Enzymatic and whole cell catalysis : Finding new strategies for old processes

The use of enzymes and whole bacterial cells has allowed the production of a plethora of compounds that have been used for centuries in foods and beverages. However, only recently we have been able to master techniques that allow the design and development of new biocatalysts with high stability and productivity. Rational redesign and directed evolution have lead to engineered enzymes with new characteristics whilst the understanding of adaptation mechanisms in bacterial cells has allowed their use under new operational conditions. Bacteria able to thrive under the most extreme conditions have also provided new and extraordinary catalytic processes. In this review, the new tools available for the improvement of biocatalysts are presented and discussed.

[1]  Shintaro Iwatani,et al.  Introduction of a stress-responsive gene, yggG, enhances the yield of l-phenylalanine with decreased acetic acid production in a recombinant Escherichia coli , 2009, Biotechnology Letters.

[2]  M. Adams,et al.  Release of lignin from kraft pulp by a hyperthermophilic xylanase from Thermatoga maritima , 1997 .

[3]  Akihiko Kondo,et al.  Effect of fatty acid membrane composition on whole-cell biocatalysts for biodiesel-fuel production , 2004 .

[4]  Gürkan Sin,et al.  Application of mechanistic models to fermentation and biocatalysis for next-generation processes. , 2010, Trends in biotechnology.

[5]  W. M. Vos,et al.  Characterization of pyrolysin, a hyperthermoactive serine protease from the archaebacterium Pyrococcus furiosus. , 1990 .

[6]  Hou-Jin Li,et al.  Biotransformation of limonene by marine bacteria , 2006 .

[7]  C. Yanofsky,et al.  Improving the catalytic activity of a thermophilic enzyme at low temperatures. , 2000, Biochemistry.

[8]  Y.‐H.P. Zhang,et al.  Production of biocommodities and bioelectricity by cell-free synthetic enzymatic pathway biotransformations: challenges and opportunities. , 2010, Biotechnology and bioengineering.

[9]  D. Yernool,et al.  Purification, characterization, and molecular analysis of thermostable cellulases CelA and CelB from Thermotoga neapolitana. , 1998, Applied and environmental microbiology.

[10]  Yusuf Chisti,et al.  Biotechnology-a sustainable alternative for chemical industry. , 2005, Biotechnology advances.

[11]  F. Arnold,et al.  Directed evolution of enzyme catalysts. , 1997, Trends in biotechnology.

[12]  Guan-Chiun Lee,et al.  Gene cloning, expression, and biochemical characterization of a recombinant trehalose synthase from Picrophilus torridus in Escherichia coli. , 2006, Journal of agricultural and food chemistry.

[13]  C. Vorgias,et al.  Extreme environments as a resource for microorganisms and novel biocatalysts. , 2005, Advances in biochemical engineering/biotechnology.

[14]  Donald A. Comfort,et al.  Impact of Substrate Glycoside Linkage and Elemental Sulfur on Bioenergetics of and Hydrogen Production by the Hyperthermophilic Archaeon Pyrococcus furiosus , 2007, Applied and Environmental Microbiology.

[15]  N J Russell,et al.  Membranes as a target for stress adaptation. , 1995, International journal of food microbiology.

[16]  K. Kong,et al.  The highly stable alcohol dehydrogenase of Thermomicrobium roseum: purification and molecular characterization. , 2002, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[17]  Gürkan Sin,et al.  Matrix notation for efficient development of first‐principles models within PAT applications: Integrated modeling of antibiotic production with Streptomyces coelicolor , 2008, Biotechnology and bioengineering.

[18]  Christopher A. Voigt,et al.  De novo design of biocatalysts. , 2002, Current opinion in chemical biology.

[19]  W. Hummel,et al.  Cloning, sequence analysis, and heterologous expression of the gene encoding a (S)-specific alcohol dehydrogenase from Rhodococcus erythropolis DSM 43297 , 2003, Applied Microbiology and Biotechnology.

[20]  E. Sym.  Action of esterase in the presence of organic solvents. , 1936, Biochemical Journal.

[21]  Axel Zeeck,et al.  Big Effects from Small Changes: Possible Ways to Explore Nature's Chemical Diversity , 2002, Chembiochem : a European journal of chemical biology.

[22]  Rainer Kalscheuer,et al.  Microdiesel: Escherichia coli engineered for fuel production. , 2006, Microbiology.

[23]  P. Cirino,et al.  Advancing Biocatalysis through Enzyme, Cellular, and Platform Engineering , 2008, Biotechnology progress.

