生物资源  2017, Vol. 39 Issue (6): 398-405  DOI: 10.14188/j.ajsh.2017.06.002

引用本文  

霍颖异, 戎振, 许学伟. 细菌SGNH家族水解酶的研究进展[J]. 生物资源, 2017, 39(6): 398-405.
HUO Yingyi, RONG Zhen, XU Xuewei. Progress in bacterial SGNH family hydrolases[J]. Biotic Resources, 2017, 39(6): 398-405.

基金项目

国家自然科学基金(41506183;31770004)

通讯联系人

许学伟, E-mail:xuxw@sio.org.cn

作者简介

霍颖异(1984-),女,副研究员,博士,现主要从事酯类水解酶的结构与功能研究。E-mail:yingyihuo@gmail.com

文章历史

收稿日期:2017-09-29
修回日期:2017-10-25
细菌SGNH家族水解酶的研究进展
霍颖异 , 戎振 , 许学伟     
国家海洋局 第二海洋研究所/海洋生态系统与生物地球化学重点实验室,浙江 杭州 310012
0
摘要:SGNH水解酶家族是一类在四个保守序列区上具有严格保守催化残基Ser、Gly、Asn和His的水解酶,该家族水解酶广泛存在于真核生物和原核生物中。细菌来源的SGNH水解酶家族具有来源广泛、功能多样且催化机制独特等特点,在细菌致病性、碳源代谢和天然产物合成等方面发挥重要生物学功能,在医药、化工、生物燃料和环境修复等领域具有广泛的应用潜力。本文从氨基酸序列、蛋白结构特征、酶学催化机制、细菌生理功能及应用领域等方面对细菌来源的SGNH水解酶家族成员进行综述。
关键词SGNH水解酶家族    细菌    晶体结构    催化机制    应用潜力    
Progress in bacterial SGNH family hydrolases
Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration,
Abstract: The SGNH hydrolase family consists of enzymes possessing four strictly conserved catalytic residues Ser, Gly, Asn and His in four conserved blocks, respectively, which are widespread in eukaryotes and prokaryotes. Bacterial SGNH family hydrolases are widely distributed and versatile with unique catalytic mechanisms. They play important roles in many biological processes such as bacterial virulence, carbon source metabolism and natural product synthesis. The enzymes also cover a broad spectrum of biotechnological applications in medicine, chemical engineering, biofuel, environmental bioremendiation, etc. The present review describes the amino acid sequence, protein structure, catalytic mechanism, physiological function and application potential of bacterial SGNH family hydrolases.
Key words: SGNH hydrolase family    bacterium    crystal structure    catalytic mechanism    application potential    
0 引言

SGNH水解酶家族因在四个保守序列区上具有四个严格保守残基Ser(S)、Gly(G)、Asn(N)和His(H)而得名,其由Upton和Buckley[1]首次鉴定保守序列特征,由MØlgaard等提出名称[2]。SGNH家族水解酶广泛存在于细菌[3~5]、真菌[1, 6]、植物[7~9]、哺乳动物[10, 11]和病毒[12, 13]中,其底物谱广泛,具有羧酸酯酶、脂肪酶、蛋白酶、硫酯酶、溶血磷脂酶、芳基酯酶、酰基转移酶等多种活性,可参与细菌毒力和植物生长发育、形态发生以及防御等多种生理功能[14, 15]

随着二代测序技术快速发展以及测序成本不断降低,越来越多的全基因组被测序和注释,特别是微生物基因组,数据库中已保藏大量SGNH家族水解酶基因序列。截至2017年9月19日,NCBI(http://www.ncbi.nlm.nih.gov)数据库中已有44.4万条SGNH家族水解酶蛋白记录,其中39.0万条为细菌来源,3.3万条为植物来源。然而,目前SGNH家族水解酶的研究多针对植物来源的酶,针对微生物来源的SGNH家族水解酶的研究仍十分有限。本文针对微生物SGNH水解酶家族成员的氨基酸序列、蛋白结构特征、酶催化机制、微生物生理功能及应用领域进行较为全面的综述,旨在为进一步深入研究该家族蛋白提供基础。

