Structural Basis for the Thermostability of Sulfur Oxygenase Reductases

›› 2012, Vol. 20 ›› Issue (1): 52-61.

Structural Basis for the Thermostability of Sulfur Oxygenase Reductases

尤晓颜¹, 孟珍², 陈栋炜¹, 郭旭¹, Josef Zeyer³, 刘双江¹, 姜成英¹

1. State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China;
2. Scientific Data Center, Computer Network Information Center, Chinese Academy of Sciences, Beijing 100190, China;
3. Environmental Microbiology, Institute for Biogeochemistry and Pollutant Dynamics(IBP), Federal Institute of Technology(ETH), Switzerland

收稿日期:2011-10-08 修回日期:2011-12-19 出版日期:2012-02-28 发布日期:2012-05-03
通讯作者: LIU Shuangjiang,E-mail:liusj@sun.im.ac.cn;JIANG Chengying,E-mail:jiangcy@im.ac.cn
基金资助:
Supported by the National Natural Science Foundation of China (31070042,30870039,30921065);partially by Open Funding Project of the National Key Laboratory of Biochemical Engineering,China (2010KF-2)

Structural Basis for the Thermostability of Sulfur Oxygenase Reductases

YOU Xiaoyan¹, MENG Zhen², CHEN Dongwei¹, GUO Xu¹, Josef Zeyer³, LIU Shuangjiang¹, JIANG Chengying¹

1. State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China;
2. Scientific Data Center, Computer Network Information Center, Chinese Academy of Sciences, Beijing 100190, China;
3. Environmental Microbiology, Institute for Biogeochemistry and Pollutant Dynamics(IBP), Federal Institute of Technology(ETH), Switzerland

Received:2011-10-08 Revised:2011-12-19 Online:2012-02-28 Published:2012-05-03
Supported by:
Supported by the National Natural Science Foundation of China (31070042,30870039,30921065);partially by Open Funding Project of the National Key Laboratory of Biochemical Engineering,China (2010KF-2)

摘要/Abstract

摘要： The thermostability of three sulfur oxygenase reductases(SORs) was investigated from thermoacidophilic achaea Acidianus tengchongensis(SOR_AT) and Sulfolobus tokodaii(SOR_ST) as well as the moderately thermophilic bacterium Acidithiobacillus sp.SM-1(SOR_SB).The optimal temperatures for catalyzing sulfur oxidation were 80℃(SORAT),85℃(SORST),and 70(SOR_SB),respectively.The half-lives of the three SORs at their optimal catalytic conditions were 100 min(SORAT),58 min(SOR_ST),and 37 min(SOR_SB).In order to reveal the structural basis of the thermostability of these SORs,three-dimensional structural models of them were generated by homology modeling using the previously reported high-resolution X-ray structure of SORAA(from Acidianus ambivalens) as a template.The results suggest that thermostability was dependent on:(a) high number of the charged amino acid glutamic acid and the flexible amino acid proline,(b) low number of the thermolabile amino acid glutamine,(c) increased number of ion pairs,(d) decreased ratio of hydrophobic accessible solvent surface area(ASA) to charged ASA,and(e) increased volumes of the cavity.The number of cavities and the number of hydrogen bonds did not significantly affect the thermostability of SORs,whereas the cavity volumes increased as the thermal stability increased.

关键词: sulfur oxygenase reductase(SOR), thermostability, homology modeling, Acidianus,Sulfolobus,Acid-ithiobacillus

Abstract: The thermostability of three sulfur oxygenase reductases(SORs) was investigated from thermoacidophilic achaea Acidianus tengchongensis(SOR_AT) and Sulfolobus tokodaii(SOR_ST) as well as the moderately thermophilic bacterium Acidithiobacillus sp.SM-1(SOR_SB).The optimal temperatures for catalyzing sulfur oxidation were 80℃(SORAT),85℃(SORST),and 70(SOR_SB),respectively.The half-lives of the three SORs at their optimal catalytic conditions were 100 min(SORAT),58 min(SOR_ST),and 37 min(SOR_SB).In order to reveal the structural basis of the thermostability of these SORs,three-dimensional structural models of them were generated by homology modeling using the previously reported high-resolution X-ray structure of SORAA(from Acidianus ambivalens) as a template.The results suggest that thermostability was dependent on:(a) high number of the charged amino acid glutamic acid and the flexible amino acid proline,(b) low number of the thermolabile amino acid glutamine,(c) increased number of ion pairs,(d) decreased ratio of hydrophobic accessible solvent surface area(ASA) to charged ASA,and(e) increased volumes of the cavity.The number of cavities and the number of hydrogen bonds did not significantly affect the thermostability of SORs,whereas the cavity volumes increased as the thermal stability increased.

