生物配体模型（BLM）对于评价金属联合毒性的适用性研究
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摘要
在受污染的环境中,金属通常是相互混合并且相互作用的。然而,目前对污染物的风险评价通常还是以单一污染物的效应评价为基础的。近年来,生物配体模型(Biotic Ligand Model, BLM)由于其在金属水质标准制定以及生态风险评价中的应用而日益受到重视。BLM的方法具备应用于混合金属风险评价的能力,但其无法被简单直接的应用于金属混合物效应的评价,而且目前仍不清楚模型的一些简单假设能否满足混合金属复杂的相互作用。因此,应当谨慎地将BLM的方法应用于金属相互作用的模拟。本文简要的介绍了BLM的发展以及理论基础,在对模型的优势和应用中存在的问题进行分析的基础上,对模型的应用范围进行了探索性的研究。首先,以天津地区的一系列景观水体与实验室配制的模拟溶液为例,对已开发的应用于大型溞(Daphnia magna)的急性Zn-BLM的预测能力进行评价。其次,尝试将BLM的方法应用于斑马鱼胚胎毒性的预测,以探讨将模型推广到其他生物(或其他发育阶段)的适用性。为探明Ca2+浓度增加是否会使鱼类早期发育阶段对铅毒性的敏感性升高,以及Ca2+单独减弱铅毒性的浓度范围,选用斑马鱼胚胎作为实验材料,记录在不同的水化学参数条件下,胚胎发育过程中一些具有代表性的毒理学终点,采用相对易于观察且敏感的指标——72 h孵化率进行分析。论文重点探讨了量化微量营养元素铜(Cu)与非必需金属铅(Pb)积累的相互作用,以验证BLM的一些基本假设。在人工配置的已知离子浓度的实验溶液中,采用野生型淡水单细胞绿藻Chlamydomonas reinhardtii做短时积累实验,暴露浓度范围是5X10-8至5x10-6M,同时测定Pb和Cu单独存在时的内化通量,以使用常数的倒数来确定Michaelis-Menten稳定常数。在此基础上,论述BLM是否具有预测另一种生物效应——基因表达的潜力。研究不同Cu和Pb的浓度下,绿藻生物积累和与金属效应相关的基因表达的变化。着重研究以下几个基因,编码：自然抵抗联合巨噬细胞蛋白(natural resistance associated macrophage protein, nramp1),铜传输位点(copper transporter, ctr2),氧化压力效应基因——谷胱甘肽过氧(化)物酶(glutathione peroxidase, gpx5),以及谷胱甘肽转移酶(glutathione S-transferase, gsts2)。研究采用Visual MINTEQ version 2.5.2进行BLM的相关计算以及金属与溶液中离子的化学形态分析。本文的研究结果可以用来扩展BLM对于金属混合物的预测能力,从而提高该模型预测金属混合物毒性的能力。
论文研究结果表明：
(1)在测试的水化学参数范围内,认为以锌对大型蚤的急性毒性数据建立起来的模型是一种有用的工具,能够在锌的生态风险评价中考虑生物有效性的问题,对所有水体(包括不同稀释倍数的水样)的预测结果与测试结果近似,80%的实测值在预测值67%-150%范围内。但以鱼类为基础开发的,通过下调LA50被应用于水蚤的急性Zn-BLM的预测值普遍高于实测值,其实测值为预测值的约2至4倍。通过调整LA50拓展模型适用性的方法过于简单,正受到质疑。
(2)当Ca2+浓度从0.25 mmol/L增加到2.00 mmol/L时,导致了以自由铅离子活度({Pb2+})和溶解态铅总浓度([Pb]T)表示的72-h EC5o的增加(表现为发育延迟),两者之间存在良好的线性关系。通过这一线性关系,可以对Ca2+浓度对铅毒性的影响进行预测。这一结果支持了生物配体模型(BLM)概念的假设,说明在胚胎的表面,铅离子与钙离子可能在传输和毒性作用位点上存在竞争作用。而当Ca2+浓度从2.00 mmol/L增加到4.00 mmol/L时,72-h EC50 {Pb2+}和72-h EC50 [Pb]T并没有显著的增加。
(3)Cu的稳定常数为105.8M-1,与Pb的常数(105.9M-1)相似。然而,竞争实验没有表现出直接的拮抗作用,这与BLM的预测不符。当Pb存在时,在高浓度条件下,Cu的积累会由于Pb的影响而降低,但当Cu的浓度低于10-7M时,Cu的积累不受Pb的影响。在高浓度的Cu(>1μM)条件下,Cu表现出竞争抑制；而在低Cu条件下,Cu对Pb的积累有协同效应,这种协同效应无法用BLM的观点解释。为了解释这一效应,进一步进行了细胞活动能力试验,膜渗透性试验以及基因表达试验。在Pb存在的条件下,ctr2(一段编码Cu传输位点的基因)的表达增加,表明生物积累是一个比模型假设更加复杂的动态过程。
(4)不同基因会产生不同的相互作用,表明每种基因都可能会产生其特异的细胞内的反馈与调节,这也会与不同的金属有关。这与稳定状态模型的一个假设不符：在敏感位点上不会引起显著的生物调节。即使在短时间的暴露实验中,仍然难以满足该假设。不同金属传输位点所出现的效应不同(ctr2和nrampl),表明传输分子发生了调解与改变。而且,BLM的假设认为金属的生物效应是由于金属富集在生物配体上所产生的,是金属积累的函数。虽然金属必须先积累在生物体中才能产生生物效应,但如仅简单认为金属的积累与其毒性效应之间存在着某种比例关系,这一假设显然太过于简单。Cu的保护效应,表明重金属的积累并不是总与毒性相关,这与BLM的假设不一致。
Contamination rarely occurs for single metals and is invariably due to complex mixtures in the environment. However, risk assessments of toxic compounds are routinely based upon effects evaluations of single substances. During recent years, the biotic ligand model (BLM) approach has gained widespread interest amongst the scientific, regulated and regulatory communities because of its potential for use in developing water quality criteria (WQC) and in performing