Biochemical characterization of a catalase from Vibrio vulnificus, a pathogen that causes gastroenteritis

• Authors: Jihua Pei , Haijun Wang , Limin Wu , Shenglong Xia , Changlong Xu , Bo Zheng , Tianya Li , Yi Jiang
• Languages of publication: EN

Abstracts

EN

Vibrio vulnificus is a virulent human pathogen causing gastroenteritis and possibly life threatening septicemia in patients. Most V. vulnificus are catalase positive and can deactivate peroxides, thus allowing them to survive within the host. In the study presented here, a catalase from V. vulnificus (CAT-Vv) was purified to homogeneity after expression in Escherichia coli. The kinetics and function of CAT-Vv were examined. CAT-Vv catalyzed the reduction of H2O2 at an optimal pH of 7.5 and temperature of 35°C. The Vmax and Km values were 65.8±1.2 U/mg and 10.5±0.7 mM for H2O2, respectively. Mutational analysis suggests that amino acids involved in heme binding play a key role in the catalysis. Quantitative reverse transcription-PCR revealed that in V. vulnificus, transcription of CAT-Vv was upregulated by low salinity, heat, and oxidative stresses. This research gives new clues to help inhibit the growth of, and infection by V. vulnificus.

Keywords

EN

catalase; Vibrio vulnificus; kinetics; mutation; gastroenteritis.

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2017
• Volume: 64
• Issue: 3
• Pages: 543-549

Dates

published

2017

received

2017-02-22

revised

2017-04-24

accepted

2017-04-24

(unknown)

2017-09-12

Contributors

author

Jihua Pei

• Department of Gastroenterology, The second Affiliated Hospital of Wenzhou Medical University, Wenzhou 325027, Zhejiang, China

author

Haijun Wang

• College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, Liaoning, China

author

Limin Wu

• Department of Gastroenterology, The second Affiliated Hospital of Wenzhou Medical University, Wenzhou 325027, Zhejiang, China

author

Shenglong Xia

• Department of Gastroenterology, The second Affiliated Hospital of Wenzhou Medical University, Wenzhou 325027, Zhejiang, China

author

Changlong Xu

• Department of Gastroenterology, The second Affiliated Hospital of Wenzhou Medical University, Wenzhou 325027, Zhejiang, China

author

Bo Zheng

• Department of Gastroenterology, The second Affiliated Hospital of Wenzhou Medical University, Wenzhou 325027, Zhejiang, China

author

Tianya Li

• College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, Liaoning, China

author

Yi Jiang

• Department of Gastroenterology, The second Affiliated Hospital of Wenzhou Medical University, Wenzhou 325027, Zhejiang, China

