Cloning, Expression, and Characterization of a Cold-Adapted Shikimate Kinase from the Psychrophilic Bacterium Colwellia psychrerythraea 34H

Wahyu Sri Kunto  Nugroho; Dong-Woo  Kim; Jong-Cheol  Han; Young Baek  Hur; Soo-Wan  Nam  and Hak Jun  Kim

doi:10.4014/jmb.1608.08049

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Biotechnology and Bioengineering (BB) | Enzyme, Protein Engineering, and Metabolic Engineering

Cloning, Expression, and Characterization of a Cold-Adapted Shikimate Kinase from the Psychrophilic Bacterium Colwellia psychrerythraea 34H

Wahyu Sri Kunto Nugroho ¹, Dong-Woo Kim ¹, Jong-Cheol Han ², Young Baek Hur ², Soo-Wan Nam ³ and Hak Jun Kim ^1*

¹Department of Chemistry, Pukyong National University, Busan 48547, Republic of Korea, ²Southeast Sea Fisheries Research Institute, National Fisheries Research and Development Institute, Tongyeong 53085, Republic of Korea, ³Department of Biotechnology and Bioengineering, Dong-Eui University, Busan 47340, Republic of Korea

Received: August 24, 2016; Accepted: September 5, 2016

J. Microbiol. Biotechnol. 2016; 26(12): 2087-2097

Published December 28, 2016 https://doi.org/10.4014/jmb.1608.08049

Abstract

Most cold-adapted enzymes possess higher Km and kcat values than those of their mesophilic counterparts to maximize the reaction rate. This characteristic is often ascribed to a high structural flexibility and improved dynamics in the active site. However, this may be less convincing to cold-adapted metabolic enzymes, which work at substrate concentrations near Km. In this respect, cold adaptation of a shikimate kinase (SK) in the shikimate pathway from psychrophilic Colwellia psychrerythraea (CpSK) was characterized by comparing it with a mesophilic Escherichia coli homolog (EcSK). The optimum temperatures for CpSK and EcSK activity were approximately 30°C and 40°C, respectively. The melting points were 33°C and 45°C for CpSK and EcSK, respectively. The ΔGH2O (denaturation in the absence of denaturing agent) values were 3.94 and 5.74 kcal/mol for CpSK and EcSK, respectively. These results indicated that CpSK was a cold-adapted enzyme. However, contrary to typical kinetic data, CpSK had a lower Km for its substrate shikimate than most mesophilic SKs, and the kcat was not increased. This observation suggested that CpSK may have evolved to exhibit increased substrate affinity at low intracellular concentrations of shikimate in the cold environment. Sequence analysis and homology modeling also showed that some important salt bridges were lost in CpSK, and higher Arg residues around critical Arg 140 seemed to increase flexibility for catalysis. Taken together, these data demonstrate that CpSK exhibits characteristics of cold adaptation with unusual kinetic parameters, which may provide important insights into the cold adaptation of metabolic enzymes.

Keywords

cold adaptation, shikimate kinase, psychrophile, The Michaelis-Menten constant, turnover number

