All Title Author
Keywords Abstract


Enzymatic Hydrolysis of an Organic Sulfur Compound

DOI: 10.4236/aer.2019.71001, PP. 1-13

Keywords: Enzymes, Sulfatases, Organic Sulfur Mineralization

Full-Text   Cite this paper   Add to My Lib

Abstract:

Sulfatases which cleave sulfate esters in biological systems are key enzymes that deserve special attention due to their significant roles in organic sulfur (OS) mineralization and inorganic sulfur (\"\") release. In this study, in-vitro experiments were conducted to evaluate S bonded substrate hydrolysis by a commercially available arylsulfatase (EC 3.1.6.1) from Aerobacter aerogenes. The enzyme-substrate interactions were assessed to determine: 1) rate of hydrolysis, 2) catalytic efficiency, 3) thermal stability, and 4) optimal pH of this enzyme. Arylsulfatase exhibited substrate hydrolysis with a high affinity for p-nitrophenyl sulfate (potassium 4-nitrophenyl sulfate (pNPS)). The optimum activity for the enzyme was observed to occur at a pH of 7.1. The optimal temperature was 37°C but ranged from 35°C - 45°C. The apparent Km and Kcat of the enzyme for pNPS hydrolysis at the optimal pH, and temperature were determined to be 1.03 mM and 75.73 μM/min, respectively. This work defines the catalytic and kinetic properties of arylsulfatase (EC 3.1.6.1) and confirms the optimal conditions for sulfatase activity testing. The resulting information is useful in elucidating the contributions that individual enzymes have for specific reactions rather than relying on traditional total enzyme activity measurements.