Key words: sulfur oxygenase reductase(SOR), thermostability, homology modeling, Acidianus,Sulfolobus,Acid-ithiobacillus

中图分类号:

尤晓颜, 孟珍, 陈栋炜, 郭旭, Josef Zeyer, 刘双江, 姜成英. Structural Basis for the Thermostability of Sulfur Oxygenase Reductases[J]. , 2012, 20(1): 52-61.

YOU Xiaoyan, MENG Zhen, CHEN Dongwei, GUO Xu, Josef Zeyer, LIU Shuangjiang, JIANG Chengying. Structural Basis for the Thermostability of Sulfur Oxygenase Reductases[J]. , 2012, 20(1): 52-61.

参考文献

1 Britton,K.L.,Baker,P.J.,Borges,K.M.,Engel,P.C.,Pasquo,A.,Rice,D.W.,Robb,F.T.,Scandurra,R.,Stillman,T.J.,Yip,K.S.,"Insights into thermal stability from a comparison of the glutamate dehydrogenases from Pyrococcus furiosus and Thermococcus litoralis",Eur.J.Biochem.,229,688-695(1995).
2 Flam,F.,"The chemistry of life at the margins",Science,265,471-472(1994).
3 Kletzin,A.,"Molecular characterization of the sor gene,which encodes the sulfur oxygenase/reductase of the thermoacidophilic archaeum Desulfurolobus ambivalens",J.Bacteriol.,174,5854-5859 (1992).
4 He,Z.G.,Zhong,H.,Li,Y.,"Acidianus tengchongensis sp.nov.,a new species of acidothermophilic archaeon isolated from an acidothermal spring",Curr.Microbiol.,48,159-163(2004).
5 Liu,S.J.,"Archaeal and bacterial sulfur oxygenase-reductases:Genetic diversity and physiological function",In:Microbial Sulfur Metabolism,Springer-Verlag,Berlin(2008).
6 Deckert,G.,Warren,P.V.,Gaasterland,T.,Young,W.G.,Lenox,A.L.,raham,D.E.,Overbeek,R.,Snead,M.A.,Keller,M.,Aujay,M.,"The complete genome of the hyperthermophilic bacterium Aquifex aeolicus",Nature,392,353-358(1998).
7 Pelletier,N.,Leroy,G.,Guiral,M.,Giudici-Orticoni,M.T.,Aubert,C.,"First characterisation of the active oligomer form of sulfur oxygenase reductase from the bacterium Aquifex aeolicus",Extremophiles,12,205-215(2008).
8 Chen,Z.W.,Liu,Y.Y.,Wu,J.F.,She,Q.,Jiang,C.Y.,Liu,S.J.,"Novel bacterial sulfur oxygenase reductases from bioreactors treating gold-bearing concentrates",Appl.Microbiol.Biotechnol.,74,688-698(2007).
9 Li,M.,Chen,Z.W.,Zhang,P.,Pan,X.,Jiang,C.Y.,An,X.,Liu,S.J.,Chang,W.R.,"Crystal structure studies on sulfur oxygenase reductase from Acidianus tengchongensis",Biochem.Biophys.Res. Commun.,369,919-923(2008).
10 Urich,T.,Gomes,C.M.,Kletzin,A.,Frazao,C.,"X-ray structure of a self-compartmentalizing sulfur cycle metalloenzyme",Science,311,996-1000(2006).
11 Chen,Z.W.,Jiang,C.Y.,She,Q.,Liu,S.J.,Zhou,P.J.,"Key role of cysteine residues in catalysis and subcellular localization of sulfur oxygenase-reductase of Acidianus tengchongensis",Appl.Environ. Microbiol.,71,621-628(2005).
12 Suzuki,T.,Iwasaki,T.,Uzawa,T.,Hara,K.,Nemoto,N.,Kon,T.,Ueki,T.,Yamagishi,A.,Oshima,T.,"Sulfolobus tokodaii sp.nov.(f. Sulfolobus sp.strain 7),a new member of the genus Sulfolobus isolated from Beppu Hot Springs,Japan",Extremophiles,6,39-44 (2002).
13 Brock,T.D.,Brock,K.M.,Belly,R.T.,Weiss,R.L.,"Sulfolobus:A new genus of sulfur-oxidizing bacteria living at low pH and high temperature",Arch.Microbiol.,84,54-68(1972).
14 Allen,M.B.,"Studies with cyanidium caldarium,an anomalously pigmented chlorophyte",Arch.Microbiol.,32,270-277(1959).
15 Duquesne,K.,Lebrun,S.,Casiot,C.,Bruneel,O.,Personne,J.C.,Leblanc,M.,Elbaz-Poulichet,F.,Morin,G.,Bonnefoy,V.,"Immobilization of arsenite and ferric iron by Acidithiobacillus ferrooxidans and its relevance to acid mine drainage",Appl.Environ.Microbiol.,69,6165-6173,(2003).