References

Ásgeirsson B, Cekan P. 2006. Microscopic rate-constants for substrate binding and acylation in cold-adaptation of trypsin I from Atlantic cod. FEBS Lett. 580: 4639-4644.
Bentahir M. 2000. Structural, kinetic, and calorimetric characterization of the cold-active phosphoglycerate kinase from the antarctic Pseudomonas sp. TACII18. J. Biol. Chem. 275: 11147-11153.
Cerasoli E, Kelly SM, Coggins JR, Boam DJ, Clarke DT, Price NC. 2002. The refolding of type II shikimate kinase from Erwinia chrysanthemi a ft er d enat urat ion in u rea. Eur. J. Biochem. 269: 2124-2132.
Cheng W-C, Chang Y-N, Wang W-C. 2005. Structural basis for shikimate-binding specificity of Helicobacter pylori shikimate kinase. J. Bacteriol. 187: 8156-8163.
Cheng W-C, Chen Y-F, Wang H-J, Hsu K-C, Lin S-C, Chen T-J, et al. 2012. Structures of Helicobacter pylori shikimate kinase reveal a selective inhibitor-induced-fit mechanism. PLoS One 7: e33481.
Collins T, Meuwis M-A, Stals I, Claeyssens M, Feller G, Gerday C. 2002. A novel family 8 xylanase, functional and physicochemical characterization. J. Biol. Chem. 277: 3513335139.
Coracini JD, de Azevedo WF. 2014. Shikimate kinase, a protein target for drug design. Curr. Med. Chem. 21: 592-604.
D’Amico S, Claverie P, Collins T, Georlette D, Gratia E, Hoyoux A, et al. 2002. Molecular basis of cold adaptation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 917-925.
D’Amico S, Collins T, Marx J-C, Feller G, Gerday C. 2006. Psychrophilic microorganisms: challenges for life. EMBO Rep. 7: 385-389.
DeFeyt er RC, P it t ard J. 1 986. P urification a nd p ropert ies of shikimate kinase II from Escherichia coli K-12. J. Bacteriol. 165: 331-333.
DeLano WL. 2002. The PyMOL Molecular Graphics System. Accessible at http://www.pymol.org.
De Santi C, Tedesco P, Ambrosino L, Altermark B, Willassen N-P, de Pascale D. 2014. A new alkaliphilic cold-active esterase from the psychrophilic marine bacterium Rhodococcus sp.: functional and structural studies and biotechnological potential. Appl. Biochem. Biotechnol. 172: 3054-3068.
Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang J-M, et al. 2011. T-Coffee: a Web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39: W13-W17.
Feller G, Gerday C. 1997. Psychrophilic enzymes: molecular basis of cold adaptation. Cell. Mol. Life Sci. 53: 830-841.
Feller G, Narinx E, Arpigny JL, Ait taleb M, Baise E, Genicot S, et al. 1996. Enzymes from psychrophilic organisms. FEMS Microbiol. Rev. 18: 189-202.
Feller G, Zekhnini Z, Lamotte-Brasseur J, Gerday C. 1997. Enzymes from cold-adapted microorganisms - t he c lass C beta-lactamase from the antarctic psychrophile Psychrobacter Immobilis A5. Eur. J. Biochem. 244: 186-191.
Fucile G, Garcia C, Carlsson J, Sunnerhagen M, Christendat D. 2011. Structural and biochemical investigation of two Arabidopsis s hikimat e kinases: t he h eat -inducible i soform i s thermostable. Protein Sci. 20: 1125-1136.
Gan J , Gu Y , Li Y , Yan H, J i X. 2 006. C ryst al s t ructure of Mycobacterium tuberculosis shikimate kinase in complex with shikimic acid and an ATP analogue. Biochemistry 45: 85398545.
Genicot S, Feller G, Gerday C. 1988. Trypsin from antarctic fish (Paranotothenia magellanica forster) as compared with trout (Salmo gairdneri) trypsin. Comp. Biochem. Physiol. B 90:601-609.