1 SGNH家族水解酶的氨基酸序列特征

SGNH水解酶家族成员的氨基酸序列含有五个保守序列区(blocks Ⅰ~Ⅴ),在其中四个保守序列区上(blocks Ⅰ,Ⅱ,Ⅲ和Ⅴ)各具有一个在催化反应中发挥关键作用的保守残基Ser、Gly、Asn和His[1, 2] (图 1)。与α/β水解酶家族催化残基Ser位于氨基酸序列中部的Gly-X-Ser-X-Gly五肽保守序列不同,SGNH水解酶家族的催化残基Ser位于靠近氨基酸序列N端的Gly-Asp-Ser-Leu (X)保守序列中,因此,SGNH水解酶家族又被称为GDSL家族[2, 14]。通常保守残基Ser、His及Asp(或Glu)共同组成了催化三联体(catalytic triad),其中Ser和His分别为亲核残基和碱性残基,Ser、Gly和Asn则共同参与了氧阴离子洞(oxyanion hole)的形成[14]。SGNH家族水解酶催化三联体中的酸性残基Asp或Glu常位于His残基之前三位,但该位点并不完全保守于所有该家族水解酶中,有些SGNH家族水解酶不具有催化三联体酸性残基[3, 16](图 1)。

图 1 SGNH家族水解酶氨基酸序列比对图 Figure 1 Sequence alignment of four conserved blocks in the SGNH-hydrolase family 注:序列包括大肠杆菌(Escherichia coli) TAP(PDB code:1IVN),铜绿假单胞菌(Pseudomonas aeruginosa) TesA(PDB code:4JGG),铜绿假单胞菌EstA(PDB code:3KVN),土霉素链霉菌(Streptomyces rimosus) SrLip(PDB code:5MAL)和疥疮链霉菌(S. scabies) SsEst(PDB code:1ESC)。氨基酸序列位置序号以1IVN为参考。蓝框表示一致和相似残基。一致和相似残基分别以红底白字和白底红字表示。黑框表示SGNH家族保守序列区Block Ⅰ、Ⅱ、Ⅲ和Ⅴ。黑色实心圆表示SGNH家族的典型严格保守残基Ser、Gly、Asn和His的位置。红色和蓝色实心三角表示催化三联体和氧阴离子洞的位置 Note: selected sequences include E. coli TAP (PDB code: 1IVN), P. aeruginosa TesA (PDB code: 4JGG), P. aeruginosa EstA (PDB code: 3KVN), S. rimosus SrLip (PDB code: 5MAL) and S. scabies SsEst (PDB code: 1ESC). Identical and similar residues are boxed by blue lines. Identical and similar residues are shown as white letters with red background and red letters with white background, respectively. Four consensus blocks Ⅰ, Ⅱ, Ⅲ and Ⅴ are boxed by black lines. The catalytic triad and oxyanion hole residues are indicated by red and blue filled triangles, respectively
2 SGNH家族水解酶的三维结构特征

SGNH家族水解酶常具有多功能性的独特性质,其催化机制是科学家关注的焦点。认识酶的结构特征是研究其催化机制的基础,蛋白质三维结构解析更是研究酶催化机制的有效手段。目前,SGNH水解酶家族中已有19个细菌来源的蛋白晶体结构被成功解析和发表(表 1)。

表 1 结构已知的细菌来源SGNH家族水解酶 Table 1 Bacterial SGNH hydrolases with known crystal structures

来源于大肠杆菌(Escherichia coli)的TAP因其多功能性成为最受关注且研究最为深入的SGNH家族水解酶。该蛋白的晶体结构于2003年被成功解析,分辨率达到1.9 Å[4]。它具有典型的SGNH家族水解酶三维结构,其中心为平行的β-折叠,β-折叠两侧覆盖若干α-螺旋,构成α/β/α折叠结构(图 2A)。序列保守区Block I中的亲核残基Ser位于N末端第一个α-螺旋和第一个β-折叠之间的刚性区域,序列保守区Block V中的碱性残基His和酸性残基Asp/Glu位于C末端α-螺旋前的柔性环上(图 2A)。残基Ser的侧链羟基与His咪唑环上的亚氨基形成氢键,His咪唑环上另一个亚氨基又与Asp/Glu侧链羧基形成氢键用于稳定His咪唑环构象,三个氨基酸残基共同组成催化三联体。

图 2 SGNH家族水解酶三维结构飘带图 Figure 2 Cartoon representation of SGNH family hydrolases 注:A, 大肠杆菌TAP(PDB code:1IVN),α-螺旋和β-折叠折叠分别以蓝色和绿色表示,催化三联点以棍状模型表示。B, 铜绿假单胞菌EstA(PDB code:3KVN),乘客结构域以蓝色表示,β桶状结构域以绿色表示,两结构域的连接α-螺旋以红色表示,催化三联点以棍状模型表示 Note:A, structure of Escherichia coli TAP (PDB code: 1IVN). The α helices and β strands are colored in blue and green, respectively. The catalytic triad residues are indicated as stick models colored in green. B, structure of Pseudomonas aeruginosa EstA (PDB code: 3KVN). The passenger domain, β-barrel domain and the connecting helix are colored in blue, green and red, respectively. The catalytic triad residues are indicated as stick models

