Abstract
Multiple forms of one enzyme occur in a wide variety of microorganisms. Their synthesis is often dependent on culture characteristics such as medium composition, physico-chemical parameters, culture age and the presence of inducing or inhibiting agents. Multiform enzymes increase the capability of the producing organism to adapt to and cope with a wide variety of environmental changes, such that the physiological advantages outweigh the apparent wasteful hyperproduction of multiple forms of one enzyme.
References
Abe K, Ito Y, Ohmachi T, Asada Y (1997) Purification and properties of two isozymes of gamma-glutamyltranspeptidase from Bacillus subtilis TAM-4. Biosci. Biotechnol. Biochem. 61: 1621–1625.
Alves AMCR, Euverink GJW, Santos H, Dijkhuizen L (2001) Different physiological roles of ATP-and PPi-dependent phosphofructokinase isoenzymes in the methylotrophic actinomycete Amycolatopsis methanolica. J. Bacteriol. 183: 7231–7240.
Bartling S, Wegener C, Oslen O (1995) Synergism between Erwinia pectate lyase isoenzymes that depolymerize both pectate and pectin. Microbiology 141: 873–881.
Beecher J, Grogan G, Roberts S, Willetts A (1996) Enantioselective oxidations by the diketocamphane monooxygenase isozymes from Pseudomonas putida. Biotechnol. Lett. 18: 571–576.
Bonacker LG, Baudner S, Moerschel E, Boecher R, Thauer RK (1994) Properties of the two isoenzymes of methyl-coenzyme M reductase in Methanobacterium thermoautotrophicum. Eur. J. Biochem. 217: 587–595.
Briganti F, Pessione E, Giunta C, Mazzoli R, Scozzafava A (2000) Purification and catalytic properties of two catechol-1,2-dioxygenase isozymes from benzoate-grown cells of Acinetobacter radioresistens. J. Protein Chem. 19: 709–716.
Burne RA, Penders JEC (1994) Differential localization of the Streptococcus mutans GS-5 fructan hydrolase enzyme, FruA. FEMS Microbiol. Lett. 121: 243–250.
Delgado MJ, Fernandez-Lopez M, Bedmar EJ (1998) Soluble and membrane bound nitrate reductase from Bradyrhizobium japonicum bacteroids. Plant Physiol. Biochem. 36: 279–283.
Ferguson DJ, Krzycki JA, Grahame DA (1996) Specific roles of methylcobamide: coenzyme M methyltransferase isozymes in metabolism of methanol and methylamines in Methanosarcina barkeri. J. Biol. Chem. 271: 5189–5194.
Fernandez-Lopez M, Olivares J, Bedmar EJ (1994) Two differentially regulated nitrate reductases required for nitrate-dependent, microaerobic growth of Bradyrhizobium japonicum. Arch. Microbiol. 162: 310–315.
Froehlich KU, Wiedemann M, Lottspeich F, Mecke D (1989) Substitution of a pentalenolactone-sensitive glyceraldehyde-3-phosphate dehydrogenase by a genetically distinct resistant isoform accompanies pentalenolactone production in Streptomyces arenae. J. Bacteriol. 171: 6696–6702.
Grahame DA (1989) Different isozymes of methylcobalamin: 2-mercaptoethanesulfonate methyltransferase predominate in methanol-versus acetate-grown Methanosarcina barkeri. J. Biol. Chem. 264: 12890–12894.
Han YW (1990) Microbial levan. Adv. Appl. Microbiol. 35: 171–194.
Hayashi NR, Arai H, Kodama T, Igarashi Y (1999) The cbbQ genes, located downstream of the form I and form II RubisCO genes, affect the activity of both RubisCOs. Biochem. Biophys. Res. Commun. 265: 177–183.
Hazra PP, Sengupta T, Mukhopadhyay A, Ghosh AK, Mukherjee M, Sengupta S (1997) Regulation of protein secretion by mycelial culture of the mushroom Termitomyces clypeatus. FEMS Microbiol. Lett. 154: 239–243.
He L, Bickerstaff GF, Paterson A, Buswell JA (1994) Evaluation of catalytic activity and synergism between two xylanase isoenzymes in enzymic hydrolysis of two separate xylans in different states of solubility. Enzyme Microb. Technol. 16: 696–702.
Hicks DB (1995) Purification of three catalase isozymes from facultatively alkaliphilic Bacillus firmus OF4. Biochim. Biophys. Acta 1229: 347–355.
Hochheimer A, Hedderich R, Thauer RK (1998) The formylmethanofuran dehydrogenase isoenzymes in Methanobacterium wolfei and Methanobacterium thermoautotrophicum: induction of the molybdenum isoenzyme by molybdate and constitutive synthesis of the tungsten isoenzyme. Arch. Microbiol. 170: 389–393.
Hunter RL, Markert CL (1957) Histochemical demonstration of enzymes separated by zone electrophoresis in starch gels. Science 125: 1294–1295.
Hussain M, Pastor FIJ, Lampen JO (1987) Cloning and sequencing of the blaZ gene encoding ?-lactamase III, a lipoprotein of Bacillus cereus 569/H. J. Bacteriol. 169: 579–586.
