疣孢漆斑菌（Myrothecium verrucaria）NF-05漆酶的产生、特性及应用研究
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摘要
漆酶,即p-对苯二酚：双氧氧化还原酶(laccase,p-diphenol:dioxygen oxidoreductase, EC1.10.3.2),是一种多酚类氧化还原蛋白,属于蓝多铜氧化酶家族(blue multicopper oxidoreductase, BMCOs)。本研究从伊春凉水国家级自然保护区土壤样品中分离到一株漆酶高产真菌,纯化了胞外漆酶蛋白,考察了生化、酶学、光谱学及电化学性质,并进行了转化芳香类化合物及降解合成染料的应用研究,获得主要结果如下：
(1)漆酶高产真菌的分离鉴定
从土壤样品中筛选到一株具有胞外漆酶活性的真菌NF-05,菌丝白色绒毛状呈同心轮状扩散生长,分生孢子由黄色至淡绿色,最终为墨绿色胶黏团块状；显微形态分生孢子宽梭状,分生孢子梗单生或丛生,顶端帚状分枝较多,边缘菌丝卷曲状分枝,壁有疣状突起,分生孢子座座状或浅杯状,为半知菌亚门(Deuteromycotina)漆斑菌属(Myrothecium. sp)真菌；rDNA-ITS序列片段长度544bp,在NCBI数据库进行BLAST比对分析(accession number HM347341),结合形态学研究结果,鉴定为疣孢漆斑菌(M.verrucaria)。
(2)产酶条件的优化
M.verrucaria NF-05在产酶基础培养基中发酵至第五天达到产酶高峰,初始酶活8.38U/ml,菌丝生长与胞外漆酶分泌部分耦合。菌株产酶最适碳源为4%葡萄糖,3%蛋白胨,培养基初始pH值7.0,装液量60ml/250ml,接种量4%,最适培养条件为30℃下140rpm振荡培养,没食子酸及Fe3+对菌株产酶有显著促进作用,NF-05产酶水平提高至12.82U/ml。响应面法(RSM)优化中PB设计结果表明葡萄糖、Cu2+和没食子酸对菌株产酶有显著影响,经最陡爬坡试验及中心组合试验(CCD),葡萄糖浓度为26.47g/l,Cu2+和没食子酸浓度分别为236.3μM和138.4μM时,模型拟合方程有极大值19.82U/ml,是初始酶活的2.37倍。
(3)胞外漆酶的诱导
Cu2+在0.1-4mM范围内对NF-05胞外漆酶有显著诱导作用,最优浓度为0.2mM,发酵液漆酶活性43.23U/ml；16种供试酚类对菌株产酶有明显诱导作用,阿魏酸效果最好,酶活达到234.15U/ml；14种显著诱导菌株产酶的胺类物质中,3,3-二甲基-4,4-二氨基联苯使酶活提高至258.11U/ml；6种非酚胺类漆酶底物也对NF-05漆酶产生有显著诱导效果,木质素磺酸钠浓度为1mM时,发酵液漆酶活性为267.92U/ml,是目前报道的真菌漆酶活性最高值；4种染料显著诱导产酶,偶氮类丽春红效果最好,酶活从对照处理的43.23U/ml提高至61.16U/ml。
(4)蛋白的纯化与鉴定
以M.verrucaria NF-05发酵液为粗酶液,采用硫酸铵盐析、DEAE-SepharoseFast Flow阴离子交换层析和SephadexG-75凝胶过滤层析纯化,经SDS-PAGE和native-PAGE检测,目的片段为单体蛋白,具有漆酶活性,分子量66kDa。N端10个氨基酸序列为APQISPQYPM,结合基质辅助激光解吸电离飞行时间质谱(MALDI-TOF-/MS)对肽段序列的比对分析,鉴定所获M.verrucarid NF-05胞外目的蛋白为漆酶蛋白。
(5)光谱学特性
经电感耦合等离子体原子发射光谱(ICP-AES)测定,每个M.Verrucaria NF-05漆酶蛋白分子含铜离子3.08±0.3个,铁离子0.95±0.2个,二者比例为3：1。目的蛋白在300-650nm波长范围内全扫描,无特征吸收峰,顺磁共振(EPR)也未检测到磁性信号。我们推断M.Verrucaria NF-05漆酶蛋白中铜离子处于正一价态,全满状态的d10核外电子排布,不能产生d-d跃迁,易于电子传递,是造成光谱学“静默”的原因,也赋予NF-05漆酶异常高的酶活性。NF-05漆酶蛋白是一种活性中心金属组分及光谱学特性不同与已知报道的新白色漆酶。
(6)酶学特性
M.Verrucaria NF-05漆酶最适作用pH值4.0,最适作用温度40℃;Na+、 Mn2+、Cu2+和Zn2+对漆酶活性有显著促进；在5%供试有机溶剂中,漆酶活性保持在50%以上,常规蛋白抑制剂L-半胱氨酸、SDS、DTT和NaN3浓度为1mM时,酶活性基本丧失；卤族元素阴离子是供试漆酶特异性抑制剂；与常规漆酶底物ABTS亲和性较好,Km值为85.9μM。
(7)对合成染料的脱色与降解
偶氮类染料中,NF-05漆酶对橙黄Ⅰ和甲基橙脱色效果最好,无介体参与反应8天后脱色率即可达到90%以上；TE、VA和HBT对橙黄G6、ACE对苋菜红有明显促进脱色效果,脱色率达到90%以上。介体的参与可小幅提高NF-05漆酶对供试蒽醌类染料的脱色效率。芳甲烷类染料中碱性品红脱色效果最好。无介体参与并增大漆酶浓度后,反应10min时橙黄Ⅰ、铬黑T、碱性品红和苯酚红的特征吸收峰即完全被降解。
(8)对芳香酚胺的转化
NF-05漆酶对没食子酸等14种酚类底物、对氨基-N,N-二甲基苯胺等15种胺类底物及ABTS等6种非酚胺类底物的催化效率均高于两种对照商品酶。
(9)电化学性质
在充氮条件下,M.Verrucaria NF-05漆酶直接吸附于GP和GC裸电极上,与电极间均可进行直接电子转移,发生可逆的电化学反应；对过氧化氢的电催化还原效率均高于对照商品漆酶和胆红素氧化酶,过氧化氢氧化还原起始电势与裸电极相比均有明显正移。