risk assessments for metals. The BLM approach has significant implications for advances in the area of metal mixture risk assessment. Unfortunately, the BLM approach cannot yet be easily used to assess the effects in metal mixtures, which is more common. It is also unclear whether simple modifications of the BLM will be sufficient to account for such complex interactions. Therefore, the BLM should be used with caution when attempting to model metal interactions. Based on the development and theoretical basis of the biotic ligand model (BLM) overview, we examined the advantages and limitations in application of the BLM. Some important future research directions were identified. Based on the review we assessed the predictive capacities of two biotic ligand models (BLMs) for acute zinc toxicity to Daphnia magna as applied to a number of landscape waters from Tianjin and synthetic laboratory-prepared waters. To examine the possibility of extending the BLM approach to other organisms (or life stage), we tested the hypothesis that increased Ca2+ content increases the sensitivity of the developing embryos and larvae of zebrafish (Danio rerio) to Pb. And the aim of the study was to investigate the extent to which calcium can individually mitigate lead ion toxicity based on the concept of biotic ligand model (BLM). Embryos of the zebrafish were exposed to various Pb concentrations. Different chemical characteristics of water and some representative toxicological endpoints of zebrafish embryo were recorded. And general growth retardation as a major toxicological endpoint was used for analysis at 72 h due to its sensitivity and facility. After that, copper (Cu), an essential micronutrient and lead (Pb), a nonessential toxic metal, uptake by the unicellular green alga, Chlamydomonas reinhardtii, have been quantified in single metal exposures and in metal mixtures in order to test some of the key assumptions of the BLM. Furthermore, we tested the potential of the BLM to predict other biological effects, gene expression. Their responses to various combinations of Cu and Pb in the green algae C. reinhardtii were studied by following bioaccumulation and expression levels of genes known to be involved in the metal responses. The study concentrated on the expression levels of genes coding for natural resistance associated macrophage protein (nrampl), copper transporter (ctr2), oxidative stress responding gene-glutathione peroxidase (gpx5) and glutathione S-transferase (gsts2) after an exposure to Pb and Cu. The software of Visual MINTEQ (version 2.5.2) was employed to calculate the biotic ligand models and the chemical speciation in the solution. Results of this study can be used to help extend current predictive toxicity models (e.g. the BLM) to metal mixtures.