Georlette D, Bentahir M, Claverie P, Collins T, D’Amico S, Delille D, et al. 2002. Physics and Chemistry Basis of Biotechnology. Springer Netherlands, Dordrecht.
Greenfield NJ. 2006. Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat. Protoc. 1: 2527-2535.
Han C, Zhang J, Chen L, Chen K, Shen X, Jiang H. 2007. Discovery of Helicobacter pylori shikimate kinase inhibitors:bioassay and molecular modeling. Bioorg. Med. Chem. 15:656-662.
Herrmann KM, Weaver LM. 1999. The shikimate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 473-503.
Hoyoux A, Jennes I, Dubois P, Genicot S, Dubail F, François JM, et al. 2001. Cold-adapted beta-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis. Appl. Environ. Microbiol. 67: 1529-1535.
Jahandideh M, Barkooie SMH, Jahandideh S, Abdolmaleki P, Movahedi MM, Hoseini S, et al. 2008. Elucidating the protein cold-adaptation: investigation of the parameters enhancing protein psychrophilicity. J. Theor. Biol. 255: 113-118.
Kaufmman S (ed.). 1987. Methods in Enzymology, Vol. 147:Metabolism of Aromatic Amino Acids and Amines. Academic Press; Elsevier, Amsterdam.
Kim S-Y, Hwang KY, Kim S-H, Sung H-C, Han YS, Cho Y. 1999. Structural basis for cold adaptation: sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium arcticum. J. Biol. Chem. 274: 11761-11767.
Kim YO, Park IS, Nam BH, Kim DG, Jee YJ, Lee SJ, et al. 2014. A novel esterase from Paenibacillus sp. PBS-2 is a new member of the β-lactamase belonging to the family VIII lipases/esterases. J. Microbiol. Biotechnol. 24: 1260-1268.
Krell T, Maclean J, Boam DJ, Cooper A, Resmini M, Brocklehurst K, et al. 2001. Biochemical and X-ray crystallographic studies on shikimate kinase: the important structural role of the P-loop lysine. Protein Sci. 10: 1137-1149.
Kulakova L, Galkin A, Nakayama T, Nishino T, Esaki N. 2004. Cold-active esterase from Psychrobacter s p. A nt 300:gene cloning, characterization, and the effects of Gly → Pro substitution near the active site on its catalytic activity and stability. Biochim. Biophys. Acta 1696: 59-65.
Kumar M, Thakur V, Raghava GPS. 2008. COPid: composition based protein identification. In Silico Biol. 8: 121-128.
Lakowicz JR. 2006. Principles of Fluorescence Spectroscopy. Springer US, Boston, MA.
Lee Y S, B ok H J, L ee J H, C hoi YL. 2014. A c old-adapt ed carbohydrate esterase from the oil-degrading marine bacterium Microbulbifer thermotolerans DAU221: gene cloning, purification, and characterization. J. Microbiol. Biotechnol. 24: 925-935.
Leiros I, Moe E, Lanes O, Smalås AO, Willassen NP. 2003. The structure of uracil-DNA glycosylase from Atlantic cod (Gadus morhua) reveals cold-adaptation features. Acta Crystallogr. D Biol. Crystallogr. 59: 1357-1365.
Li S, Yang X, Zhang L, Yu W, Han F. 2015. Cloning, expression and characterization of a cold-adapted and surfactant-stable alginate lyase from marine bacterium Agarivorans sp. L11. J. Microbiol. Biotechnol. 25: 681-686.
Maiangwa J, Ali MSM, Salleh AB, Rahman RNZRA, Shariff FM, Leow TC. 2015. Adaptational properties and applications of cold-active lipases from psychrophilic bacteria. Extremophiles 19: 235-247.
Metpally RPR, Reddy BVB. 2009. Comparative proteome analysis of psychrophilic versus mesophilic bacterial species:insights into the molecular basis of cold adaptation of proteins. BMC Genomics 10: 11.
Moyer CL, Morita RY. 2007. Psychrophiles and psychrotrophs. eLS DOI: 10.1002/9780470015902.a0000402.pub2.