Laccase (p-diphenol:dioxygen oxidoreductase, EC1.10.3.2) is a kind of multiphenolic oxidoreductase which belongs to the family of blue multicopper oxidoreductases. In this research, we isolated a laccase-producing fungus strain and reported a comprehensive investigation on the biochemical, spectral, enzymatic and electrochemical properties of the purified laccase protein. Further more, we also made some practical research on optimization and inducement of laccase production, declorisation and degradation of dyes together with transformation of phenols and amines. The major techniques and results of this research are as follows:
(1) Isolation and identification of laccase-producing strain
A fungus named NF-05with high laccase-producing ability was selected from soil sample. When cultured at30℃on a PDA plate for6days, the colony of NF-05was large, flat, rounded, with short and velvety white hyphae, white color on the surface and brown on the back. On the tenth day, light yellow spores emerged then turned to dark green and agglomerated. Strain NF-05was morphologically identified to deuteromycotina, Myrothecium. Combining with rDNA-ITS sequencing (544bp) and BLAST analysis (NCBI accession number HM347341), NF-05was identified as M.verrucaria.
(2) Optimization of laccase production
M.verrucaria NF-05reached the highest enzyme activity at8.38U/ml on the fifth day in basal medium, partially coupling with hyphae growing. Variance and multiple comparison analysis based on single factor experiments illustrated the optimum medium components and cultivation conditions were:4%glucose,3%peptone, initial pH value7.0, liquid volume60ml/250ml, inoculum4%,30℃and140rpm. Gallic acid and Fe3+significantly increased laccase production of NF-05. Laccase activity reached to12.82U/ml owing to single factor experiments. Response surface methodology was performed for further optimization. Plackett Burman design indicated the significant effects of glucose, Cu2+and gallic acid on laccase production process. Central composite design was preceded based on steepest ascent experiment. A fitting equation was achieved and testified with the maximum laccase activity at19.82U/ml, which was2.37fold of the initial value. The optimum concentration of glucose, Cu2+and gallic acid were26.47g/L,236.3μM and138.4μM, respectively.