The results indicated that:
(1) Within these ranges of water chemistry parameters, the model based on toxicological data of acute zinc to Daphnia magna may be considered as a useful tool for taking into account bioavailability in regulatory assessments of zinc. This model generally predicted 80% effect concentrations by an error of less than a factor of 1.5. However, the predicted values of the acute Zn-BLM, which was developed in fish and subsequently adopted for Daphnia magna through downward adjustment of LA50 were normally lower than measured values. Acute toxicity to Daphnia magna (LC50) was underestimated by a factor 2 to 4. The method of adjusting the LA50 to extent the model applicability should be considered only the simplest means of calibrating the BLM, and might be suspected.
(2) The results showed that when Ca2+ concentration increased from 0.25 mmol/L to 2.00 mmol/L, the toxicity of lead on embryos of zebrafish (Danio rerio) decreased markedly after 72 h. And a large part of these decrease can be explained by the positive linear relations between EC50 {Pb2+}/EC50 [Pb]T (express as lead ion activity/dissolved total concentration) and activity/total concentration of Ca2+ through which the influence of Ca2+ on toxicity could be predicted. The results support the assumptions of the BLM and have often been associated with competition between lead and calcium for binding on transport and toxic action sites on biological surfaces. However, when Ca2+ concentration increased from 2.00 mmol/L to 4.00 mmol/L, the toxicity of lead on embryos of zebrafish (Danio rerio) seems to be constant at 72 h.
(3) Stability constants for the interaction of the metals with biological uptake sites by Chlamydomonas reinhardtii were determined from measured short term internalization fluxes. In the absence of competition, a value of 105.8M-1 was obtained for Cu while 105.9M-1 was obtained for Pb. Competition experiments did not show a straightforward antagonistic competition, as would be predicted by the BLM. Only at high Cu2+ concentrations (>1μM) did Cu behave as a competitive inhibitor of Pb transport. Surprisingly, low concentrations of Cu2+ had a synergistic effect on Pb uptake. Furthermore, Cu uptake was independent of Pb when Cu concentrations were below 10-7 M. In order to explain the observed discrepancies with the BLM, membrane permeability and Cu transporter expression levels were probed. The expression of ctr2, a gene coding for a Cu transporter, increased significantly in the presence of Pb, indicating that bioaccumulation is much more dynamic than assumed in the equilibrium models.
(4) The variability of interactive effects across genes suggests they are the product of intracellular feedback or regulatory processes specific to each gene and often binary metal combination. That is not consisting with one assumption of steady-state model:no significant biological regulation is induced by binding to sensitive sites, even in the short-term exposure experiments. Variable effect of different metal transporter (ctr2 and nrampl) suggested that the carrier molecule might possess regulatory and modification. The assumption of BLM considers biological effect as a function of metal uptake following bound amount of metal to the organism. Although the metal must first be accumulated before an effect is observed, it is oversimplification to link metal accumulation to proportional toxic effect. Besides that, protection effect of Cu suggesting that accumulation of heavy metals is not always related to their toxicity, which is not consistent with the assumption of BLM.