Pace CN, Treviño S, Prabhakaran E, Scholtz JM. 2004. Protein structure, stability and solubility in water and other solvents. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359: 12251234; discussion 1234-5.
Paredes DI, Watters K, Pitman DJ, Bystroff C, Dordick JS. 2011. Comparative void-volume analysis of psychrophilic and mesophilic enzymes: structural bioinformatics of psychrophilic enzymes reveals sources of core flexibility. BMC Struct. Biol. 11: 42.
Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42: W320-W324.
Romanowski MJ, Burley SK. 2002. Crystal structure of the Escherichia coli shikimate kinase I (AroK) that confers sensitivity to mecillinam. Proteins 47: 558-562.
Rosado LA, Vasconcelos IB, Palma MS, Frappier V, Najmanovich RJ, Santos DS, et al. 2013. The mode of action of recombinant Mycobacterium tuberculosis shikimate kinase:kinetics and thermodynamics analyses. PLoS One 8: e61918.
Siddiqui KS, Cavicchioli R. 2006. Cold-adapted enzymes. Annu. Rev. Biochem. 75: 403-433.
Siddiqui KS, Poljak A, Guilhaus M, De Francisci D, Curmi PMG, Feller G, et al. 2006. Role of lysine versus arginine in enzyme cold-adaptation: modifying lysine to homo-arginine stabilizes the cold-adapted α-amylase from Pseudoalteramonas haloplanktis. Proteins 64: 486-501.
Simithy J, Gill G, Wang Y, Goodwin DC, Calderón AI. 2015. Development of an ESI-LC-MS-based assay for kinetic evaluation of Mycobacterium tuberculosis shikimate kinase activity and inhibition. Anal. Chem. 87: 2129-2136.
Simithy J, Reeve N, Hobrath JV, Reynolds RC, Calderón AI. 2014. Identification of shikimate kinase inhibitors among anti-Mycobacterium tuberculosis compounds by LC-MS. Tuberculosis (Edinb.) 94: 152-158.
Simpson BK, Haard NF. 2011. Purification and characterization of trypsin from the Greenland cod (Gadus ogac). 1. Kinetic and thermodynamic characteristics. Can. J. Biochem. Cell Biol. 62: 894-900.
Singh P, Singh SM, Dhakephalkar P. 2014. Diversity, cold active enzymes and adaptation strategies of bacteria inhabiting glacier cryoconite holes of High Arctic. Extremophiles 18:229-242.
Smalås AO, Leiros HK, Os V, Willassen NP. 2000. Cold adapted enzymes. Biotechnol. Annu. Rev. 6: 1-57.
Struvay C, Feller G. 2012. Optimization to low temperature activity in psychrophilic enzymes. Int. J. Mol. Sci. 13: 1164311665.
Su H, Mai Z, Yang J, Xiao Y, Tian X, Zhang S. 2016. Cloning, expression and characterization of a cold-active and organic solvent-tolerant lipase from Aeromicrobium sp. SCSIO 25071. J. Microbiol. Biotechnol. 26: 1067-1076.
Sutton KA, Breen J, MacDonald U, Beanan JM, Olson R, Russo TA, et al. 2015. Structure of shikimate kinase, an in vivo essential metabolic enzyme in the nosocomial pathogen Acinetobacter baumannii, in complex with shikimate. Acta Crystallogr. D Biol. Crystallogr. 71: 1736-1744.
Szilágyi A, Závodszky P. 2000. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8: 493-504.
Tang MAK, Motoshima H, Watanabe K. 2014. Cold adaptation:structural and functional characterizations of psychrophilic and mesophilic acetate kinase. Protein J. 33: 313-322.
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Zanphorlin LM, de Giuseppe PO, Honorato RV, Tonoli CCC, Fattori J, Crespim E, et al. 2016. Oligomerization as a strategy for cold adaptation: structure and dynamics of the GH1 β-glucosidase from Exiguobacterium antarcticum B7. Sci. Rep. 6: 23776.