Ishii A, Suzuki M, Sahara T, Takada Y, Sasaki S, Fukunaga N (1993) Genes encoding two isocitrate dehydrogenase isozymes of a psychrophilic bacterium, Vibrio sp. strain ABE-1. J. Bacteriol. 175: 6873–6880.
Iwashita K, Nagahara T, Kimura H, Takano M, Shimoi H, Ito K (1999) The bglA gene of Aspergillus kawachii encodes both extracellular and cell wall-bound ?-glucosidases. Appl. Environ. Microbiol. 65: 5546–5553.
Iwashita K, Shimoi H, Ito K (2001) Extracellular soluble polysaccharide (ESP) from Aspergillus kawachii improves the stability of extracellular ?-glucosidase (EX-1 and EX-2) and is involved in their localization. J. Biosci. Bioeng. 91: 134–140.
Kalcheva EO, Faiziev MM, Shanskaya VO, Maluta SS (1994) Regulation of two aspartokinase isozymes in Streptococcus bovis. Can. J. Microbiol. 40: 224–227.
Klotz MG, Anderson AJ (1994) The role of catalase isozymes in the culturability of the root colonizer Pseudomonas putida after exposure to hydrogen peroxide and antibiotics. Can. J. Microbiol. 40: 382–387.
Laan H, Smid EJ, de Leij L, Schwander E, Konings WN (1988) Monoclonal antibodies to the cell-wall-associated proteinase of Lactococcus lactis subsp. cremoris Wg2. Appl. Environ. Microbiol. 54: 2250–2256.
LeClerc GM, Grahame DA (1996) Methylcobamide: coenzyme M methyltransferase isozymes from Methanosarcina barkeri. J. Biol. Chem. 271: 18725–18731.
Lee MJ, Lee YC, Kim CH (1997) Intracellular and extracellular forms of alkaline pullulanase from an alkaliphilic Bacillus sp. S-1. Arch. Biochem. Biophys. 337: 308–316.
Lotti M, Monticelli S, Montesinos JL, Brocca S, Valero F, Lafuente J (1998) Physiological control on the expression and secretion of Candida rugosa lipase. Chem. Phys. Lipids 93: 143–148.
Marsh EN, Chang MDT, Townsend CA (1992) Two isozymes of clavaminate synthase central to clavulanic acid formation: cloning and sequencing of both genes from Streptomyces clavuligerus. Biochemistry 31: 12648–12657.
Mattson P, Meklin S, Korpela T (1990) Analysis of cyclomaltodextrin glucanotransferase isoenzymes by isoelectric focusing in immobilized pH gradients. J. Biochem. Biophys. Meth. 20: 237–246.
McMillan GP, Johnston DJ, Perombelon MCM (1992) Purification to homogeneity of extracellular polygalacturonase and isoenzymes of pectate lyase of Erwinia carotovora ssp. atroseptica by column chromatography. J. Appl. Bacteriol. 73: 83–86.
Mitamura T, Urabe I, Okada H (1989) Enzymatic properties of isozymes and variants of glucose dehydrogenase from Bacillus megaterium. Eur. J. Biochem. 186: 389–394.
Mitchell CG, Anderson S, El-Mansi EMT (1995) Purification and characterization of citrate synthase isoenzymes from Pseudomonas aeruginosa. Biochem. J. 309: 507–511.
Moss GP (1992) Nomenclature of multiple forms of enzymes. In: Liébecq C, ed. Biochemical Nomenclature and Related Documents, 2nd edn. Seattle: Portland Press.
Murakami S, Wang CL, Naito A, Shinke R, Aoki K (1998) Purification and characterization of four catechol-1,2-dioxygenase isozymes from the benzamide-assimilating bacterium Arthrobacter species BA-5-17. Microbiol. Res. 153: 163–171.
Murrell JC, Gilbert B, McDonald IR (2000) Molecular biology and regulation of methane monooxygenase. Arch. Microbiol. 173: 325–332.
Nagao T, Mitamura T, Wang XH, Negoro S, Yomo T, Urabe I, Okada H (1992) Cloning, nucleotide sequences, and enzymatic properties of glucose dehydrogenase isozymes from Bacillus megaterium IAM 1030. J. Bacteriol. 174: 5013–5020.
Nakai C, Horiike K, Kuramitsu S, Kagamiyama H, Nozaki M (1990) Three isozymes of catechol-1,2-dioxygenase (pyrocatechase), alpha-alpha, alpha-beta, and beta-beta, from Pseudomonas arvilla C-1. J. Biol. Chem. 265: 660–665.
Novak J, Kopecky J, Vanek Z (1997) Nitrogen source regulates expression of alanine dehydrogenase isoenzymes in Streptomyces avermitilis in a chemically defined medium. Can. J. Microbiol. 43: 189–193.
Novak JS, Tabita FR (1999) Molecular approaches to probe differential NADH activation of phosphoribulokinase isozymes from Rhodobacter sphaeroides. Arch. Biochem. Biophys. 363: 273–282.