References

[1]  Barbeyron, T., Brillet-Guéguen, L., Carré, W., Carrière, C., Caron, C., Czjzek, M., Hoebeke, M. and Michel, G. (2016) Matching the Diversity of Sulfated Biomolecules: Creation of a Classification Database for Sulfatases Reflecting Their Substrate Specificity. PLoS ONE, 11, e0164846.
[2]  De Hostos, E.L., Schilling, J. and Grossman, A.R. (1989) Structure and Expression of the Gene Encoding the Periplasmic Arylsulfatase of Chlamydomonas reinhardtii. Molecular and General Genetics MGG, 218, 229-239.
https://doi.org/10.1007/BF00331273
[3]  Dodgson, K.S., White, G.F. and Fitzgerald, J.W. (2018) Sulfatases of Microbial Origin. CRC Press, Boca Raton.
[4]  Tabatabai, M.A. and Bremner, J.M. (1970) Arylsulfatase Activity of Soils. Soil Science Society of America Journal, 34, 225-229.
https://doi.org/10.2136/sssaj1970.03615995003400020016x
[5]  Tabatabai, M.A. and Bremner, J.M. (1970) Factors Affecting Soil Arylsulfatase Activity. Soil Science Society of America Journal, 34, 427-429.
https://doi.org/10.2136/sssaj1970.03615995003400030023x
[6]  Riffaldi, R., Saviozzi, A., Cardelli, R., Cipolli, S. and Levi-Minzi, R. (2006) Sulphur Mineralization Kinetics as Influenced by Soil Properties. Biology and Fertility of Soils, 43, 209-214.
https://doi.org/10.1007/s00374-006-0095-4
[7]  Crozier, C., Hoyt, G. and Hardy, D. (2014) Soil Facts: Sulfur Fertilization of North Carolina Crops. NC State Extension Publications, Raleigh.
https://content.ces.ncsu.edu/sulfur-fertilization-of-north-carolina-crops
[8]  Raper, T.B., Mcclure, A.T., Yin, F. and Brown, B. Sulfur and Tennessee Row Crops Sulfur and Tennessee Row Crops 2.
https://extension.tennessee.edu/publications/Documents/W435.pdf
[9]  Scherer, H.W. (2009) Sulfur in Soils. Journal of Plant Nutrition and Soil Science, 172, 326-335.
https://doi.org/10.1002/jpln.200900037
[10]  Siwik-Ziomek, A., Lemanowicz, J. and Koper, J. (2016) Arylsulphatase Activity and Sulphate Content in Relation to Crop Rotation and Fertilization of Soil. International Agrophysics, 30, 359-367.
https://doi.org/10.1515/intag-2015-0098
[11]  Bohn, H.L. and McNeal, B.L. (2001) Soil Chemistry. 3rd Edition, John Wiley & Sons, Inc., New York.
[12]  Freney, J.R. (1986) Forms and Reactions of Organic Sulfur Compounds in Soils. In: Sulfur in Agriculture, American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, WI, 207-232.
[13]  Castellano, R.P. and Dick, S.D. (1991) Cropping and Sulfur Fertilization Influence on Sulfur Transformations in Soil. Soil Science Society of America Journal, 54, 114-121.
https://doi.org/10.2136/sssaj1991.03615995005500010020x
[14]  Cregut, M., Piutti, S., Slezack-Deschaumes, S. and Benizri, E. (2013) Compartmentalization and Regulation of Arylsulfatase Activities in Streptomyces sp., Microbacterium sp. and Rhodococcus sp. Soil Isolates in Response to Inorganic Sulfate Limitation. Microbiological Research, 168, 12-21.
https://doi.org/10.1016/j.micres.2012.08.001
[15]  Farrell, R.E., Gupta, V.V.S.R. and Germida, J.J. (1994) Effects of Cultivation on the Activity and Kinetics of Arylsulfatase in Saskatchewan Soils. Soil Biology and Biochemistry, 26, 1033-1040.
https://doi.org/10.1016/0038-0717(94)90118-X
[16]  Gardner, T., Acosta-Martinez, V., Senwo, Z. and Dowd, S.E. (2011) Soil Rhizosphere Microbial Communities and Enzyme Activities under Organic Farming in Alabama. Diversity, 3, 308-328.
https://doi.org/10.3390/d3030308
[17]  Gupta, V.V.S.R. and Germida, J.J. (1988) Distribution of Microbial Biomass and Its Activity in Different Soil Aggregate Size Classes as Affected by Cultivation. Soil Biology and Biochemistry, 20, 777-786.