还有一类以致病菌铜绿假单胞菌(Pseudomonas aeruginosa)的EstA[24]为代表的特殊SGNH家族水解酶,该类蛋白为自转运蛋白,由两部分组成:一个N端具有催化功能的SGNH乘客结构域和一个C端具有自转运蛋白功能的β桶状结构域(图 2B)。β桶状结构域又由12个连续的β-折叠构成跨膜β桶状结构和一条位于β桶状结构内腔的α-螺旋构成。

3 SGNH家族水解酶的催化机制 3.1 SGNH家族水解酶催化一般机制

SGNH家族水解酶催化作用于酯键,其催化过程符合丝氨酸水解酶的一般机制[32~34]:底物进入催化口袋时,残基Ser羟基上的质子H+转移至残基His咪唑环,残基Ser的羟基亲核攻击底物的羰基C原子(图 3A); 底物羰基双键断裂,形成瞬间的四面体复合物,其中羰基O2-负离子通过与氧阴离子洞的主链-NH-形成氢键而稳定(图 3B); His咪唑环上的质子H转移至酯键的醇羟基,酯键断裂生成游离醇,羰基O与氧阴离子洞的氢键打开,羰基与质子化的丝氨酸重新形成氢键从而形成稳定的酰基-酶共价中间体复合物(图 3C); 残基His又从水分子获取质子H+,被激活的水分子羟基攻击底物羰基C(图 3C),再次形成四面体复合物(图 3D),His再次转移质子H+至Ser的O2-负离子,释放游离羧基化合物(图 3E)。

图 3 SGNH家族水解酶催化机制[34] Figure 3 Mechanism of the hydrolysis reaction of ester bonds catalyzed by SGNH family hydrolases[34] 注:催化三联体和水分子以黑色表示,氧阴离子洞以蓝色表示,底物以红色表示。A, Ser的羟基亲核攻击底物羰基C; B, 四面体复合物; C, 游离醇生成,形成酰基-酶共价中间体复合物,水分子亲核攻击底物羰基C; D, 四面体复合物; E, 游离羧基化合物和酶 Note: catalytic triad and water are shown in black; the oxyanion hole residues are in blue; the substrate is in red. A, nucleophilic attack of the serine hydroxyl on the carbonyl carbon of the substrate; B, tetrahedral intermediate; C, free alcohol, acyl-enzyme intermediate and nucleophilic attack by water; D, tetrahedral intermediate; E, free carboxylic acid and enzyme
3.2 底物结合诱导的构象变化

底物结合口袋构象的可变性,可能使其可以结合更广泛的底物,从而赋予SGNH家族水解酶的多功能性。以大肠杆菌TAP为例,分子动力学分析显示,其中心β-折叠和长α-螺旋是刚性的,而底物结合口袋表现出高度可变性,从而使该底物结合口袋可以通过构象改变结合多种底物[35]。因此,TAP具有硫酯酶、羧酸酯酶、芳基酯酶、蛋白酶和溶血磷脂酶等多功能性。这一现象与诱导契合理论(induced-fit theory)相符,即虽然酶活性中心的原始结构并不完全适合底物,但由于活性中心附近结构的可变性,底物的结合诱导活性中心结构改变,从而使活性中心结构与底物匹配[36]。而SGNH家族水解酶被不同底物结合诱导的不同构象变化,还需更多的酶-底物复合体结构数据支持和验证。

3.3 三个氨基酸残基构成的氧阴离子洞

与大部分丝氨酸水解酶的氧阴离子洞由两个氨基酸残基组成不同,SGNH家族水解酶的氧阴离子洞常由三个严格保守氨基酸残基(Ser、Gly和Asn)组成。以E. coli TAP为例,蛋白三维结构显示,其氧阴离子洞由残基Ser10、Gly44和Asn73组成,每个残基彼此距离超过3.5 Å,说明当底物结合在氧阴离子洞时,三个残基都是高度极化的[4]。而TAP中缺少大部分丝氨酸水解酶中存在的催化碱性残基His咪唑环C原子与蛋白质主链羰基之间的氢键。三个高度极化残基构成的氧阴离子洞的存在补偿了催化残基His与主链羰基之间无氢键的问题。同时,一个独特的氢键网络也为活性中心提供了稳定性,这说明SGNH家族水解酶可能具有与常见丝氨酸水解酶不同的催化机制[4]