[24]  Karl-Erich Jaeger,et al.  Prospecting for biocatalysts and drugs in the genomes of non-cultured microorganisms. , 2004, Current opinion in biotechnology.

[25]  Mark V Brown,et al.  Culture clash: challenging the dogma of microbial diversity , 2007, The ISME Journal.

[26]  A. Abate,et al.  Ultrahigh-throughput screening in drop-based microfluidics for directed evolution , 2010, Proceedings of the National Academy of Sciences.

[27]  A. Wiseman,et al.  Novel biocatalytic enzymes by directed evolution. , 2001, Trends in biotechnology.

[28]  B. Lee,et al.  Biotechnological Methods to Accelerate Cheddar Cheese Ripening , 2006, Critical reviews in biotechnology.

[29]  C. Carvalho,et al.  Bacterial Whole Cell Biotransformations: In Vivo Reactions Under In Vitro Conditions , 2009 .

[30]  Xinhao Ye,et al.  Biofuels Production by Cell-Free Synthetic Enzymatic Technology , 2008 .

[31]  Matthias Heinemann,et al.  Exploiting cell‐free systems: Implementation and debugging of a system of biotransformations , 2010, Biotechnology and bioengineering.

[32]  QUANTITATIVE ANALYSES OF BIOCHEMICAL KINETIC RESOLUTIONS OF ENANTIOMERS , 1983 .

[33]  Carla C. C. R. de Carvalho,et al.  Adaptation of Rhodococcus erythropolis cells to high concentrations of toluene , 2007, Applied Microbiology and Biotechnology.

[34]  J. Huska,et al.  Effect of starvation and chloramphenicol on acceleration of bacterial dihexyl sulfosuccinate biotransformation , 2008, Folia Microbiologica.

[35]  Christoph Hold,et al.  Towards the engineering of in vitro systems , 2009, Journal of The Royal Society Interface.

[36]  G. Challis,et al.  2-Alkyl-4-hydroxymethylfuran-3-carboxylic acids, antibiotic production inducers discovered by Streptomyces coelicolor genome mining , 2008, Proceedings of the National Academy of Sciences.

[37]  Kiran L. Kadam,et al.  Flexible biorefinery for producing fermentation sugars, lignin and pulp from corn stover , 2008, Journal of Industrial Microbiology & Biotechnology.

[38]  D. Cowan,et al.  An extremely thermostable extracellular proteinase from a strain of the archaebacterium Desulfurococcus growing at 88 degrees C. , 1987, The Biochemical journal.

[39]  E. Sym.  Lipase and its action: The synthetic action of pancreatic lipase in the system: oleic acid-glycerol-water-dissolved lipase. , 1930, The Biochemical journal.

[40]  M. Yasuda,et al.  Effect of exchange of amino acid residues of the surface region of the PST-01 protease on its organic solvent-stability. , 2007, Biochemical and biophysical research communications.

[41]  J. Chaudhuri,et al.  Biocatalysis in organic media using enzymes from extremophiles , 1999 .

[42]  V. Stojanoff,et al.  Structure determination of the extracellular xylanase from Geobacillus stearothermophilus by selenomethionyl MAD phasing. , 2004, Acta crystallographica. Section D, Biological crystallography.

[43]  C. A. Fewson,et al.  Biotransformations catalyzed by the genus Rhodococcus. , 1994, Critical reviews in biotechnology.

[44]  Ramesh N. Patel.  Synthesis of chiral pharmaceutical intermediates by biocatalysis , 2008 .

[45]  J. Hurley,et al.  Determinants of cofactor specificity in isocitrate dehydrogenase: structure of an engineered NADP+ --> NAD+ specificity-reversal mutant. , 1996, Biochemistry.

[46]  B Hauer,et al.  Environmentally directed mutations and their impact on industrial biotransformation and fermentation processes. , 2000, Current opinion in microbiology.

[47]  M. Pons,et al.  Behaviour of Mycobacterium sp. NRRL B-3805 whole cells in aqueous, organic-aqueous and organic media studied by fluorescence microscopy , 2004, Applied Microbiology and Biotechnology.

[48]  M. Reetz,et al.  Directed evolution of enantioselective enzymes for organic chemistry. , 2000, Current opinion in chemical biology.

[49]  D. Sell,et al.  Applied biocatalysis for the synthesis of natural flavour compounds – current industrial processes and future prospects , 2004, Biotechnology Letters.

[50]  M. Brimble,et al.  Molecules derived from the extremes of life. , 2009, Natural product reports.