https://doi.org/10.1016/0038-0717(88)90082-X
[18]  Deng, S.P. and Tabatabai, M.A. (1996) Effect of Tillage and Residue Management on Enzyme Activities in Soils. Biology and Fertility of Soils, 22, 208-213.
https://doi.org/10.1007/BF00382514
[19]  Kertesz, M.A. (2000) Riding the Sulfur Cycle—Metabolism of Sulfonates and Sulfate Esters in Gram-Negative Bacteria. FEMS Microbiology Reviews, 24, 135-175.
[20]  Klose, S., Bilen, S., Tabatabai, M.A. and Dick, W.A. (2011) Sulfur Cycle Enzymes. In: Dick, R.P., Ed., Methods of Soil Enzymology, Soil Science Society of America, Wisconsin.
[21]  Beil, S., Kehrli, H., James, P., Staudenmann, W., Cook, A.M., Leisinger, T. and Kertesz, M.A. (1995) Purification and Characterization of the Arylsulfatase Synthesized by Pseudomonas aeruginosa PAO during Growth in Sulfate-Free Medium and Cloning of the Arylsulfatase Gene (atsA). European Journal of Biochemistry, 229, 385-394.
https://doi.org/10.1111/j.1432-1033.1995.0385k.x
[22]  Boltes, I., Czapinska, H., Kahnert, A., Von Bülow, R., Dierks, T., Schmidt, B., Von Figura, K., Kertesz, M.A. and Usón, I. (2001) 1.3 Å Structure of Arylsulfatase from Pseudomonas aeruginosa Establishes the Catalytic Mechanism of Sulfate Ester Cleavage in the Sulfatase Family. Structure, 9, 483-491.
https://doi.org/10.1016/S0969-2126(01)00609-8
[23]  Fowler, L.R. and Rammler, D.H. (1964) Sulfur Metabolism of Aerobactor aerogenes II. The Purification and Some Properties of a Sulfatase. Biochemistry, 3, 230-237.
https://doi.org/10.1021/bi00890a015
[24]  Henderson, M. and Milazzo, F.H. (1979) Arylsulfatase in Salmonella Typhimurium: Detection and Influence of Carbon Source and Tyramiine on Its Sysnthesis. Journal of Bacteriology, 139, 80-87.
[25]  Miech, C., Dierks, T., Selmer, T., Von Figura, K. and Schmidt, B. (1998) Arylsulfatase from Klebsiella Pneumoniae Carries a Formylglycine Generated from a Serine. Journal of Biological Chemistry, 273, 4835-4837.
[26]  Murooka, Y., Yim, M.H. and Harada, T. (1980) Formation and Purification of Serratia Marcescens Arylsulfatase. Applied and Environmental Microbiology, 39, 812-817.
http://www.ncbi.nlm.nih.gov/pubmed/16345546
[27]  Hummerjohann, J., Küttel, E., Quadroni, M., Ragaller, J., Leisinger, T. and Kertesz, M.A. (1998) Regulation of the Sulfate Starvation Response in Pseudomonas aeruginosa: Role of Cysteine Biosynthetic Intermediates. Microbiology, 144, 1375-1386.
https://doi.org/10.1099/00221287-144-5-1375
[28]  Quadroni, M., James, P., Dainese-Hatt, P. and Kertesz, M.A. (1999) Proteome Mapping, Mass Spectrometric Sequencing and Reverse Transcription-PCR for Characterization of the Sulfate Starvation-Induced Response in Pseudomonas aeruginosa PAO1. European Journal of Biochemistry, 266, 986-996.
https://doi.org/10.1046/j.1432-1327.1999.00941.x
[29]  Fromageot, C. (1950) Sulfatase. In: Summer, J.B. and Myrback, K., Eds., The Enzymes, Vol. 1, Academic Press, New York, 517-526.
[30]  Roy, A.B. (1971) The Hydrolysis of Sulfate Esters. The Enzymes, 5, 1-19.
https://doi.org/10.1016/S1874-6047(08)60084-0
[31]  Lad, C., Williams, N.H. and Wolfenden, R. (2003) The Rate of Hydrolysis of Phosphomonoester Dianions and the Exceptional Catalytic Proficiencies of Protein and Inositol Phosphatases. Proceedings of the National Academy of Sciences of the United States of America, 100, 5607-5610.
https://doi.org/10.1073/pnas.0631607100
[32]  Gao, J., Ma, S., Major, D.T., Nam, K., Pu, J. and Truhlar, D.G. (2006) Mechanisms and Free Energies of Enzymatic Reactions. Chemical Reviews, 106, 3188-3209.