3.4 催化二联体

一种与典型丝氨酸水解酶催化三联体不同的催化二联体(catalytic dyad)已在多个SGNH家族水解酶中被发现[3, 16, 20, 30],但催化二联体的催化机制仍不明确。1995年,Wei等[16]在来源于马铃薯致病菌疥疮链霉菌(Streptomyces scabies)的酯酶SsEst中首次发现SGNH水解酶家族催化二联体(Ser14和His283)现象,其活性中心附近没有保守的酸性氨基酸Asp和Glu,而His283咪唑环亚氨基与Trp280主链羰基O之间形成氢键,这个氢键可能补偿了催化酸性氨基酸稳定His咪唑环构象的作用。在大肠杆菌中也发现了具有催化二联体的9-O-唾液酸酯酶NanS(9-O-acetyl N-acetylneuraminic acid esterase),蛋白质三维结构分析结合突变体实验排除了催化中心附近氨基酸成为第三个催化残基的可能性[20]。在微白黄链霉菌(S. albidoflavus)的SaPLA1[30]和龟裂链霉菌(S. rimosus)的SrLip[3]蛋白质三维结构中也发现了催化二联体中His咪唑环构象由其与主链羰基O之间的氢键稳定,同时,分子动力学分析也揭示了SrLip催化二联体的催化过程。

4 SGNH家族水解酶的功能与应用

SGNH家族水解酶具有底物广泛和多功能性的独特性质,使其发挥多种生理功能,也具有广泛的应用潜力。虽然细菌来源SGNH家族水解酶生理功能仍有待深入研究,针对部分蛋白的现有研究已经让我们对其生理功能的重要性有了初步认识。同时,SGNH家族水解酶催化底物谱非常广泛,且具有嗜热[37]、热稳定[38~40]、冷适应[41, 42]、碱性[37]、耐盐[5]、耐有机溶剂[40]、手性催化[43]等优良特性,在医疗、食品、洗涤、农业、造纸、纺织、化工、生物燃料、环境修复和科学研究等诸多领域具有广泛的应用潜力。下面列举部分SGNH家族水解酶的生理功能和应用潜力。

在细菌致病性方面,SGNH家族水解酶通过多种机制参与细菌致病过程,从而在药物开发中具有应用潜力。首先,致病菌铜绿假单胞菌TesA可解毒外源溶血磷脂,同时还可通过改变磷脂的不饱和脂肪酸量调节细胞膜流动性[23]; 嗜肺性军团病杆菌(Legionella pneumophila)的PlaA可解毒溶血磷脂胆碱[44]。它们可作为良好细菌来源溶血磷脂解毒剂。其次,牛莫拉氏杆菌(Moraxella bovis)产生的酶PLB具有磷脂酶B(phospholipase B)的活性,它可能在牛角膜炎(infectious bovine keratoconjunctivitis,IBK)的感染发病中发挥作用。IBK是一种在家畜中传染性很强的眼部疾病,可导致角膜溃烂甚至暂时或永久性失明,对其催化和致病机制的深入研究可在未来牛角膜炎的预防和治疗方面得到应用[45]。再次,生物大分子的乙酰化修饰在细菌致病中发挥重要作用。致病菌铜绿假单胞菌海藻酸盐乙酰酯酶(alginate acetylesterase)AlgX和AlgJ是参与胞外多糖海藻酸盐合成的乙酰转移酶,它们通过对海藻酸盐的乙酰化修饰,使生物膜的细胞更好的附着于囊肿性纤维化肺病患者的肺上皮细胞,并使其可以抵抗宿主免疫系统和抗生素的影响[22, 46]。真核宿主溶菌酶水解细菌细胞壁肽聚糖是其抵抗细菌入侵的第一道防线,脑膜炎奈瑟式菌(Neisseria meningitidis)中发现的肽聚糖乙酰酯酶通过对肽聚糖的乙酰化修饰避免其被溶菌酶水解[19, 47]。针对这类蛋白的三维结构和催化机制研究可为靶向药物的开发提供基础。

在碳源代谢及其应用方面,脱乙酰作用常参与生物大分子的降解及其碳源代谢,也参与病原微生物的毒力相关功能。大肠杆菌中的唾液酸酯酶NanS催化唾液酸的脱乙酰反应,使大肠杆菌可利用唾液酸作为碳源和氮源[20]。如嗜热脂肪土芽胞杆菌(Geobacillus stearothermophilus)Axe2[48]、嗜热纤维梭菌(Clostridium thermocellum)CtCes3[28]以及来源于瘤胃的解蛋白丁酸弧菌(Butyrivibrio proteoclasticus)Est2A[26]参与微生物对植物细胞壁多糖木质素降解和利用的重要生理过程,可应用于基于木质纤维素类的生物燃料的生产。