Pennings JLA, De Wijs JLJ, Keltjens JT, Van Der Drift C (1997) Medium-reductant directed expression of methyl coenzyme M reductase isoenzymes in Methanobacterium thermoautotrophicum (strain DELTA-H). FEBS Lett. 410: 235–237.
Pessione E, Giuffrida MG, Mazzoli R, Caposio P, Landolfo S, Conti A, Giunta C, Gribaudo G (2001) The catechol-1,2 dioxygenase system of Acinetobacter radioresistens: isoenzymes, inductors and gene localisation. Biol. Chem. 382: 1253–1261.
Pihl TD, Sharma S, Reeve JN (1994) Growth phase-dependent transcription of the genes that encode the two methyl coenzyme M reductase isoenzymes and N-5-methyltetrahydromethanopterin: coenzyme M methyltransferase in Methanobacterium thermoautotrophicum DELTA-H. J. Bacteriol. 176: 6384–6391.
Pugsley AP, Schwartz M (1985) Export and secretion of proteins by bacteria. FEMS Microbiol. Rev. 32: 3–38.
Purich DL, Allison RD (2000) Handbook of Biochemical Kinetics. London: Academic Press.
Robyt JF, Walseth TF (1979) Production, purification and properties of dextransucrase from Leuconostoc mesenteroides NRRL B-512F. Carbohydr. Res. 68: 95–111.
Rossi M, Defez R, Chiurazzi M, Lamberti A, Fuggi A, Iaccarino M (1989) Regulation of glutamine synthetase isoenzymes in Rhizobium leguminosarum biovar viceae. J. Gen. Microbiol. 135: 629–638.
Roth J, Bendayan M, Orci L (1978) Immunocytochemical localization of intracellular antigens by the use of protein A-gold complex. J. Histochem. Cytochem. 26: 1074–1081.
Schmitz RA, Albracht SPJ, Thauer RK (1992) A molybdenum and a tungsten isoenzyme of formylmethanofuran dehydrogenase in the thermophilic archaeon Methanobacterium wolfei. Eur. J. Biochem. 209: 1013–1018.
Sengupta T, Hazra PP, Mukhopadhyay A, Sengupta S (1998) Termitomyces clypeatus controls secretion of extracellular amyloglucosidase by regulating exocytosis of vacuolar enzyme. FEMS Microbiol. Lett. 158: 101–105.
Shaw CR (1969) Isozymes: classification, frequency, and significance. Int. Rev. Cytol. 25: 297–332.
Shimada Y, Sugihara A, Nagao T, Tominaga Y (1992) Induction of Geotrichum candidum lipase by long-chain fatty acids. J. Ferment. Bioeng. 74: 77–80.
Silhavy TJ, Benson SA, Emr SD (1983) Mechanisms of protein localization. Microbiol. Rev. 47: 313–344.
Stanier RY, Ingraham JL, Wheelis ML, Painter PR (1986) The Microbial World, 5th edn. New Jersey: Prentice-Hall.
Stanley SH, Prior SD, Leak DJ, Dalton H (1983) Copper stress underlies the fundamental change in intracellular location of methane monooxygenase in methan-oxidising organisms: studies in batch and continuous cultures. Biotechnol. Lett. 5: 487–492.
Suzuki M, Sahara T, Tsuruha JI, Takada Y, Fukunaga N (1995) Differential expression in Escherichia coli of the Vibrio sp. strain ABE-1 icdI and icdII genes encoding structurally different isocitrate dehydrogenase isozymes. J. Bacteriol. 177: 2138–2142.
Tamarit J, Cabiscol E, Aguilar J, Ros J (1997) Differential inactivation of alcohol dehydrogenase isoenzymes in Zymomonas mobilis by oxygen. J. Bacteriol. 179: 1102–1104.
Tamoi M, Ishikawa T, Takeda T, Shigeoka S (1996) Molecular characterization and resistance to hydrogen peroxide of two fructose-1,6-biphosphatase from Synechococcus PCC 7942. Arch. Biochem. Biophys. 334: 27–36.
Vacik DN, Toren ECJ (1982) Separation and measurement of isoenzymes and other proteins by high-performance liquid chromatography. J. Chromatogr. 228: 1–31.
Van Den Bergh ERE, Van Der Krooij TAW, Dijkhuizen L, Meijer WG (1995) Fructosebiphosphatase isoenzymes of the chemoautotroph Xanthobacter flavus. J. Bacteriol. 177: 5860–5864.
Vorholt JA, Vaupel M, Thauer RK (1997) A selenium-dependent and a selenium-independent formylmethanofuran dehydrogenase and their transcriptional regulation in the hyperthermophilic Methanopyrus kandleri. Mol. Microbiol. 23: 1033–1042.
Yeliseev A, Gaertner P, Harms U, Linder D, Thauer RK (1993) Function of methylcobalamin: coenzyme m methyltransferase isoenzyme II in Methanosarcina barkeri. Arch. Microbiol. 159: 530–536.
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Naessens, M., Vandamme, E.J. Multiple forms of microbial enzymes. Biotechnology Letters 25, 1119–1124 (2003). https://doi.org/10.1023/A:1024540902848
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DOI: https://doi.org/10.1023/A:1024540902848