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J. Microbiol. Biotechnol. 2016; 26(12): 2087-2097

Published online December 28, 2016 https://doi.org/10.4014/jmb.1608.08049

Cloning, Expression, and Characterization of a Cold-Adapted Shikimate Kinase from the Psychrophilic Bacterium Colwellia psychrerythraea 34H

Wahyu Sri Kunto Nugroho ¹, Dong-Woo Kim ¹, Jong-Cheol Han ², Young Baek Hur ², Soo-Wan Nam ³ and Hak Jun Kim ^1*

¹Department of Chemistry, Pukyong National University, Busan 48547, Republic of Korea, ²Southeast Sea Fisheries Research Institute, National Fisheries Research and Development Institute, Tongyeong 53085, Republic of Korea, ³Department of Biotechnology and Bioengineering, Dong-Eui University, Busan 47340, Republic of Korea

Received: August 24, 2016; Accepted: September 5, 2016

Abstract

Most cold-adapted enzymes possess higher Km and kcat values than those of their mesophilic
counterparts to maximize the reaction rate. This characteristic is often ascribed to a high
structural flexibility and improved dynamics in the active site. However, this may be less
convincing to cold-adapted metabolic enzymes, which work at substrate concentrations near
Km. In this respect, cold adaptation of a shikimate kinase (SK) in the shikimate pathway from
psychrophilic Colwellia psychrerythraea (CpSK) was characterized by comparing it with a
mesophilic Escherichia coli homolog (EcSK). The optimum temperatures for CpSK and EcSK
activity were approximately 30°C and 40°C, respectively. The melting points were 33°C and
45°C for CpSK and EcSK, respectively. The ΔGH2O (denaturation in the absence of denaturing
agent) values were 3.94 and 5.74 kcal/mol for CpSK and EcSK, respectively. These results
indicated that CpSK was a cold-adapted enzyme. However, contrary to typical kinetic data,
CpSK had a lower Km for its substrate shikimate than most mesophilic SKs, and the kcat was not
increased. This observation suggested that CpSK may have evolved to exhibit increased
substrate affinity at low intracellular concentrations of shikimate in the cold environment.
Sequence analysis and homology modeling also showed that some important salt bridges were
lost in CpSK, and higher Arg residues around critical Arg 140 seemed to increase flexibility for
catalysis. Taken together, these data demonstrate that CpSK exhibits characteristics of cold
adaptation with unusual kinetic parameters, which may provide important insights into the
cold adaptation of metabolic enzymes.

Keywords: cold adaptation, shikimate kinase, psychrophile, The Michaelis-Menten constant, turnover number