在药物合成应用方面,酰基转移酶和脱乙酰基酶常参与天然产物的生物合成,链霉菌(Streptomyces sp.)的水杨酰酰基转移酶(salicylyl-acyltransferase)SsfX3参与生物合成四环素类抗癌天然药物SF2575[31]。另外,脱乙酰头孢菌素是半合成β-内酰胺类抗生素工业生产的重要原料。这类化合物由7-氨基头孢烷酸(7-aminocephalosporanic acid,7-ACA)脱乙酰化生成。目前已经发现一些细菌产生的SGNH家族水解酶具有7-氨基头孢烷酸脱乙酰基酶(7-ACA deacetylase)活性,包括芽胞杆菌(Bacillus sp.)CAH[49]、枯草芽胞杆菌(B. subtilis)YesT[50]和腾冲脂环酸芽胞杆菌(Alicyclobacillus tengchongensis)EstD1[51],可被应用于β-内酰胺类抗生素的合成。

在环境污染修复应用方面,邻苯二甲酸二异丁酯(diisobutyl phthalate,DiBP)是一种常用的增塑剂,但易引起水体和陆地环境污染,也对哺乳动物有毒性。芽胞杆菌K91 CarEW可水解DiBP的两个酯键,可应用于DiBP污染环境的修复[52]

此外,来源于致病菌铜绿假单胞菌的自转运蛋白EstA参与鼠李糖脂生物表面活性剂的产生,鼠李糖脂生物表面活性剂是免疫细胞的毒力因子,同时它还影响细胞运动性和生物膜形成[53, 54]。自转运蛋白已被应用于将靶蛋白功能性表达并定位于细菌表面,从而构建细菌表面展示系统,用于靶蛋白研究或应用,如免疫激活细胞分选技术(fluorescence-activated cell sorting, FACS)[54]

5 结语与展望

SGNH家族水解酶来源广泛、功能多样、催化机制独特且应用潜力广泛,然而目前针对细菌来源SGNH家族水解酶的研究还十分有限,还有很多科学问题尚待解答。例如,已研究的细菌SGNH家族水解酶多来源于病原、淡水和土壤环境,海洋作为生物基因资源的宝藏,海洋细菌来源SGNH家族水解酶资源有待进一步挖掘和研究; 不同SGNH家族水解酶之间具有显著的序列和功能差异,它们的系统发育关系和演化过程仍不明确,可靠的分类方式也有待建立; 已知细菌SGNH家族水解酶具有多功能性,但其生理功能还极少被揭示,其在生命活动过程中实际发挥的生理功能仍需更多研究来验证和明确。此外,近年来不断有新的细菌SGNH家族水解酶催化机制被阐释,相信随着更多蛋白晶体结构被解析和研究,对细菌SGNH家族水解酶催化机制的科学认识将得到进一步完善。在充分挖掘基因资源、明确了解生理功能和详细阐释催化机制的基础上,细菌来源SGNH家族水解酶未来将有更广阔的应用前景。