[51]  Linda G. Otten,et al.  Enzyme engineering for enantioselectivity: from trial-and-error to rational design? , 2010, Trends in biotechnology.

[52]  W. Liebl.  Cellulolytic enzymes from Thermotoga species. , 2001, Methods in enzymology.

[53]  H. Heipieper,et al.  Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems , 2007, Applied Microbiology and Biotechnology.

[54]  Jason A. Papin,et al.  Genome-Scale Reconstruction and Analysis of the Pseudomonas putida KT2440 Metabolic Network Facilitates Applications in Biotechnology , 2008, PLoS Comput. Biol..

[55]  G. Feller,et al.  Some like it cold: biocatalysis at low temperatures. , 2004, FEMS microbiology reviews.

[56]  G. Stephanopoulos,et al.  Metabolic flux distributions in Corynebacterium glutamicum during growth and lysine overproduction , 2000, Biotechnology and bioengineering.

[57]  P S Miller,et al.  Extremophile‐inspired strategies for enzymatic biomass saccharification , 2010, Environmental technology.

[58]  E. Delong,et al.  Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing , 1991, Journal of bacteriology.

[59]  Carla C. C. R. de Carvalho,et al.  Cell adaptation to solvent, substrate and product: a successful strategy to overcome product inhibition in a bioconversion system , 2005, Applied Microbiology and Biotechnology.

[60]  F. Arnold,et al.  Protein engineering of oxygenases for biocatalysis. , 2002, Current opinion in chemical biology.

[61]  A. Dean,et al.  Redesigning secondary structure to invert coenzyme specificity in isopropylmalate dehydrogenase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[62]  F. Keulen,et al.  Modelling the biokinetic resolution of diastereomers present in unequal initial amounts , 2002 .

[63]  Abdul W Basit,et al.  The gastrointestinal microbiota as a site for the biotransformation of drugs. , 2008, International journal of pharmaceutics.

[64]  J. Handelsman.  Metagenomics: Application of Genomics to Uncultured Microorganisms , 2004, Microbiology and Molecular Biology Reviews.

[65]  Shu-Wei Chang,et al.  Biocatalysis for the production of industrial products and functional foods from rice and other agricultural produce. , 2008, Journal of agricultural and food chemistry.

[66]  K. Soda,et al.  A Cold-Adapted Lipase of an Alaskan Psychrotroph,Pseudomonas sp. Strain B11-1: Gene Cloning and Enzyme Purification and Characterization , 1998, Applied and Environmental Microbiology.

[67]  R. Kelly,et al.  The genus Thermotoga: recent developments , 2010, Environmental technology.

[68]  B. G. Davis,et al.  Biocatalysis and Enzymes in Organic Synthesis , 2002 .

[69]  Jonathan D. Trent,et al.  DNA from Uncultured Organisms as a Source of 2,5-Diketo-d-Gluconic Acid Reductases , 2001, Applied and Environmental Microbiology.

[70]  A. Pandey,et al.  An organic-solvent-tolerant esterase from thermophilic Bacillus licheniformis S-86. , 2009, Bioresource technology.

[71]  S. Adhikari,et al.  Biorefineries: Current Status, Challenges, and Future Direction , 2006 .

[72]  J. D. Egan,et al.  Making Taq DNA polymerase in the undergraduate biology laboratory , 2007 .

[73]  F. Arnold,et al.  Directed evolution of biocatalysts. , 1999, Current opinion in chemical biology.

[74]  U. Krings,et al.  Biotechnological production of flavours and fragrances , 1998, Applied Microbiology and Biotechnology.

[75]  A. Ginolhac,et al.  Environmental metagenomics: An innovative resource for industrial biocatalysis , 2007 .

[76]  N. Qureshi,et al.  High-throughput screening of cellulase F mutants from multiplexed plasmid sets using an automated plate assay on a functional proteomic robotic workcell , 2006, Proteome Science.

[77]  R. Daniel,et al.  Thermostable beta-glucosidase and beta-xylosidase from Thermotoga sp. strain FjSS3-B.1. , 1993, Biochimica et biophysica acta.

[78]  P. Halling,et al.  Why did biocatalysis in organic media not take off in the 1930s? , 1999, Trends in biotechnology.

[79]  T. Fukui,et al.  A Unique Chitinase with Dual Active Sites and Triple Substrate Binding Sites from the Hyperthermophilic Archaeon Pyrococcus kodakaraensis KOD1 , 1999, Applied and Environmental Microbiology.