论文研究结果表明：
(1)在测试的水化学参数范围内,认为以锌对大型蚤的急性毒性数据建立起来的模型是一种有用的工具,能够在锌的生态风险评价中考虑生物有效性的问题,对所有水体(包括不同稀释倍数的水样)的预测结果与测试结果近似,80%的实测值在预测值67%-150%范围内。但以鱼类为基础开发的,通过下调LA50被应用于水蚤的急性Zn-BLM的预测值普遍高于实测值,其实测值为预测值的约2至4倍。通过调整LA50拓展模型适用性的方法过于简单,正受到质疑。
(2)当Ca2+浓度从0.25 mmol/L增加到2.00 mmol/L时,导致了以自由铅离子活度({Pb2+})和溶解态铅总浓度([Pb]T)表示的72-h EC5o的增加(表现为发育延迟),两者之间存在良好的线性关系。通过这一线性关系,可以对Ca2+浓度对铅毒性的影响进行预测。这一结果支持了生物配体模型(BLM)概念的假设,说明在胚胎的表面,铅离子与钙离子可能在传输和毒性作用位点上存在竞争作用。而当Ca2+浓度从2.00 mmol/L增加到4.00 mmol/L时,72-h EC50 {Pb2+}和72-h EC50 [Pb]T并没有显著的增加。
(3)Cu的稳定常数为105.8M-1,与Pb的常数(105.9M-1)相似。然而,竞争实验没有表现出直接的拮抗作用,这与BLM的预测不符。当Pb存在时,在高浓度条件下,Cu的积累会由于Pb的影响而降低,但当Cu的浓度低于10-7M时,Cu的积累不受Pb的影响。在高浓度的Cu(>1μM)条件下,Cu表现出竞争抑制；而在低Cu条件下,Cu对Pb的积累有协同效应,这种协同效应无法用BLM的观点解释。为了解释这一效应,进一步进行了细胞活动能力试验,膜渗透性试验以及基因表达试验。在Pb存在的条件下,ctr2(一段编码Cu传输位点的基因)的表达增加,表明生物积累是一个比模型假设更加复杂的动态过程。
(4)不同基因会产生不同的相互作用,表明每种基因都可能会产生其特异的细胞内的反馈与调节,这也会与不同的金属有关。这与稳定状态模型的一个假设不符：在敏感位点上不会引起显著的生物调节。即使在短时间的暴露实验中,仍然难以满足该假设。不同金属传输位点所出现的效应不同(ctr2和nrampl),表明传输分子发生了调解与改变。而且,BLM的假设认为金属的生物效应是由于金属富集在生物配体上所产生的,是金属积累的函数。虽然金属必须先积累在生物体中才能产生生物效应,但如仅简单认为金属的积累与其毒性效应之间存在着某种比例关系,这一假设显然太过于简单。Cu的保护效应,表明重金属的积累并不是总与毒性相关,这与BLM的假设不一致。
Contamination rarely occurs for single metals and is invariably due to complex mixtures in the environment. However, risk assessments of toxic compounds are routinely based upon effects evaluations of single substances. During recent years, the biotic ligand model (BLM) approach has gained widespread interest amongst the scientific, regulated and regulatory communities because of its potential for use in developing water quality criteria (WQC) and in performing risk assessments for metals. The BLM approach has significant implications for advances in the area of metal mixture risk assessment. Unfortunately, the BLM approach cannot yet be easily used to assess the effects in metal mixtures, which is more common. It is also unclear whether simple modifications of the BLM will be sufficient to account for such complex interactions. Therefore, the BLM should be used with caution when attempting to model metal interactions. Based on the development and theoretical basis of the biotic ligand model (BLM) overview, we examined the advantages and limitations in application of the BLM. Some important future research directions were identified. Based on the review we assessed the predictive capacities of two biotic ligand models (BLMs) for acute zinc toxicity to Daphnia magna as applied to a number of landscape waters from Tianjin and synthetic laboratory-prepared waters. To examine the possibility of extending the BLM approach to other organisms (or life stage), we tested the hypothesis that increased Ca2+ content increases the sensitivity of the developing embryos and larvae of zebrafish (Danio rerio) to Pb. And the aim of the study was to investigate the extent to which calcium can individually mitigate lead ion toxicity based on the concept of biotic ligand model (BLM). Embryos of the zebrafish were exposed to various Pb concentrations. Different chemical characteristics of water and some representative toxicological endpoints of zebrafish embryo were recorded. And general growth retardation as a major toxicological endpoint was used for analysis at 72 h due to its sensitivity and facility. After that, copper (Cu), an essential micronutrient and lead (Pb), a nonessential toxic metal, uptake by the unicellular green alga, Chlamydomonas reinhardtii, have been quantified in single metal exposures and in metal mixtures in order to test some of the key assumptions of the BLM. Furthermore, we tested the potential of the BLM to predict other biological effects, gene expression. Their responses to various combinations of Cu and Pb in the green algae C. reinhardtii were studied by following bioaccumulation and expression levels of genes known to be involved in the metal responses. The study concentrated on the expression levels of genes coding for natural resistance associated macrophage protein (nrampl), copper transporter (ctr2), oxidative stress responding gene-glutathione peroxidase (gpx5) and glutathione S-transferase (gsts2) after an exposure to Pb and Cu. The software of Visual MINTEQ (version 2.5.2) was employed to calculate the biotic ligand models and the chemical speciation in the solution. Results of this study can be used to help extend current predictive toxicity models (e.g. the BLM) to metal mixtures.