参考文献
[1]
Upton C, Buckley J T. A new family of lipolytic enzymes?[J]. Trends Biochem Sci, 1995, 20(5): 178. DOI:10.1016/S0968-0004(00)89002-7
[2]
Mølgaard A, Kauppinen S, Larsen S. Rhamnogalacturonan acetylesterase elucidates the structure and function of a new family of hydrolases[J]. Structure, 2000, 8(4): 373. DOI:10.1016/S0969-2126(00)00118-0
[3]
Lešči ć Ašler I, Štefani ć Z, Maršavelski A, et al. The catalytic dyad in the SGNH hydrolase superfamily: in-depth insight into structural parameters tuning the catalytic process of extracellular lipase from Streptomyces rimosus[J]. ACS Chem Biol, 2017, 12(7): 1928-1936. DOI:10.1021/acschembio.6b01140
[4]
Lo Y C, Lin S C, Shaw J F, et al. Crystal structure of Escherichia coli thioesterase I/protease I/lysophospholipase L1: consensus sequence blocks constitute the catalytic center of SGNH-hydrolases through a conserved hydrogen bond network[J]. J Mol Biol, 2003, 330(3): 539-551. DOI:10.1016/S0022-2836(03)00637-5
[5]
Wang G, Wang Q, Lin X, et al. A novel cold-adapted and highly salt-tolerant esterase from Alkalibacterium sp. SL3 from the sediment of a soda lake[J]. Sci Rep, 2016, 6: 19494. DOI:10.1038/srep19494
[6]
Ma J, Lu Q, Yuan Y, et al. Crystal structure of isoamyl acetate-hydrolyzing esterase from Saccharomyces cerevisiae reveals a novel active site architecture and the basis of substrate specificity[J]. Proteins, 2011, 79(2): 662-668. DOI:10.1002/prot.v79.2
[7]
Lai C P, Huang L M, Chen L O, et al. Genome-wide analysis of GDSL-type esterases/lipases in Arabidopsis[J]. Plant Mol Biol, 2017, 6: 1-17.
[8]
Zhang B, Zhang L, Li F, et al. Control of secondary cell wall patterning involves xylan deacetylation by a GDSL esterase[J]. Nat Plants, 2017, 3(3): 17017. DOI:10.1038/nplants.2017.17
[9]
Bitto E, Bingman C A, McCoy J G, et al. The structure at 1.6 Å resolution of the protein product of the At4g34215 gene from Arabidopsis thaliana[J]. Acta Crystallogr D Biol Crystallogr, 2005, 61(Pt 12): 1655-1655.
[10]
Ho Y S, Swenson L, Derewenda U, et al. Brain acetylhydrolase that inactivates platelet-activating factor is a G-protein-like trimer[J]. Nature, 1997, 385(6611): 89-93. DOI:10.1038/385089a0
[11]
Tarricone C, Perrina F, Monzani S, et al. Coupling PAF signaling to dynein regulation : structure of LIS1 in complex with PAF-acetylhydrolase[J]. Neuron, 2004, 44(5): 809-821.
[12]
Zeng Q, Langereis M A, Vliet A L W V, et al. Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution[J]. Proc Natl Acad Sci U S A, 2008, 105(26): 9065-9069. DOI:10.1073/pnas.0800502105
[13]
Langereis M A, Zeng Q, Gerwig G J, et al. Structural basis for ligand and substrate recognition by torovirus hemagglutinin esterases[J]. Proc Natl Acad Sci U S A, 2009, 106(37): 15897-15902. DOI:10.1073/pnas.0904266106
[14]
Akoh C C, Lee G C, Liaw Y C, et al. GDSL family of serine esterases/lipases[J]. Prog Lipid Res, 2004, 43(6): 534. DOI:10.1016/j.plipres.2004.09.002
[15]
Leic' A I, Ivic' N, Kovaic' F, et al. Probing enzyme promiscuity of SGNH hydrolases[J]. ChemBioChem, 2010, 11(15): 2158. DOI:10.1002/cbic.v11:15
[16]
Wei Y, Schottel J L, Derewenda U, et al. A novel variant of the catalytic triad in the Streptomyces scabies esterase[J]. Nat Struct Biol, 1995, 2(3): 218-223. DOI:10.1038/nsb0395-218
[17]
Kim K, Ryu B H, Kim S S, et al. Structural and biochemical characterization of a carbohydrate acetylesterase from Sinorhizobium meliloti 1021[J]. FEBS Lett, 2015, 589(1): 117-122. DOI:10.1016/j.febslet.2014.11.033
[18]
Oh C, Ryu B H, An D R, et al. Structural and biochemical characterization of an octameric carbohydrate acetylesterase from Sinorhizobium meliloti[J]. FEBS Lett, 2016, 590(8): 1242-1252. DOI:10.1002/1873-3468.12135
[19]
Williams A H, Veyrier F J, Bonis M, et al. Visualization of a substrate-induced productive conformation of the catalytic triad of the Neisseria meningitidis peptidoglycan O-acetylesterase reveals mechanistic conservation in SGNH esterase family members[J]. Acta Crystallogr D Biol Crystallogr, 2014, 70(Pt 10): 2631-2639.