Abstract

References

Ásgeirsson B, Cekan P. 2006. Microscopic rate-constants for substrate binding and acylation in cold-adaptation of trypsin I from Atlantic cod. FEBS Lett. 580: 4639-4644.
Bentahir M. 2000. Structural, kinetic, and calorimetric characterization of the cold-active phosphoglycerate kinase from the antarctic Pseudomonas sp. TACII18. J. Biol. Chem. 275: 11147-11153.
Cerasoli E, Kelly SM, Coggins JR, Boam DJ, Clarke DT, Price NC. 2002. The refolding of type II shikimate kinase from Erwinia chrysanthemi a ft er d enat urat ion in u rea. Eur. J. Biochem. 269: 2124-2132.
Cheng W-C, Chang Y-N, Wang W-C. 2005. Structural basis for shikimate-binding specificity of Helicobacter pylori shikimate kinase. J. Bacteriol. 187: 8156-8163.
Cheng W-C, Chen Y-F, Wang H-J, Hsu K-C, Lin S-C, Chen T-J, et al. 2012. Structures of Helicobacter pylori shikimate kinase reveal a selective inhibitor-induced-fit mechanism. PLoS One 7: e33481.
Collins T, Meuwis M-A, Stals I, Claeyssens M, Feller G, Gerday C. 2002. A novel family 8 xylanase, functional and physicochemical characterization. J. Biol. Chem. 277: 3513335139.
Coracini JD, de Azevedo WF. 2014. Shikimate kinase, a protein target for drug design. Curr. Med. Chem. 21: 592-604.
D’Amico S, Claverie P, Collins T, Georlette D, Gratia E, Hoyoux A, et al. 2002. Molecular basis of cold adaptation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 917-925.
D’Amico S, Collins T, Marx J-C, Feller G, Gerday C. 2006. Psychrophilic microorganisms: challenges for life. EMBO Rep. 7: 385-389.
DeFeyt er RC, P it t ard J. 1 986. P urification a nd p ropert ies of shikimate kinase II from Escherichia coli K-12. J. Bacteriol. 165: 331-333.
DeLano WL. 2002. The PyMOL Molecular Graphics System. Accessible at http://www.pymol.org.
De Santi C, Tedesco P, Ambrosino L, Altermark B, Willassen N-P, de Pascale D. 2014. A new alkaliphilic cold-active esterase from the psychrophilic marine bacterium Rhodococcus sp.: functional and structural studies and biotechnological potential. Appl. Biochem. Biotechnol. 172: 3054-3068.
Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang J-M, et al. 2011. T-Coffee: a Web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39: W13-W17.
Feller G, Gerday C. 1997. Psychrophilic enzymes: molecular basis of cold adaptation. Cell. Mol. Life Sci. 53: 830-841.
Feller G, Narinx E, Arpigny JL, Ait taleb M, Baise E, Genicot S, et al. 1996. Enzymes from psychrophilic organisms. FEMS Microbiol. Rev. 18: 189-202.
Feller G, Zekhnini Z, Lamotte-Brasseur J, Gerday C. 1997. Enzymes from cold-adapted microorganisms - t he c lass C beta-lactamase from the antarctic psychrophile Psychrobacter Immobilis A5. Eur. J. Biochem. 244: 186-191.
Fucile G, Garcia C, Carlsson J, Sunnerhagen M, Christendat D. 2011. Structural and biochemical investigation of two Arabidopsis s hikimat e kinases: t he h eat -inducible i soform i s thermostable. Protein Sci. 20: 1125-1136.
Gan J , Gu Y , Li Y , Yan H, J i X. 2 006. C ryst al s t ructure of Mycobacterium tuberculosis shikimate kinase in complex with shikimic acid and an ATP analogue. Biochemistry 45: 85398545.
Genicot S, Feller G, Gerday C. 1988. Trypsin from antarctic fish (Paranotothenia magellanica forster) as compared with trout (Salmo gairdneri) trypsin. Comp. Biochem. Physiol. B 90:601-609.
Georlette D, Bentahir M, Claverie P, Collins T, D’Amico S, Delille D, et al. 2002. Physics and Chemistry Basis of Biotechnology. Springer Netherlands, Dordrecht.
Greenfield NJ. 2006. Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat. Protoc. 1: 2527-2535.
Han C, Zhang J, Chen L, Chen K, Shen X, Jiang H. 2007. Discovery of Helicobacter pylori shikimate kinase inhibitors:bioassay and molecular modeling. Bioorg. Med. Chem. 15:656-662.
Herrmann KM, Weaver LM. 1999. The shikimate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 473-503.
Hoyoux A, Jennes I, Dubois P, Genicot S, Dubail F, François JM, et al. 2001. Cold-adapted beta-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis. Appl. Environ. Microbiol. 67: 1529-1535.
Jahandideh M, Barkooie SMH, Jahandideh S, Abdolmaleki P, Movahedi MM, Hoseini S, et al. 2008. Elucidating the protein cold-adaptation: investigation of the parameters enhancing protein psychrophilicity. J. Theor. Biol. 255: 113-118.
Kaufmman S (ed.). 1987. Methods in Enzymology, Vol. 147:Metabolism of Aromatic Amino Acids and Amines. Academic Press; Elsevier, Amsterdam.
Kim S-Y, Hwang KY, Kim S-H, Sung H-C, Han YS, Cho Y. 1999. Structural basis for cold adaptation: sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium arcticum. J. Biol. Chem. 274: 11761-11767.
Kim YO, Park IS, Nam BH, Kim DG, Jee YJ, Lee SJ, et al. 2014. A novel esterase from Paenibacillus sp. PBS-2 is a new member of the β-lactamase belonging to the family VIII lipases/esterases. J. Microbiol. Biotechnol. 24: 1260-1268.