16 Kletzin.A,"Coupled enzymatic production of sulfite,thiosulfate,and hydrogen sulfide from sulfur:purification and properties of a sulfur oxygenase reductase from the facultatively anaerobic archaebacterium Desulfurolobus ambivalens",J.Bacteriol.,171,1638-1643(1989).
17 DS Modeling 1.1,Accelrys Inc.,San Diego,CA,USA(2002).
18 Thompson,J.D.,Higgins,D.G.,Gibson,T.J.,"CLUSTAL W:improving the sensitivity of progressive multiple sequence alignment through sequence weighting,position-specific gap penalties and weight matrix choice",Nucleic Acids Res.,22,4673-4680(1994).
19 Laskowski,R.A.,Moss,D.S.,Thornton,J.M.,"PROCHECK:a program to check the stereo chemical quality of protein structures",J. Appl.Cryst.,26,283-291(1993).
20 Olszewski,K.A.,Yan,L.,Edwards,D.J.,"SeqFold—fully automated fold recognition and modeling software—evaluation and application",Theoretical Chemistry Accounts:Theory,Computation and Modeling(Theoretica Chimica Acta),101,57-61(1999).
21 Brooks,B.,Bruccoleri,R.,Olafson,B.,States,D.,Swaminathan,S.,Karplus,M.,"CHARMM:A program for macromolecular energy,minimization,and dynamics calculations",J.Comput.Chem.,4,187-217(1983).
22 Sippl,M.J.,"Recognition of errors in three-dimensional structures of proteins",Proteins,17,355-362(1993).
23 Hooft,R.W.,Vriend,G.,Sander,C.,Abola,E.E.,"Errors in protein structures",Nature,381,272(1996).
24 Connolly,M.L.,"Solvent-accessible surfaces of proteins and nucleic acids",Science,221,709-713(1983).
25 Kleywegt,G.J.,Jones,T.A.,"Detection,delineation,measurement and display of cavities in macromolecular structures",Acta Crystallogr.D Biol.Crystallogr.,50,178-185(1994).
26 Collaborative Computational Project Number 4,"The CCP4 suite: Programs for protein crystallography",Acta Cryst.D Biol.Cryst.,50,760-763(1994).
27 Chothia,C.,Lesk,A.M.,"The relation between the divergence of sequence and structure in proteins",Embo.J.,5,823-826(1986).
28 Lesk,A.M.,Chothia,C.,"How different amino acid sequences determine similar protein structures:the structure and evolutionary dynamics of the globins",J.Mol.Biol.,136,225-270(1980).
29 Sali,A.,"Comparative protein modeling by satisfaction of spatial restraints",Mol.Med.Today,1,270-277(1995).
30 Wiederstein,M.,Sippl,M.J.,"ProSA-web:interactive web service for the recognition of errors in three-dimensional structures of proteins",Nucleic Acids Res.,35,407-410(2007).
31 Gouet,P.,Courcelle,E.,Stuart,D.I.,Métoz,F.,"ESPript:analysis of multiple sequence alignments in PostScript",Bioinformatics,15,305-308(1999).
32 Argos,P.,Rossman,M.G.,Grau,U.M.,Zuber,H.,Frank,G.,Tratschin,J.D.,"Thermal stability and protein structure",Biochemistry,18,5698-5703(1979).
33 Bougault,C.M.,Eidsness,M.K.,Prestegard,J.H.,"Hydrogen bonds in rubredoxins from mesophilic and hyperthermophilic organisms",Biochemistry,42,4357-4372(2003).
34 Criswell,A.R.,Bae,E.,Stec,B.,Konisky,J.,Phillips,G.N.Jr.,"Structures of thermophilic and mesophilic adenylate kinases from the genus Methanococcus",J.Mol.Biol.,330,1087-1099(2003).
35 Perl,D.,Mueller,U.,Heinemann,U.,Schmid,F.X.,"Two exposed amino acid residues confer thermostability on a cold shock protein",Nat.Struct.Biol.,7,380-383(2000).
36 Szilagyi,A.,Zavodszky,P.,"Structural differences between mesophilic,moderately thermophilic and extremely thermophilic protein subunits:results of a comprehensive survey",Structure,8,493-504 (2000).
37 Tanner,J.J.,Hecht,R.M.,Krause,K.L.,Determinants of enzyme thermostability observed in the molecular structure of thermus aquaticus D-glyceraldehyde-3-phosphate dehydrogenase at 25 angstroms resolution",Biochemistry,35,2597-2609(1996).