References

• Anjum NA, Sharma P, Gill SS, Hasanuzzaman M, Khan EA, Kachhap K, Mohamed AA, Thangavel P, Devi GD, Vasudhevan P, Sofo A, Khan NA, Misra AN, Lukatkin AS, Singh HP, Pereira E, Tuteja N (2016) Catalase and ascorbate peroxidase-representative H2O2-detoxifying heme enzymes in plants. Environ Sci Pollut Res Int 23: 19002--19029. doi: 10.1007/s11356-016-7309-6.
• Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
• Carpena X, Soriano M, Klotz MG, Duckworth HW, Donald LJ, Melik-Adamyan W, Fita I, Loewen PC (2003) Structure of the Clade 1 catalase, CatF of Pseudomonas syringae, at 1.8 Å resolution. Proteins 50: 423-436. doi: 10.1002/prot.10284.
• Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61: 192-208. doi: 10.1007/s00018-003-3206-5.
• Chung HY, Kim YT, Kim S, Na EJ, Ku HJ, Lee KH, Heo ST, Ryu S, Kim H, Choi SH, Lee JH (2016) Complete genome sequence of Vibrio vulnificus FORC_017 isolated from a patient with a hemorrhagic rash after consuming raw dotted gizzard shad. Gut Pathog 8: 22. doi: 10.1186/s13099-016-0104-6.
• Deisseroth A, Dounce AL (1970) Catalase: Physical and chemical properties, mechanism of catalysis, and physiological role. Physiol Rev 50: 319-375.
• Efimov V, Danin-Poleg Y, Green SJ, Elgavish S, Kashi Y (2015) Draft genome sequence of the pathogenic bacterium Vibrio vulnificus V252 biotype 1, isolated in Israel. Genome Announc 3: e01182-15. doi: 10.1128/genomeA.01182-15.
• Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146: 359-388. doi: 10.1046/j.1469-8137.2000.00667.x
• Gasteiger E, Hoogland C, Gattiker A, Duvaud Se, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook, Walker JM ed, pp 571-607. Humana Press. New York.
• Hara I, Ichise N, Kojima K, Kondo H, Ohgiya S, Matsuyama H, Yumoto I (2007) Relationship between the size of the bottleneck 15 Å from iron in the main channel and the reactivity of catalase corresponding to the molecular size of substrates. Biochemistry 46: 11-22. doi: 10.1021/bi061519w.
• Jones MK, Oliver JD (2009) Vibrio vulnificus: Disease and Pathogenesis. Infect Immun 77: 1723-1733. doi: 10.1128/IAI.01046-08.
• Kitamura C, Yamauchi Y, Yamaguchi T, Aida Y, Ito K, Ishizawa Y, Saitoh K, Kasai T, Ohnishi M (2016) Successful treatment of a case of necrotizing fasciitis due to Vibrio vulnificus in a cold climate in Japan. Intern Med 55: 1007-1010. doi: 10.2169/internalmedicine.55.5231.
• Klotz MG, Klassen GR, Loewen PC (1997) Phylogenetic relationships among prokaryotic and eukaryotic catalases. Mol Biol Evol 14: 951-958.
• Lee BC, Choi SH, Kim TS (2008) Vibrio vulnificus RTX toxin plays an important role in the apoptotic death of human intestinal epithelial cells exposed to Vibrio vulnificus. Microbes Infect 10: 1504-1513. doi: 10.1016/j.micinf.2008.09.006.
• Lee BC, Kim MS, Choi SH, Kim KY, Kim TS (2009) In vitro and in vivo antimicrobial activity of water-soluble chitosan oligosaccharides against Vibrio vulnificus. Int J Mol Med 24: 327-333. doi: 10.3892/ijmm_00000236.
• Loewen PC, Villanueva J, Switala J, Donald LJ, Ivancich A (2015) Unprecedented access of phenolic substrates to the heme active site of a catalase: substrate binding and peroxidase-like reactivity of Bacillus pumilus catalase monitored by X-ray crystallography and EPR spectroscopy. Proteins 83: 853-866. doi: 10.1002/prot.24777.
• Lushchak VI (2014) Free radicals, reactive oxygen species, oxidative stresses and its classifications. Chem Biol Interact 224: 164-175. doi: 10.1016/j.cbi.2014.10.016.
• Mahmoud BS (2009) Reduction of Vibrio vulnificus in pure culture, half shell and whole shell oysters (Crassostrea virginica) by X-ray. Int J Food Microbiol 130: 135-139. doi: 10.1016/j.ijfoodmicro.2009.01.023.
• Melody K, Senevirathne R, Janes M, Jaykus LA, Supan J (2008) Effectiveness of icing as a postharvest treatment for control of Vibrio vulnificus and Vibrio parahaemolyticus in the eastern oyster (Crassostrea virginica). J Food Prot 71: 1475-1480.
• Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI's conserved domain database. Nucleic Acids Res 43: D222-D226. doi: 10.1093/nar/gku1221.