Krell T, Maclean J, Boam DJ, Cooper A, Resmini M, Brocklehurst K, et al. 2001. Biochemical and X-ray crystallographic studies on shikimate kinase: the important structural role of the P-loop lysine. Protein Sci. 10: 1137-1149.
Kulakova L, Galkin A, Nakayama T, Nishino T, Esaki N. 2004. Cold-active esterase from Psychrobacter s p. A nt 300:gene cloning, characterization, and the effects of Gly → Pro substitution near the active site on its catalytic activity and stability. Biochim. Biophys. Acta 1696: 59-65.
Kumar M, Thakur V, Raghava GPS. 2008. COPid: composition based protein identification. In Silico Biol. 8: 121-128.
Lakowicz JR. 2006. Principles of Fluorescence Spectroscopy. Springer US, Boston, MA.
Lee Y S, B ok H J, L ee J H, C hoi YL. 2014. A c old-adapt ed carbohydrate esterase from the oil-degrading marine bacterium Microbulbifer thermotolerans DAU221: gene cloning, purification, and characterization. J. Microbiol. Biotechnol. 24: 925-935.
Leiros I, Moe E, Lanes O, Smalås AO, Willassen NP. 2003. The structure of uracil-DNA glycosylase from Atlantic cod (Gadus morhua) reveals cold-adaptation features. Acta Crystallogr. D Biol. Crystallogr. 59: 1357-1365.
Li S, Yang X, Zhang L, Yu W, Han F. 2015. Cloning, expression and characterization of a cold-adapted and surfactant-stable alginate lyase from marine bacterium Agarivorans sp. L11. J. Microbiol. Biotechnol. 25: 681-686.
Maiangwa J, Ali MSM, Salleh AB, Rahman RNZRA, Shariff FM, Leow TC. 2015. Adaptational properties and applications of cold-active lipases from psychrophilic bacteria. Extremophiles 19: 235-247.
Metpally RPR, Reddy BVB. 2009. Comparative proteome analysis of psychrophilic versus mesophilic bacterial species:insights into the molecular basis of cold adaptation of proteins. BMC Genomics 10: 11.
Moyer CL, Morita RY. 2007. Psychrophiles and psychrotrophs. eLS DOI: 10.1002/9780470015902.a0000402.pub2.
Pace CN, Treviño S, Prabhakaran E, Scholtz JM. 2004. Protein structure, stability and solubility in water and other solvents. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359: 12251234; discussion 1234-5.
Paredes DI, Watters K, Pitman DJ, Bystroff C, Dordick JS. 2011. Comparative void-volume analysis of psychrophilic and mesophilic enzymes: structural bioinformatics of psychrophilic enzymes reveals sources of core flexibility. BMC Struct. Biol. 11: 42.
Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42: W320-W324.
Romanowski MJ, Burley SK. 2002. Crystal structure of the Escherichia coli shikimate kinase I (AroK) that confers sensitivity to mecillinam. Proteins 47: 558-562.
Rosado LA, Vasconcelos IB, Palma MS, Frappier V, Najmanovich RJ, Santos DS, et al. 2013. The mode of action of recombinant Mycobacterium tuberculosis shikimate kinase:kinetics and thermodynamics analyses. PLoS One 8: e61918.
Siddiqui KS, Cavicchioli R. 2006. Cold-adapted enzymes. Annu. Rev. Biochem. 75: 403-433.
Siddiqui KS, Poljak A, Guilhaus M, De Francisci D, Curmi PMG, Feller G, et al. 2006. Role of lysine versus arginine in enzyme cold-adaptation: modifying lysine to homo-arginine stabilizes the cold-adapted α-amylase from Pseudoalteramonas haloplanktis. Proteins 64: 486-501.
Simithy J, Gill G, Wang Y, Goodwin DC, Calderón AI. 2015. Development of an ESI-LC-MS-based assay for kinetic evaluation of Mycobacterium tuberculosis shikimate kinase activity and inhibition. Anal. Chem. 87: 2129-2136.
Simithy J, Reeve N, Hobrath JV, Reynolds RC, Calderón AI. 2014. Identification of shikimate kinase inhibitors among anti-Mycobacterium tuberculosis compounds by LC-MS. Tuberculosis (Edinb.) 94: 152-158.
Simpson BK, Haard NF. 2011. Purification and characterization of trypsin from the Greenland cod (Gadus ogac). 1. Kinetic and thermodynamic characteristics. Can. J. Biochem. Cell Biol. 62: 894-900.
Singh P, Singh SM, Dhakephalkar P. 2014. Diversity, cold active enzymes and adaptation strategies of bacteria inhabiting glacier cryoconite holes of High Arctic. Extremophiles 18:229-242.
Smalås AO, Leiros HK, Os V, Willassen NP. 2000. Cold adapted enzymes. Biotechnol. Annu. Rev. 6: 1-57.
Struvay C, Feller G. 2012. Optimization to low temperature activity in psychrophilic enzymes. Int. J. Mol. Sci. 13: 1164311665.
Su H, Mai Z, Yang J, Xiao Y, Tian X, Zhang S. 2016. Cloning, expression and characterization of a cold-active and organic solvent-tolerant lipase from Aeromicrobium sp. SCSIO 25071. J. Microbiol. Biotechnol. 26: 1067-1076.
Sutton KA, Breen J, MacDonald U, Beanan JM, Olson R, Russo TA, et al. 2015. Structure of shikimate kinase, an in vivo essential metabolic enzyme in the nosocomial pathogen Acinetobacter baumannii, in complex with shikimate. Acta Crystallogr. D Biol. Crystallogr. 71: 1736-1744.
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