进作用增强。纳米Al_2O_3浓度为5mmol/L时达到最高,可以提高RP4接合转移100倍以上。纳米Al_2O_3浓度高于5mmol/L时,促进作用减弱,但是与空白对照组和大颗粒组比较,仍能显著促进RP4接合转移。纳米Al_2O_3的作用效果随浓度变化有峰值出现,原因可能是纳米材料,尤其是高浓度纳米材料能使细胞产生严重的氧化应激反应,造成细菌大量死亡。利用数学模型排除细菌死亡影响,5mmol/L纳米Al_2O_3能提高接合转移常数5个数量级。纳米Al_2O_3作用下,随着接合菌密度升高和接合时间延长,接合子数量逐渐增加,与空白对照和大颗粒组比较,增加显著。纳米Al_2O_3作用后,接合温度低于20℃时,随温度升高生成的接合子数量增加；温度高于20℃时,接合子生成数量增加不明显。接合体系的pH值对接合子生成无明显影响。在富营养条件下(LB培养基),接合子生成的数量更多。利用正交实验分析各因素的作用情况发现,各因素对接合子生成影响的重要次序为：初始菌密度>纳米Al_2O_3浓度>接合时间>接合温度>初始菌密度与纳米浓度的交互作用。纳米Al_2O_3浓度已成为仅次于初始菌密度的影响因素。在最适宜的条件下能够提高RP4在PBS中跨种属转移效率200倍,提高RP4在LB中同种属内的转移效率250倍。
纳米Al_2O_3促进RP4接合转移机制研究发现：纳米Al_2O_3能促使细菌细胞产生大量OH·,激发细菌的氧化抗氧化反应。透射电镜与原子力显微镜的结果也表明,纳米Al_2O_3对细菌细胞膜产生影响,细胞膜表面变得不光滑,甚至部分细胞膜发生溶解。浓度越高,纳米Al_2O_3对细菌细胞膜影响越严重。大颗粒Al_2O_3却无类似的结果,说明纳米Al_2O_3的纳米结构是产生细胞膜损伤的主要因素。纳米Al_2O_3对细菌细胞膜的影响为供体菌和受体菌的细胞膜融合和DNA跨膜转运提供了便利条件。纳米Al_2O_3通过抑制korA和korB的mRNA表达,激活了trbBp基因的mRNA表达,进而促使供体菌与受体菌间形成“接合桥”,促进了接合转移的第一个过程。电镜结果也证实纳米Al_2O_3使形成的“接合桥”数量增加。同时纳米Al_2O_3通过抑制korB和trbA的mRNA的表达,激活了trfAp基因的mRNA表达,促使RP4质粒的转移与复制,促进了接合转移的第二个过程。
总的来说,纳米材料能通过影响细菌细胞膜状态,影响与接合转移过程相关的调控基因mRNA表达而促进了接合质粒的接合转移。
本课题利用生命科学的新技术,研究材料领域的纳米粒子对环境安全领域的细菌耐药性接合转移的影响规律与机制,是典型的学科交叉研究,也是相关学科的前沿领域,将开辟纳米材料环境安全研究的新领域。本课题的研究结果将进一步增加人们对细菌耐药性转移与获得的认识程度,丰富相关的科学知识,同时也将提高人们对环境中残留纳米材料所引起的环境与生态风险的认识。本研究提示我们应更加认真的对纳米材料进行相关的安全性评价和谨慎地使用纳米材料,以便控制或减少由纳米材料导致的环境中耐药菌的形成与增加。
The development of antibiotic resistance in bacteria is one of the most serious threats to global public health, as exemplified by the appearance of a new 'super bug' in2010in South of Asia and our country. The spread of antibiotic resistance genes is due to the selective pressures caused by increases in the use and misuse of antibiotics in medicine and animal feedstuffs. Also important is the presence of increasing amounts of these substances in the environment by horizontal transfer between bacteria, rather than by the sequential modification of gene function by the accumulation of point mutations. Of all the mechanisms and mobile elements that mediate horizontal gene transfer between bacteria, conjugation by self-transferable plasmids may be the most important. The critical role that plasmids play in the rapid spread of antibiotic resistance genes is particularly salient. Aquatic environments and water treatment processes are able to affect the efficiency of antibiotic resistance gene transfer.