(3) Inducement of extracellular laccase
Variance and multiple comparison analysis illustrated that Cu2+in range of 0.1-4.0mM significantly increased laccase production of NF-05. The laccase activity was43.23U/ml with0.2mM Cu2+as inducers. Sixteen tested phenols remarkably induced laccase-producing process, especially ferulic acid with the enzyme activity of234.15U/ml.3,3'-dimethylbiphenyl-4,4'-diamine was the best inducer with the enzyme activity at258.11U/ml among all the14amines which exerted significant inducement on extracellular laccase of NF-05. Another six substrates also increased laccase production, the best among which was sodium lignosulphonate. The laccase activity was267.92U/ml which was the highest level of microbial laccase so far. Four synthetic dyes showed remarkable positive effects for laccase inducement particularly Ponceau S.
(4) Purification and identification of target protein
Target protein was purified from the fermentation liquid of strain NF-05via salting out of (NH4)2SO4，anion change chromatography of DEAE-sepharose fast flow and filtration chromatography of sephadexG-75gel. SDS-PAGE and native-PAGE revealed that the purified protein was a monomer with a molecular weight of66kDa which oxidized ABTS to green band. The first ten amino acid sequences were APQISPQYPM. Together with the peptide analysis based on matrix-assisted laser desorption/ionization time of fight mass spectrometry, the purified protein was identified as laccase protein.
(5) Spectral properties
The average numbers of copper and fermium ions were3.08±0.3and0.95±0.2per protein molecule respectively, resulting in the ratio of3:1. The ultraviolet-visible scan figure among300-650nm showed no absorption peak. Further more, there was no obvious signal in electron paramagnanetic resonance detection. In view of the "silence" spectral properties, it could be deduced that the lack of absorption in visible light range and absence of EPR signal probably resulted from the existence of incomplete oxidation state of copper (Cu+), which had a fully occupied electron configuration of d10and no d-d transition could take place. The incomplete oxidation of metal ions might confer the easiness of electron transfer in active center of the laccase and also render the protein extra high activity. Consequently, NF-05laccase was a white laccase with new metal composition and spectral properties.
(6) Enzymatic properties
The optimum catalyze condition of NF-05laccase was pH4.0,40℃. Na+, Mn2+Cu2+and Zn2+significantly increased enzyme activity at specific concentration. The protein maintained more than50%activity in presence of5%tested organic solvent. Regular protein inhibitors such as L-cysteine, SDS, DTT and Na3N almost totally inhibited enzyme activity at the concentration of1mM. Halogen anions were special inhibitors for NF-05laccase. NF-05laccase showed great intimacy to ABTS with a Km value of85.9μM.
(7) Decolorization and degradation of synthetic dyes
Among azo dyes, more than90%of orange I and methyl orange was decolorized by NF-05laccase without mediators. Decolorization rate of orange G6reached to more than90%in TE, VA or HBT mediated system; ACE could well mediate the decolorisation system of amaranth. Mediators could increase the decolorisation rate for anthraquinone dyes to a less extent. The decolorisation rate of basic fuchsin was59.33%, which was the highest among all tested arylmethane dyes without mediators. Malachite green was the second best arylmethane dyes decolorized by NF-05laccase. PZ mediated system could increase the decolorization rate from48.68%to91.42%. NF-05laccase could not efficiently decolorize the tested dyes of other structure types. The decolorization systems under higher enzyme concentration and without mediators involvement were scanned under400-700nm. The specific absorption peaks of orange I, eriochrome black T, fuchsin basic and phenol red were almost totally degraded within10min.
(8) Transformation of phenols and amines
Comparison studies of catalyzing phenols and amines by NF-05laccase and control commercial oxidoreductases (laccase and bilirubin oxidase) were conducted. The reaction was coupled with4-aminoantipyrine and referenced by phenol. NF-05laccase exerted higher transforming efficiency of14phenols,15amines and6other type substrates than control enzymes.