The results indicated that:
(1) Within these ranges of water chemistry parameters, the model based on toxicological data of acute zinc to Daphnia magna may be considered as a useful tool for taking into account bioavailability in regulatory assessments of zinc. This model generally predicted 80% effect concentrations by an error of less than a factor of 1.5. However, the predicted values of the acute Zn-BLM, which was developed in fish and subsequently adopted for Daphnia magna through downward adjustment of LA50 were normally lower than measured values. Acute toxicity to Daphnia magna (LC50) was underestimated by a factor 2 to 4. The method of adjusting the LA50 to extent the model applicability should be considered only the simplest means of calibrating the BLM, and might be suspected.
(2) The results showed that when Ca2+ concentration increased from 0.25 mmol/L to 2.00 mmol/L, the toxicity of lead on embryos of zebrafish (Danio rerio) decreased markedly after 72 h. And a large part of these decrease can be explained by the positive linear relations between EC50 {Pb2+}/EC50 [Pb]T (express as lead ion activity/dissolved total concentration) and activity/total concentration of Ca2+ through which the influence of Ca2+ on toxicity could be predicted. The results support the assumptions of the BLM and have often been associated with competition between lead and calcium for binding on transport and toxic action sites on biological surfaces. However, when Ca2+ concentration increased from 2.00 mmol/L to 4.00 mmol/L, the toxicity of lead on embryos of zebrafish (Danio rerio) seems to be constant at 72 h.
(3) Stability constants for the interaction of the metals with biological uptake sites by Chlamydomonas reinhardtii were determined from measured short term internalization fluxes. In the absence of competition, a value of 105.8M-1 was obtained for Cu while 105.9M-1 was obtained for Pb. Competition experiments did not show a straightforward antagonistic competition, as would be predicted by the BLM. Only at high Cu2+ concentrations (>1μM) did Cu behave as a competitive inhibitor of Pb transport. Surprisingly, low concentrations of Cu2+ had a synergistic effect on Pb uptake. Furthermore, Cu uptake was independent of Pb when Cu concentrations were below 10-7 M. In order to explain the observed discrepancies with the BLM, membrane permeability and Cu transporter expression levels were probed. The expression of ctr2, a gene coding for a Cu transporter, increased significantly in the presence of Pb, indicating that bioaccumulation is much more dynamic than assumed in the equilibrium models.
(4) The variability of interactive effects across genes suggests they are the product of intracellular feedback or regulatory processes specific to each gene and often binary metal combination. That is not consisting with one assumption of steady-state model:no significant biological regulation is induced by binding to sensitive sites, even in the short-term exposure experiments. Variable effect of different metal transporter (ctr2 and nrampl) suggested that the carrier molecule might possess regulatory and modification. The assumption of BLM considers biological effect as a function of metal uptake following bound amount of metal to the organism. Although the metal must first be accumulated before an effect is observed, it is oversimplification to link metal accumulation to proportional toxic effect. Besides that, protection effect of Cu suggesting that accumulation of heavy metals is not always related to their toxicity, which is not consistent with the assumption of BLM.
引文
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