[20]
Rangarajan E S, Ruane K M, Proteau A, et al. Structural and enzymatic characterization of NanS (YjhS), a 9-O-Acetyl N-acetylneuraminic acid esterase from Escherichia coli O157:H7[J]. Protein Sci, 2011, 20(7): 1208-1219. DOI:10.1002/pro.v20.7
[21]
Brzuszkiewicz A, Norwak E, Dauter Z, et al. Structure of EstA esterase from psychrotrophic Pseudoalteromonas sp. 643A covalently inhibited by monoethylphosphonate[J]. Acta Crystallogr, 2009, 65(9): 862-865.
[22]
Riley L M, Weadge J T, Baker P, et al. Structural and functional characterization of Pseudomonas aeruginosa AlgX: role of AlgX in alginate acetylation[J]. J Biol Chem, 2013, 288(31): 22299-22314. DOI:10.1074/jbc.M113.484931
[23]
Kovaic' F, Granzin J, Wilhelm S, et al. Structural and functional characterisation of TesA -a novel lysophospholipase A from Pseudomonas aeruginosa[J]. PLoS One, 2013, 8(7): e69125. DOI:10.1371/journal.pone.0069125
[24]
van den Berg B. Crystal structure of a full-length autotransporter[J]. J Mol Biol, 2010, 396(3): 627-633. DOI:10.1016/j.jmb.2009.12.061
[25]
Lansky S, Alalouf O, Solomon H V, et al. A unique octameric structure of Axe2, an intracellular acetyl-xylooligosaccharide esterase from Geobacillus stearothermophilus[J]. Acta Crystallogr D Biol Crystallogr, 2014, 70(Pt 2): 261-278.
[26]
Till M, Goldstone D C, Attwood G T, et al. Structure and function of an acetyl xylan esterase (Est2A) from the rumen bacterium Butyrivibrio proteoclasticus[J]. Proteins, 2013, 81(5): 911-917. DOI:10.1002/prot.v81.5
[27]
Montanier C, Money V A, Pires V M, et al. The active site of a carbohydrate esterase displays divergent catalytic and noncatalytic binding functions[J]. PLoS Biol, 2009, 7(3): e71.
[28]
Correia M A, Prates J A, Brás J, et al. Crystal structure of a cellulosomal family 3 carbohydrate esterase from Clostridium thermocellum provides insights into the mechanism of substrate recognition[J]. J Mol Biol, 2008, 379(1): 64-72. DOI:10.1016/j.jmb.2008.03.037
[29]
Mathews I, Soltis M, Saldajeno M, et al. Structure of a novel enzyme that catalyzes acyl transfer to alcohols in aqueous conditions[J]. Biochemistry, 2009, 46(31): 8969-8979.
[30]
Pickens L B, Sawaya M R, Rasool H, et al. Structural and biochemical characterization of the salicylyl-acyltranferase SsfX3 from a tetracycline biosynthetic pathway[J]. J Biol Chem, 2011, 286(48): 41539-41551. DOI:10.1074/jbc.M111.299859
[31]
Murayama K, Kano K, Matsumoto Y, et al. Crystal structure of phospholipase A1 from Streptomyces albidoflavus NA297[J]. J Struct Biol, 2013, 182(2): 192-196. DOI:10.1016/j.jsb.2013.02.003
[32]
Jaeger K E, Dijkstra B W, Reetz M T. Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases[J]. Annu Rev Microbiol, 1999, 53(1): 315-351. DOI:10.1146/annurev.micro.53.1.315
[33]
Montella I R, Schama R, Valle D. The classification of esterases: an important gene family involved in insecticide resistance—a review[J]. Mem Inst Oswaldo Cruz, 2012, 107(4): 437-449. DOI:10.1590/S0074-02762012000400001
[34]
Ribeiro B D, Castro A M D, Coelho M A Z, et al. Production and use of lipases in bioenergy: a review from the feedstocks to biodiesel production[J]. Enzyme Res, 2011, 2011(1): 615803.
[35]
Huang Y T, Liaw Y C, Gorbatyuk V Y, et al. Backbone dynamics of Escherichia coli thioesterase/protease I: evidence of a flexible active-site environment for a serine protease[J]. J Mol Biol, 2001, 307(4): 1075-1090. DOI:10.1006/jmbi.2001.4539
[36]
Koshland D E. Application of a theory of enzyme specificity to protein synthesis[J]. Proc Natl Acad Sci U S A, 1958, 44(2): 98. DOI:10.1073/pnas.44.2.98
[37]
Yu T, Ding J, Zheng Q, et al. Identification and characterization of a new alkaline SGNH hydrolase from a thermophilic bacterium Bacillus sp. K91[J]. J Microbiol Biotechnol, 2016, 26(4): 730-738. DOI:10.4014/jmb.1507.07101
[38]