(9) Electrochemical properties
Under the nitrogen saturation condition, M.verrucaria NF-05could directly absorb on GP and GC electrodes. Obvious redox peak was observed which indicated the occurrence of direct electron transfer and quasi-reversible electrochemical reaction. On GP electrode, the Epa and Epc were-0.026V and0.028V, respectively.△Ep was54mM and E0' was1mV. On GC electrode, thea and Epc were-0.027V and0.01V, respectively.△Ep was37mM and E0' was-8.5mV. The transmormfation efficiencies of peroxide electrocatalyzed by M.verrucaria NF-05lascase were higher than control commercial enzymes on both GP and GC electrodes.
(1)漆酶高产真菌的分离鉴定
从土壤样品中筛选到一株具有胞外漆酶活性的真菌NF-05,菌丝白色绒毛状呈同心轮状扩散生长,分生孢子由黄色至淡绿色,最终为墨绿色胶黏团块状；显微形态分生孢子宽梭状,分生孢子梗单生或丛生,顶端帚状分枝较多,边缘菌丝卷曲状分枝,壁有疣状突起,分生孢子座座状或浅杯状,为半知菌亚门(Deuteromycotina)漆斑菌属(Myrothecium. sp)真菌；rDNA-ITS序列片段长度544bp,在NCBI数据库进行BLAST比对分析(accession number HM347341),结合形态学研究结果,鉴定为疣孢漆斑菌(M.verrucaria)。
(2)产酶条件的优化
M.verrucaria NF-05在产酶基础培养基中发酵至第五天达到产酶高峰,初始酶活8.38U/ml,菌丝生长与胞外漆酶分泌部分耦合。菌株产酶最适碳源为4%葡萄糖,3%蛋白胨,培养基初始pH值7.0,装液量60ml/250ml,接种量4%,最适培养条件为30℃下140rpm振荡培养,没食子酸及Fe3+对菌株产酶有显著促进作用,NF-05产酶水平提高至12.82U/ml。响应面法(RSM)优化中PB设计结果表明葡萄糖、Cu2+和没食子酸对菌株产酶有显著影响,经最陡爬坡试验及中心组合试验(CCD),葡萄糖浓度为26.47g/l,Cu2+和没食子酸浓度分别为236.3μM和138.4μM时,模型拟合方程有极大值19.82U/ml,是初始酶活的2.37倍。
(3)胞外漆酶的诱导
Cu2+在0.1-4mM范围内对NF-05胞外漆酶有显著诱导作用,最优浓度为0.2mM,发酵液漆酶活性43.23U/ml；16种供试酚类对菌株产酶有明显诱导作用,阿魏酸效果最好,酶活达到234.15U/ml；14种显著诱导菌株产酶的胺类物质中,3,3-二甲基-4,4-二氨基联苯使酶活提高至258.11U/ml；6种非酚胺类漆酶底物也对NF-05漆酶产生有显著诱导效果,木质素磺酸钠浓度为1mM时,发酵液漆酶活性为267.92U/ml,是目前报道的真菌漆酶活性最高值；4种染料显著诱导产酶,偶氮类丽春红效果最好,酶活从对照处理的43.23U/ml提高至61.16U/ml。
(4)蛋白的纯化与鉴定
以M.verrucaria NF-05发酵液为粗酶液,采用硫酸铵盐析、DEAE-SepharoseFast Flow阴离子交换层析和SephadexG-75凝胶过滤层析纯化,经SDS-PAGE和native-PAGE检测,目的片段为单体蛋白,具有漆酶活性,分子量66kDa。N端10个氨基酸序列为APQISPQYPM,结合基质辅助激光解吸电离飞行时间质谱(MALDI-TOF-/MS)对肽段序列的比对分析,鉴定所获M.verrucarid NF-05胞外目的蛋白为漆酶蛋白。
(5)光谱学特性
经电感耦合等离子体原子发射光谱(ICP-AES)测定,每个M.Verrucaria NF-05漆酶蛋白分子含铜离子3.08±0.3个,铁离子0.95±0.2个,二者比例为3：1。目的蛋白在300-650nm波长范围内全扫描,无特征吸收峰,顺磁共振(EPR)也未检测到磁性信号。我们推断M.Verrucaria NF-05漆酶蛋白中铜离子处于正一价态,全满状态的d10核外电子排布,不能产生d-d跃迁,易于电子传递,是造成光谱学“静默”的原因,也赋予NF-05漆酶异常高的酶活性。NF-05漆酶蛋白是一种活性中心金属组分及光谱学特性不同与已知报道的新白色漆酶。
(6)酶学特性
M.Verrucaria NF-05漆酶最适作用pH值4.0,最适作用温度40℃;Na+、 Mn2+、Cu2+和Zn2+对漆酶活性有显著促进；在5%供试有机溶剂中,漆酶活性保持在50%以上,常规蛋白抑制剂L-半胱氨酸、SDS、DTT和NaN3浓度为1mM时,酶活性基本丧失；卤族元素阴离子是供试漆酶特异性抑制剂；与常规漆酶底物ABTS亲和性较好,Km值为85.9μM。
(7)对合成染料的脱色与降解
偶氮类染料中,NF-05漆酶对橙黄Ⅰ和甲基橙脱色效果最好,无介体参与反应8天后脱色率即可达到90%以上；TE、VA和HBT对橙黄G6、ACE对苋菜红有明显促进脱色效果,脱色率达到90%以上。介体的参与可小幅提高NF-05漆酶对供试蒽醌类染料的脱色效率。芳甲烷类染料中碱性品红脱色效果最好。无介体参与并增大漆酶浓度后,反应10min时橙黄Ⅰ、铬黑T、碱性品红和苯酚红的特征吸收峰即完全被降解。
(8)对芳香酚胺的转化