Nanomaterials, which often possess novel physical, chemical, and biological properties, are being utilised in an increasing number of fields, especially in water treatment as efficient adsorbents and oxidants. Their use in water treatment may result in a considerable amount of nanomaterial residue in the water, and cause negative impact on the environment, biological and human. Otherwise, nanosized materials at the same time they may, in fact, become new environmental hazards themselves. Some studies have indicated that nano-materials can cause disruption to bacterial membranes by the production of reactive oxygen species (ROS), can affect protein and gene, and can deliver DNA or RNA molecules into animal or plant cells. Recently, there are a large number of drug-resistant bacteria and nano materials in water environment. The extent to which nano-materials are able to cause an increase in antibiotic resistance by the regulation of the conjugative transfer of antibiotic resistance genes in bacteria is still unknown.
Based on the above data, we hypothesised that nano-materials that are present in water may promote the horizontal transfer of multidrug-resistance genes by acting on cell membranes and/or regulating genes involved in plasmid transfer. And on basis of the construction of the conjugative transfer models mediated by plasmids, we studied the effect of nano-materials in water environment on the conjugative transfer, and analyzed the effect of various factors on conjugative transfer under nano-materials induced, found out the main factors with Orthogonal experiment, and explored the mechanisms by which nano-alumina promote the horizontal transfer of antibiotic multiresistance features by morphological, biochemical, and molecular biological methods.
The main findings are as follows:
We established four kinds conjugative transfer models with RP4plasmid, including the resistance gene conjugative transfer in E. coli species, from E. coli to Salmonella, from E. coli to Enterococcus faecalis, and from Enterococcus faecalis to Enterococcus faecalis. Another two conjugative transfer models, including transfer in E. coli species with RK2plasmid and transfer in to Enterococcus faecalis with PCF10plasmid were also be established. These six models include the resistance genes transferring within species and across specie. The results showed that the six conjugative transfer models were relatively stable and could be used to evaluate the effect of nano-materials on the conjugative transfer of resistance genes.
Nano-TiO2, nano-SiO2, nano-Fe2O3and nano-Al2O3could promote the transfer of the RP4plasmid from E. coli to Salmonella. At5mmol/L, these four anomaterials could promote the conjugative transfer of RP4by up to89times,10times,20times and142times respectively compared with blank control and bulk materials. Nano-alumina gave the most significant effect. And in other conjugative transfer systems, nano-materials also could promote the resistance genes transfer.5mmol/L nano-alumina can promote the conjugative transfer of RP4between bacteria of the same genus, more specifically from E. coli to E. coli, and increase the transfer by200-fold. Nano-alumina also can significantly promote the conjugative transfer of RP4from Gram-negative bacteria to Gram-positive bacteria by more than50-fold. In other mating systems, from Enterococci to Enterococci, the conjugative transfer of RP4could also be promoted by5mmol/L nano-alumina which increased the transfer by100-fold. Nano-alumina also could promote the horizontal transfer of other conjugative plasmids, such as an unrelated conjugation system in the Gram-negative bacteria, RK2and the enterococcal pheromone-mediated conjugation system involving an endogenous enterococcal plasmid, pCF10. The results showed that nano-alumina could significantly promote the RK2and pCF10conjugational transfer when the concentration of nano-alumina ranged from0.05to50mmol/L. The conjugative transfer frequencies of RK2and pCF10were also the highest in the5mmol/L nano-alumina group, which induced an increase in the transfer of more than170-fold and120-fold compared to the control group respectively. These data showed that it might be a common phenomenon that nano-materials could promote the conjugative transfer of resistance genes. And the results that bulk nano-materials did not affect the conjugative transfer of resistance genes suggested that nanostructures rather than the chemical composition of these nano-materials played a major role in the promoting transfer.