[80]  R. Herbert.  A perspective on the biotechnological potential of extremophiles. , 1992, Trends in biotechnology.

[81]  J. Mielenz,et al.  High-Yield Hydrogen Production from Starch and Water by a Synthetic Enzymatic Pathway , 2007, PloS one.

[82]  Garabed Antranikian,et al.  Industrial relevance of thermophilic Archaea. , 2005, Current opinion in microbiology.

[83]  F. Arnold,et al.  Directed evolution of a thermostable esterase. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[84]  G. Challis,et al.  Strategies for the Discovery of New Natural Products by Genome Mining , 2009, Chembiochem : a European journal of chemical biology.

[85]  C. Carvalho,et al.  Principal component analysis applied to bacterial cell behaviour in the presence of organic solvents , 2004 .

[86]  H. Griengl,et al.  The use of substrate engineering in biohydroxylation. , 2002, Current opinion in biotechnology.

[87]  R. Marchant,et al.  Improving the quality of industrially important enzymes by directed evolution , 2001, Molecular and Cellular Biochemistry.

[88]  H. Pinheiro,et al.  Optimization of androstenedione production in an organic–aqueous two-liquid phase system , 2004 .

[89]  O. Holst,et al.  Cloning, sequencing and overexpression of a Rhodothermus marinus gene encoding a thermostable cellulase of glycosyl hydrolase family 12 , 1998, Applied Microbiology and Biotechnology.

[90]  Bertus van den Burg,et al.  Extremophiles as a source for novel enzymes. , 2003 .

[91]  K. Shanmugam,et al.  Engineering the metabolism of Escherichia coli W3110 for the conversion of sugar to redox-neutral and oxidized products: Homoacetate production , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[92]  E. Getzoff,et al.  Faster superoxide dismutase mutants designed by enhancing electrostatic guidance , 1992, Nature.

[93]  Lee R Lynd,et al.  Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield , 2008, Proceedings of the National Academy of Sciences.

[94]  Hua Zhao,et al.  Improving the Enzyme Catalytic Efficiency Using Ionic Liquids with Kosmotropic Anions , 2006 .

[95]  Jack Liang,et al.  Practical chiral alcohol manufacture using ketoreductases. , 2010, Current opinion in chemical biology.

[96]  Frances H. Arnold,et al.  Inverting enantioselectivity by directed evolution of hydantoinase for improved production of l-methionine , 2000, Nature Biotechnology.

[97]  M. Wilkinson,et al.  Mechanisms of incorporation and release of enzymes into cheese during ripening , 2005 .

[98]  S. Farajnia,et al.  Cloning and over-expression of Penicillin G acylase in Escherichia coli BL21 , 2010 .

[99]  Gregory Stephanopoulos,et al.  Engineering microbial cell factories for biosynthesis of isoprenoid molecules: beyond lycopene. , 2007, Trends in biotechnology.

[100]  C. Schmidt-Dannert,et al.  Directed evolution of industrial enzymes. , 1999, Trends in biotechnology.

[101]  W. Baumeister,et al.  A hyperthermostable protease of the subtilisin family bound to the surface layer of the Archaeon Staphylothermus marinus , 1996, Current Biology.

[102]  D. Prieur,et al.  Pyrococcus CH1, an obligate piezophilic hyperthermophile: extending the upper pressure-temperature limits for life , 2009, The ISME Journal.

[103]  M. de Rosa,et al.  The production of biocatalysts and biomolecules from extremophiles. , 2002, Trends in biotechnology.

[104]  M. Reetz,et al.  Enantioselective enzymes for organic synthesis created by directed evolution. , 2000, Chemistry.

[105]  M. Koffas,et al.  Biosynthesis of isoprenoids, polyunsaturated fatty acids and flavonoids in Saccharomyces cerevisiae , 2006, Microbial cell factories.

[106]  A. Steinbüchel,et al.  Polymer production by two newly isolated extremely halophilic archaea: application of a novel corrosion-resistant bioreactor , 2000, Applied Microbiology and Biotechnology.

[107]  Stephen H. Brown,et al.  Purification and characterization of a highly thermostable glucose isomerase produced by the extremely thermophilic eubacterium, Thermotoga maritima , 1993, Biotechnology and bioengineering.

[108]  M. Turner,et al.  Introduction to Biocatalysis, Using Enzymes and Microorganisms. , 1995 .

[109]  Gary Walsh,et al.  Therapeutic insulins and their large-scale manufacture , 2005, Applied Microbiology and Biotechnology.