NF-05漆酶对没食子酸等14种酚类底物、对氨基-N,N-二甲基苯胺等15种胺类底物及ABTS等6种非酚胺类底物的催化效率均高于两种对照商品酶。
(9)电化学性质
在充氮条件下,M.Verrucaria NF-05漆酶直接吸附于GP和GC裸电极上,与电极间均可进行直接电子转移,发生可逆的电化学反应；对过氧化氢的电催化还原效率均高于对照商品漆酶和胆红素氧化酶,过氧化氢氧化还原起始电势与裸电极相比均有明显正移。
Laccase (p-diphenol:dioxygen oxidoreductase, EC1.10.3.2) is a kind of multiphenolic oxidoreductase which belongs to the family of blue multicopper oxidoreductases. In this research, we isolated a laccase-producing fungus strain and reported a comprehensive investigation on the biochemical, spectral, enzymatic and electrochemical properties of the purified laccase protein. Further more, we also made some practical research on optimization and inducement of laccase production, declorisation and degradation of dyes together with transformation of phenols and amines. The major techniques and results of this research are as follows:
(1) Isolation and identification of laccase-producing strain
A fungus named NF-05with high laccase-producing ability was selected from soil sample. When cultured at30℃on a PDA plate for6days, the colony of NF-05was large, flat, rounded, with short and velvety white hyphae, white color on the surface and brown on the back. On the tenth day, light yellow spores emerged then turned to dark green and agglomerated. Strain NF-05was morphologically identified to deuteromycotina, Myrothecium. Combining with rDNA-ITS sequencing (544bp) and BLAST analysis (NCBI accession number HM347341), NF-05was identified as M.verrucaria.
(2) Optimization of laccase production
M.verrucaria NF-05reached the highest enzyme activity at8.38U/ml on the fifth day in basal medium, partially coupling with hyphae growing. Variance and multiple comparison analysis based on single factor experiments illustrated the optimum medium components and cultivation conditions were:4%glucose,3%peptone, initial pH value7.0, liquid volume60ml/250ml, inoculum4%,30℃and140rpm. Gallic acid and Fe3+significantly increased laccase production of NF-05. Laccase activity reached to12.82U/ml owing to single factor experiments. Response surface methodology was performed for further optimization. Plackett Burman design indicated the significant effects of glucose, Cu2+and gallic acid on laccase production process. Central composite design was preceded based on steepest ascent experiment. A fitting equation was achieved and testified with the maximum laccase activity at19.82U/ml, which was2.37fold of the initial value. The optimum concentration of glucose, Cu2+and gallic acid were26.47g/L,236.3μM and138.4μM, respectively.