Nano Al2O3and RP4plasmid were chosen as the indicators to evaluate the effect of factors on the transfer of resistance genes. Bulk alumina at any concentration had no significant effect on conjugative transfer of RP4, but nano-alumina could significantly promote conjugative transfer, and this transfer increased with increasing of nano-alumina concentrations the conjugative transfer was the highest in the5mmol/L nano-alumina group, which was more than100-fold higher than that of control group. When the nano-alumina concentration was higher than5mmol/L, the transfer rate decreased, as higher nano-alumina concentrations were found to damage the bacterial membrane severely and kill most bacteria. Furthermore, the nanoparticles may have aggregated, and thus become relatively less bioavailable at these concentrations compared with lower concentrations.The conjugative transfer of RP4increased with bacterium concentration. The conjugative transfer in each group increased with the prolongation of mating time, and the conjugative transfer in5mmol/L nano-alumina group was markedly higher than that of the control group at each time point. In order to determine the impact of nano-alumina on RP4transfer accurately, a simple mass action model was used to explain the kinetics of RP4conjugative transfer. The results showed that the conjugational transfer rate constant of5mmol/L nano-alumina group was approximately5orders magnitude higher than that of the control group. The conjugation was lower at4℃and15℃than that at20℃or higher, but showed no further increase above20℃. The pH had no significant effect on plasmid transfer. We used orthogonal design (L64(421)) with the four variables to observe the effect on the conjugative transfer of RP4. The statistical results showed that every one of these four variables had a significant effect on the conjugation, while there was an interaction between the bacterial concentration and nano-alumina concentration. The ranking of these factors in the order of importance of affecting the conjugative transfer was as follows:bacteria concentration> nano-alumina concentration> mating temperature> mating time> the interaction between bacteria concentration and nano-alumina concentration. The effect on promotion of conjugative transfer of nano-alumina was greater than the effects of mating temperature and mating time. Under the optimum conditions, the conjugative transfers of RP4across genera in PBS and within species in LB were more than200-fold and250fold higher than that when no nano-alumina was added.
We also explored the potential mechanisms of nano-alumina in promoting conjugative transfer of RP4. Our study showed that nano-alumina caused the SOS response of parent bacteria and also damage the integrity of cell membranes, as was seen from the results of TEM and AFM. The productions of hydroxyl free radicals (OH·) in bacteria were increased with the increasing of nano-alumina concentration. And other inductors of bacterial oxidative stress-response systems increased with increase in nano-alumina levels and significantly higher than those in the control group and bulk alumina groups. The cytoplasm of the bacteria agglomerated, and the parts of the cell membranes were undefined, and the cell membranes displayed wrinkles and fissures when nano-alumina induced. Nano-alumina can enhance the conjugation efficiency through the regulation of conjugative gene expression. We observed that nano-alumina significantly promoted bacteria conjugation. This phenomenon results from the promotion of RP4conjugation gene expression by nano-alumina. The trbBp expression was enhanced after treatment with nano-alumina, which led to the formation of more conjugants. In addition, nano-alumina could promote the expression of trfAp, which is a gene that plays an important role in the transfer and replication of RP4. Nano-alumina may promote the horizontal transfer by repressing the expression of global regulatory genes that are involved in RP4conjugation. We found in this study that korA, korB and trbA mRNA expression were repressed significantly by nano-alumina. These results mean that trfA and trbB are activated and increase this expression, which provides the sequential steps that enhance the efficiency of transfer.
In conclusion, this study reported that nano-materials in water increased the conjugative transfer of resistance genes involve the damage of bacterial membranes by oxidative stresses, an enhancement of the expression of conjugative genes, and the repression of the global regulatory factor genes for RP4plasmid conjugation.
This study will not only open up a new field of study on the environmental safety of nanomaterials, but also further enrich our knowledge about the the transfer of resistance genes. The results will also help us to control the generation of drug resistance bacteria, to lay theoretical and technical foundation for us to in-depth study the potential risks of nanomaterials and provide us an guidline of nano-materials production and security applications.
引文
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