• Melody K, Senevirathne R, Janes M, Jaykus LA, Supan J (2008) Effectiveness of icing as a postharvest treatment for control of Vibrio vulnificus and Vibrio parahaemolyticus in the eastern oyster (Crassostrea virginica). J Food Prot 71: 1475-1480.
• Motes ML, DePaola A, Cook DW, Veazey JE, Hunsucker JC, Garthright WE, Blodgett RJ, Chirtel SJ (1998) Influence of water temperature and salinity on Vibrio vulnificus in northern gulf and atlantic coast oysters (Crassostrea virginica). Appl Environ Microbiol 64: 1459-1465.
• Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol 141: 346-350. doi: 10.1104/pp.106.078162.
• Nakamura K, Kanno T, Mokudai T, Iwasawa A, Niwano Y, Kohno M (2012) Microbial resistance in relation to catalase activity to oxidative stress induced by photolysis of hydrogen peroxide. Microbiol Immunol 56: 48-55. doi: 10.1111/j.1348-0421.2011.00400.x.
• Nicholls P, Fita I, Loewen PC (2000) Enzymology and structure of catalases. Adv Inorg Chem 51: 51-106. doi: 10.1016/S0898-8838(00)51001-0
• Oliver JD (2015) The biology of Vibrio vulnificus. Microbiol Spectr 3: doi: 10.1128/microbiolspec.VE-0001-2014.
• Pajuelo D, Hernandez-Cabanyero C, Sanjuan E, Lee CT, Silva-Hernandez FX, Hor LI, MacKenzie S, Amaro C (2016) Iron and Fur in the life cycle of the zoonotic pathogen Vibrio vulnificus. Environ Microbiol 18: 4005-4022. doi: 10.1111/1462-2920.13424.
• Pezzoni M, Pizarro RA, Costa CS (2014) Protective role of extracellular catalase (KatA) against UVA radiation in Pseudomonas aeruginosa biofilms. J Photochem Photobiol B 131: 53-64. doi: 10.1016/j.jphotobiol.2014.01.005.
• Rahi A, Rehan M, Garg R, Tripathi D, Lynn AM, Bhatnagar R (2011) Enzymatic characterization of Catalase from Bacillus anthracis and prediction of critical residues using information theoretic measure of Relative Entropy. Biochem Biophys Res Commun 411: 88-95. doi: 10.1016/j.bbrc.2011.06.099.
• Ramos RJ, Miotto M, Squella FJ, Cirolini A, Ferreira JF, Vieira CR (2012) Depuration of oysters (Crassostrea gigas) contaminated with Vibrio parahaemolyticus and Vibrio vulnificus with UV light and chlorinated seawater. J Food Prot 75: 1501-1506. doi: 10.4315/0362-028X.JFP-11-467.
• Randa MA, Polz MF, Lim E (2004) Effects of temperature and salinity on Vibrio vulnificus population dynamics as assessed by quantitative PCR. Appl Environ Microbiol 70: 5469-5476. doi: 10.1128/AEM.70.9.5469-5476.2004.
• Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539. doi: 10.1038/msb.2011.75.
• Smith B, Oliver JD (2006) In situ and in vitro gene expression by Vibrio vulnificus during entry into, persistence within, and resuscitation from the viable but nonculturable state. Appl Environ Microbiol 72: 1445-1451. doi: 10.1128/AEM.72.2.1445-1451.2006.
• Sooch BS, Kauldhar BS, Puri M (2014) Recent insights into microbial catalases: isolation, production and purification. Biotechnol Adv 32: 1429-1447. doi: 10.1016/j.biotechadv.2014.09.003.
• Strom MS, Paranjpye RN (2000) Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect 2: 177-188.
• Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol 30: 2725-2729. doi: 10.1093/molbev/mst197.
• Tan HJ, Liu SH, Oliver JD, Wong HC (2010a) Role of RpoS in the susceptibility of low salinity-adapted Vibrio vulnificus to environmental stresses. Int J Food Microbiol 137: 137-142. doi: 10.1016/j.ijfoodmicro.2009.12.006.
• Tanabe S, Nishizawa Y, Minami E (2009) Effects of catalase on the accumulation of H2O2 in rice cells inoculated with rice blast fungus, Magnaporthe oryzae. Physiol Plant 137: 148-154. doi: 10.1111/j.1399-3054.2009.01272.x.
• Wong HC, Liu SH (2008) Characterization of the low-salinity stress in Vibrio vulnificus. J Food Prot 71: 416-419. doi: 10.4315/0362-028X.JFP-11-321.
• Ye M, Huang Y, Gurtler JB, Niemira BA, Sites JE, Chen H (2013) Effects of pre- or post-processing storage conditions on high-hydrostatic pressure inactivation of Vibrio parahaemolyticus and V. vulnificus in oysters. Int J Food Microbiol 163: 146-152. doi: 10.1016/j.ijfoodmicro.2013.02.019.

Identifiers

DOI

10.18388/abp.2017_1530