38 Vieille,C.,Burdette,D.S.,Zeikus,J.G.,"Thermozymes",Biotechnol. Annu.Rev.,2,1-83(1996).
39 Vieille,C.,Zeikus,G.J.,"Hyperthermophilic enzymes:sources,uses,and molecular mechanisms for thermostability",Microbiol.Mol. Biol.Rev.,65,1-43(2001).
40 Russell,R.J.,Ferguson,J.M.,Hough,D.W.,Danson,M.J.,Taylor,G.L.,"The crystal structure of citrate synthase from the hyperther-mophilic archaeon pyrococcus furiosus at 1.9 A resolution",Biochemistry,36,9983-9994(1997).
41 Zhou,X.X.,Wang,Y.B.,Pan,Y.J.,Li,W.F.,"Differences in amino acids composition and coupling patterns between mesophilic and thermophilic proteins",Amino Acids,34,25-33(2008).
42 Facchiano,A.M.,Colonna,G.,Ragone,R.,"Helix stabilizing factors and stabilization of thermophilic proteins:an X-ray based study",Protein Eng.,11,753-760(1998).
43 Auerbach,G.,Ostendorp,R.,Prade,L.,Korndorfer,I.,Dams,T.,Huber,R.,Jaenicke,R.,"Lactate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima:the crystal structure at 2.1 A resolution reveals strategies for intrinsic protein stabilization",Structure,6,769-781(1998).
44 Hashimoto,H.,Inoue,T.,Nishioka,M.,Fujiwara,S.,Takagi,M.,Imanaka,T.,Kai,Y.,"Hyperthermostable protein structure maintained by intra and inter-helixion-pairs in archaeal O6-methylguanine-DNA methyltransferase",J.Mol.Biol.,292,707-716(1999).
45 Knapp,S.,Kardinahl,S.,Hellgren,N.,Tibbelin,G.,Schafer,G.,Ladenstein,R.,"Refined crystal structure of a superoxide dismutase from the hyperthermophilic archaeon Sulfolobus acidocaldarius at 2.2 A resolution",J.Mol.Biol.,285,689-702(1999).
[46] Chothia,C.,"Hydrophobic bonding and accessible surface area in proteins",Nature,248,338-339(1974).
[47] Knapp,S.,de Vos,W.M.,Rice,D.,Ladenstein,R.,"Crystal structure of glutamate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima at 3.0 A resolution",J.Mol.Biol.,267,916-932(1997).
[48] Karshikoff,A.,Ladenstein,R.,"Ion pairs and the thermotolerance of proteins from hyperthermophiles:a‘traffic rule’for hot roads",Trends Biochem.Sci.,26,550-556(2001).
[49] Szilagyi,A.,Zavodszky,P.,"Structural basis for the extreme thermostability of D-glyceraldehyde-3-phosphate dehydrogenase from Thermotoga maritima:analysis based on homology modelling",Protein Eng.,8,779-789(1995).
[50] Wang,X.,He,X.,Yang,S.,An,X.,Chang,W.,Liang,D.,"Structural basis for thermostability of beta-glycosidase from the thermophilic eubacterium Thermus nonproteolyticus HG102",J.Bacteriol.,185,4248-4255(2003).
[51] Sharp,K.A.,Honig,B.,"Electrostatic interactions in macromolecules:theory and applications",Annu.Rev.Biophys.Biophys.Chem.,19,301-332(1990).
[52] Stigter,D.,Dill,K.A.,"Charge effects on folded and unfolded proteins",Biochemistry,29,1262-1271(1990).
[53] He,X.Y.,Jin,C.,Zhang,S.Z.,Yang,S.J.,"Cloning and expression of a thermostable beta-glycosidase gene from Thermus nonproteolyticus HG102",Chinese Journal of Biotechnology,18,63-68 (2002).(in Chinese)
[54] Hennig,M.,Darimont,B.,Sterner,R.,Kirschner,K.,Jansonius,J.N.,"2.0 A structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus:possible determinants of protein stability",Structure,3,1295-1306(1995).
[55] Henrissat,B.,Davies,G.,"Structural and sequence-based classification of glycoside hydrolases",Curr.Opin.Struct.Biol.,7,637-644 (1997).

Structural Basis for the Thermostability of Sulfur Oxygenase Reductases

Structural Basis for the Thermostability of Sulfur Oxygenase Reductases

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