[33]  Chae, M.Y., Postula, J.F. and Raushel, F.M. (1994) Stereospcific Enzymatic Hydrolysis of Phosphorus-Sulfur Bonds in Chiral Organophosphate Triesters. Bioorganic and Medicinal Chemistry Letters, 4, 1473-1478.
https://doi.org/10.1016/S0960-894X(01)80516-3
[34]  Okamura, H., Yamada, T., Murooka, Y. and Harada, T. (1976) Purification and Properties of Arylsulfatase of Klebsiella Aerogenes Identity of the Enzymes Formed by Non-Repressed and De-Repressed Synthesis. Agricultural and Biological Chemistry, 40, 2071-2076.
https://doi.org/10.1271/bbb1961.40.2071
[35]  Acosta-Martínez, V., Zobeck, T.M. and Allen, V. (2004) Soil Microbial, Chemical and Physical Properties in Continuous Cotton and Integrated Crop-Livestock Systems. Soil Science Society of America Journal, 68, 1875-1884.
https://doi.org/10.2136/sssaj2004.1875
[36]  Malcolm, R. (1982) Assessment of Phophatase Activity in Soils. Soil Biology and Biochemistry, 15, 403-408.
https://doi.org/10.1016/0038-0717(83)90003-2
[37]  Dodgson, K.S. and Spencer, B. (1953) Studies on Sulphatases. 5. The Determination of Inorganic Sulphate in the Study of Sulphatases. The Biochemical Journal, 55, 436-440.
https://doi.org/10.1042/bj0550436
[38]  Berg, J., Tamoczko, J. and Stryer, L. (2003) Biochemistry. W.H. Freeman and Company, New York.
https://books.google.com/books?hl=en&lr=&id=827dBgAAQBAJ&oi=fnd&pg=PR6&dq=Berg,+J.M.,
+Tymoczko,+J.L.+and+Stryer,+L.+(2003+biochemistry.+W.H.+Free-man+and+company,+New+
Yok&ots=jBZzj6ciGY&sig=L54YnhgmyI8Ro1nuNeq8ch0zIeY#v=onepage&q=Berg%2C%20J.M.%2C
&f=false
[39]  Yoon, H.Y., Kim, H.J., Jang, S. and Hong, J.I. (2017) Detection of Bacterial Sulfatase Activity through Liquid-And Solid-Phase Colony-Based Assays. AMB Express, 7, Article ID: 826.
https://doi.org/10.1186/s13568-017-0449-3
[40]  Kertesz, M.A., Kolbener, P., Stockinger, H., Beil, S. and Cook, A.M. (1994) Desulfonation of Linear Alkylbenzenesulfonate Surfactants and Related Compounds by Bacteria. Applied and Environmental Microbiology, 60, 2296-2303.
http://www.ncbi.nlm.nih.gov/pubmed/16349317
[41]  Berg, J.M., Tymoczko, J.L. and Stryer, L. (2007) The Michaelis-Menten Equation Describes the Kinetic Properties of Many Enzymes. In: Berg, J.M., Tymoczko, J.L. and Stryer, L., Eds., Biochemistry, 5th Edition, W. H. Freeman and Company, New York, 216-228.
https://www.ncbi.nlm.nih.gov/books/NBK22430/
[42]  Tazisong, I.A., Senwo, Z.N. and He, Z. (2015) Phosphatase Hydrolysis of Organic Phosphorus Compounds. Advances in Enzyme Research, 3, 39-51.
https://doi.org/10.4236/aer.2015.32005
[43]  Camilloni, C., Bonetti, D., Morrone, A., Giri, R., Dobson, C.M., Brunori, M., Gianni, S. and Vendruscolo, M. (2016) Towards a Structural Biology of the Hydrophobic Effect in Protein Folding. Scientific Reports, 6, Article No. 28285.
https://doi.org/10.1038/srep28285
[44]  Ntoko, F.A. and Senwo, Z.N. (2012) Nitrate Reduction by Commercially Available Nitrate Reductases: Bio-Catalytic Potentials and Enzymatic Activities in the Presence of Metals Ions. Journal of Environmental Science and Health, Part A, 47, 2028-2034.
https://doi.org/10.1080/10934529.2012.695572
[45]  Kim, D.E., Kim, K.H., Bae, Y.J., Lee, J.H., Jang, Y.H. and Nam, S.W. (2005) Purification and Characterization of the Recombinant Arylsulfatase Cloned from Pseudoalteromonas carrageenovora. Protein Expression and Purification, 39, 107-115.
https://doi.org/10.1016/j.pep.2004.09.007
[46]  Parham, J.A. and Deng, S.P. (2000) Detection, Quantification and Characterization of β-Glucosaminidase Activity in Soil. Soil Biology and Biochemistry, 32, 1183-1190.
https://doi.org/10.1016/S0038-0717(00)00034-1

Full-Text

comments powered by Disqus