(3) Inducement of extracellular laccase
Variance and multiple comparison analysis illustrated that Cu2+in range of 0.1-4.0mM significantly increased laccase production of NF-05. The laccase activity was43.23U/ml with0.2mM Cu2+as inducers. Sixteen tested phenols remarkably induced laccase-producing process, especially ferulic acid with the enzyme activity of234.15U/ml.3,3'-dimethylbiphenyl-4,4'-diamine was the best inducer with the enzyme activity at258.11U/ml among all the14amines which exerted significant inducement on extracellular laccase of NF-05. Another six substrates also increased laccase production, the best among which was sodium lignosulphonate. The laccase activity was267.92U/ml which was the highest level of microbial laccase so far. Four synthetic dyes showed remarkable positive effects for laccase inducement particularly Ponceau S.
(4) Purification and identification of target protein
Target protein was purified from the fermentation liquid of strain NF-05via salting out of (NH4)2SO4，anion change chromatography of DEAE-sepharose fast flow and filtration chromatography of sephadexG-75gel. SDS-PAGE and native-PAGE revealed that the purified protein was a monomer with a molecular weight of66kDa which oxidized ABTS to green band. The first ten amino acid sequences were APQISPQYPM. Together with the peptide analysis based on matrix-assisted laser desorption/ionization time of fight mass spectrometry, the purified protein was identified as laccase protein.
(5) Spectral properties
The average numbers of copper and fermium ions were3.08±0.3and0.95±0.2per protein molecule respectively, resulting in the ratio of3:1. The ultraviolet-visible scan figure among300-650nm showed no absorption peak. Further more, there was no obvious signal in electron paramagnanetic resonance detection. In view of the "silence" spectral properties, it could be deduced that the lack of absorption in visible light range and absence of EPR signal probably resulted from the existence of incomplete oxidation state of copper (Cu+), which had a fully occupied electron configuration of d10and no d-d transition could take place. The incomplete oxidation of metal ions might confer the easiness of electron transfer in active center of the laccase and also render the protein extra high activity. Consequently, NF-05laccase was a white laccase with new metal composition and spectral properties.
(6) Enzymatic properties
The optimum catalyze condition of NF-05laccase was pH4.0,40℃. Na+, Mn2+Cu2+and Zn2+significantly increased enzyme activity at specific concentration. The protein maintained more than50%activity in presence of5%tested organic solvent. Regular protein inhibitors such as L-cysteine, SDS, DTT and Na3N almost totally inhibited enzyme activity at the concentration of1mM. Halogen anions were special inhibitors for NF-05laccase. NF-05laccase showed great intimacy to ABTS with a Km value of85.9μM.
(7) Decolorization and degradation of synthetic dyes
Among azo dyes, more than90%of orange I and methyl orange was decolorized by NF-05laccase without mediators. Decolorization rate of orange G6reached to more than90%in TE, VA or HBT mediated system; ACE could well mediate the decolorisation system of amaranth. Mediators could increase the decolorisation rate for anthraquinone dyes to a less extent. The decolorisation rate of basic fuchsin was59.33%, which was the highest among all tested arylmethane dyes without mediators. Malachite green was the second best arylmethane dyes decolorized by NF-05laccase. PZ mediated system could increase the decolorization rate from48.68%to91.42%. NF-05laccase could not efficiently decolorize the tested dyes of other structure types. The decolorization systems under higher enzyme concentration and without mediators involvement were scanned under400-700nm. The specific absorption peaks of orange I, eriochrome black T, fuchsin basic and phenol red were almost totally degraded within10min.
(8) Transformation of phenols and amines
Comparison studies of catalyzing phenols and amines by NF-05laccase and control commercial oxidoreductases (laccase and bilirubin oxidase) were conducted. The reaction was coupled with4-aminoantipyrine and referenced by phenol. NF-05laccase exerted higher transforming efficiency of14phenols,15amines and6other type substrates than control enzymes.
(9) Electrochemical properties
Under the nitrogen saturation condition, M.verrucaria NF-05could directly absorb on GP and GC electrodes. Obvious redox peak was observed which indicated the occurrence of direct electron transfer and quasi-reversible electrochemical reaction. On GP electrode, the Epa and Epc were-0.026V and0.028V, respectively.△Ep was54mM and E0' was1mV. On GC electrode, thea and Epc were-0.027V and0.01V, respectively.△Ep was37mM and E0' was-8.5mV. The transmormfation efficiencies of peroxide electrocatalyzed by M.verrucaria NF-05lascase were higher than control commercial enzymes on both GP and GC electrodes.
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