[110]  Andreas Schmid,et al.  The production of fine chemicals by biotransformations. , 2002, Current opinion in biotechnology.

[111]  F. Arnold,et al.  Tuning the activity of an enzyme for unusual environments: sequential random mutagenesis of subtilisin E for catalysis in dimethylformamide. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[112]  M. Podar,et al.  New opportunities revealed by biotechnological explorations of extremophiles. , 2006, Current opinion in biotechnology.

[113]  A. Kamaruddin,et al.  Dynamic kinetic resolution: alternative approach in optimizing S-ibuprofen production , 2006, Bioprocess and biosystems engineering.

[114]  Gaosen Zhang,et al.  Soil microbial counts and identification of culturable bacteria in an extreme by arid zone , 2008, Folia Microbiologica.

[115]  Roberto Fernandez-Lafuente,et al.  Improvement of enzyme activity, stability and selectivity via immobilization techniques , 2007 .

[116]  J. Lucey,et al.  Major technological advances and trends in cheese. , 2006, Journal of dairy science.

[117]  Y. Ni,et al.  Outer membrane mutation effects on UDP-glucose permeability and whole-cell catalysis rate , 2006, Applied Microbiology and Biotechnology.

[118]  S. Q. Yang,et al.  Biobleach boosting effect of recombinant xylanase B from the hyperthermophilic Thermotoga maritima on wheat straw pulp , 2006, Applied Microbiology and Biotechnology.

[119]  D. Demirjian,et al.  Enzymes from extremophiles. , 2001, Current opinion in chemical biology.

[120]  H. Heipieper,et al.  Cell wall adaptations of planktonic and biofilm Rhodococcus erythropolis cells to growth on C5 to C16 n-alkane hydrocarbons , 2009, Applied Microbiology and Biotechnology.

[121]  H. Heipieper,et al.  Adaptation of Rhodococcus erythropolis DCL14 to growth on n-alkanes, alcohols and terpenes , 2005, Applied Microbiology and Biotechnology.

[122]  C. Carvalho,et al.  Ancient Procedures for the High-Tech World: Health Benefits and Antimicrobial Compounds from the Mediterranean Empires , 2008 .

[123]  F. Brockman,et al.  Effect of Starvation on Induction of Quinoline Degradation for a Subsurface Bacterium in a Continuous-Flow Column , 1992, Applied and environmental microbiology.

[124]  Shui-Tein Chen,et al.  Optimization of a thermostable lipase from Bacillus stearothermophilus P1: overexpression, purification, and characterization. , 2001, Protein expression and purification.

[125]  Jay D Keasling,et al.  Production of isoprenoid pharmaceuticals by engineered microbes , 2006, Nature chemical biology.

[126]  U. Bornscheuer,et al.  Directed Evolution of an Esterase from Pseudomonas fluorescens Yields a Mutant with Excellent Enantioselectivity and Activity for the Kinetic Resolution of a Chiral Building Block , 2006, Chembiochem : a European journal of chemical biology.

[127]  Joonhong Park,et al.  Effect of carbon starvation on toluene degradation activity by toluene monooxygenase-expressing bacteria , 2006, Biodegradation.

[128]  Haruyuki Atomi,et al.  Recent progress towards the application of hyperthermophiles and their enzymes. , 2005, Current opinion in chemical biology.

[129]  K. Mullis,et al.  Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. , 1988, Science.

[130]  R. Chen,et al.  Enzyme engineering: rational redesign versus directed evolution. , 2001, Trends in biotechnology.

[131]  K. Jirage,et al.  New developments in membrane-based separations. , 1999, Trends in biotechnology.

[132]  Herbert Märkl,et al.  Fermentation of extremophilic microorganisms , 1996 .

[133]  G. Antranikian,et al.  CHARACTERIZATION OF THE XYLANOLYTIC ENZYME SYSTEM OF THE EXTREME THERMOPHILIC ANAEROBIC BACTERIA THERMOTOGA MARITIMA, T. NEAPOLITANA, AND T. THERMARUM , 1997 .

[134]  Y. Zhuang,et al.  DNA shuffling of methionine adenosyltransferase gene leads to improved S-adenosyl-L-methionine production in Pichia pastoris. , 2009, Journal of biotechnology.

[135]  R. Sharp,et al.  Development of defined and minimal media for the growth of the hyperthermophilic archaeon Pyrococcus furiosus Vc1 , 1997 .

[136]  Virginia W Cornish,et al.  Milestones in directed enzyme evolution. , 2002, Current opinion in chemical biology.