Yang Z, Yong Z, Shen T, et al. Cloning, expression and biochemical characterization of a novel, moderately thermostable GDSL family esterase from Geobacillus thermodenitrificans T2[J]. J of Biosci Bioeng, 2013, 115(2): 133. DOI:10.1016/j.jbiosc.2012.08.016
[39]
Soni S, Sathe S S, Odaneth A A, et al. SGNH hydrolase-type esterase domain containing Cbes-AcXE2: a novel and thermostable acetyl xylan esterase from Caldicellulosiruptor bescii[J]. Extremophiles, 2017, 21(4): 687-697. DOI:10.1007/s00792-017-0934-2
[40]
Gururaj P, Ramalingam S, Nandhini Devi G, et al. Process optimization for production and purification of a thermostable, organic solvent tolerant lipase from Acinetobacter sp. AU07[J]. Braz J Microbiol, 2016, 47(3): 647-657. DOI:10.1016/j.bjm.2015.04.002
[41]
Wicka M, Wanarska M, Krajewska E, et al. Cloning, expression, and biochemical characterization of a cold-active GDSL-esterase of a Pseudomonas sp. S9 isolated from Spitsbergen island soil[J]. Acta Biochim Pol, 2016, 63(1): 117-125. DOI:10.18388/abp.2015_1074
[42]
Shakiba M H, Ali M S, Rahman R N, et al. Cloning, expression and characterization of a novel coldadapted GDSL family esterase from Photobacterium sp. strain J15[J]. Extremophiles, 2016, 20(1): 44-55.
[43]
Deng D, Zhang Y, Sun A, et al. Functional characterization of a novel marine microbial GDSL lipase and its utilization in the resolution of (±)-1-phenylethanol[J]. Appl Biochem Biotechnol, 2016, 179(1): 75-93. DOI:10.1007/s12010-016-1980-4
[44]
Flieger A, Neumeister B, Cianciotto N P. Characterization of the gene encoding the major secreted lysophospholipase A of Legionella pneumophila and its role in detoxification of lysophosphatidylcholine[J]. Infect Immun, 2002, 70(11): 6094-6106. DOI:10.1128/IAI.70.11.6094-6106.2002
[45]
Farn J L, Strugnell R A, Hoyne P A, et al. Molecular characterization of a secreted enzyme with phospholipase B activity from Moraxella bovis[J]. J Bacteriol, 2001, 183(22): 6717-6720. DOI:10.1128/JB.183.22.6717-6720.2001
[46]
Baker P, Ricer T, Moynihan P J, et al. P. aeruginosa SGNH hydrolase-like proteins AlgJ and AlgX have similar topology but separate and distinct roles in alginate acetylation[J]. PLoS Pathog, 2014, 10(8): e1004334. DOI:10.1371/journal.ppat.1004334
[47]
Weadge J T, Clarke A J. Identification and characterization of O-acetylpeptidoglycan esterase: a novel enzyme discovered in Neisseria gonorrhoeae[J]. Biochemistry, 2006, 45(3): 839-851. DOI:10.1021/bi051679s
[48]
Lansky S, Alalouf O, Solomon V, et al. Crystallization and preliminary crystallographic analysis of Axe2, an acetylxylan esterase from Geobacillus stearothermophilus[J]. Acta Crystallogr Sect F Struct Biol Cryst Commun, 2013, 69(Pt 4): 430-434.
[49]
Choi D H, Kim Y D, Chung I S, et al. Gene cloning and expression of cephalosporin-C deacetylase from Bacillus sp. KCCM10143[J]. J Microbiol Biotechnol, 2000, 10(2): 221-226.
[50]
Martinez-Martinez I, Navarro-Fernandez J, Daniel Lozada-Ramirez J, et al. YesT: a new rhamnogalacturonan acetyl esterase from Bacillus subtilis[J]. Proteins, 2008, 71(1): 379-388. DOI:10.1002/(ISSN)1097-0134
[51]
Ding J M, Yu T T, Han N Y, et al. Identification and characterization of a new 7-aminocephalosporanic acid deacetylase from thermophilic bacterium Alicyclobacillus tengchongensis[J]. J Bacteriol, 2015, 198(2): 311-320.
[52]
Ding J, Wang C, Xie Z, et al. Properties of a newly identified esterase from Bacillus sp. K91 and its novel function in diisobutyl phthalate degradation[J]. PLoS One, 2015, 10(3): e0119216. DOI:10.1371/journal.pone.0119216
[53]
Wilhelm S, Gdynia A, Tielen P, et al. The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation[J]. J Bacteriol, 2007, 189(18): 6695-6703. DOI:10.1128/JB.00023-07
[54]
Wilhelm S, Rosenau F, Kolmar H, et al. Autotransporters with GDSL passenger domains: molecular physiology and biotechnological applications[J]. Chem Bio Chem, 2011, 12(10): 1476-1485. DOI:10.1002/cbic.v12.10