Making variability less variable: matching expression system and host for oxygenase-based biotransformations

Journal of Industrial Microbiology and Biotechnology

Volumn 42, Issue 6, 2015, Pages 851-866

  Lindmeyer, Martin ^a   Meyer, Daniel ^a,c   Kuhn, Daniel ^a,d   Bühler, Bruno ^a,b   Schmid, Andreas ^a,b  

^a TU DORTMUND UNIVERSITY   (Germany)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^c ETH ZURICH   (Switzerland)

^d a Novartis company   (Switzerland)

Author keywords

alk regulatory system; Clonal variability; Monooxygenase; Pseudomonas putida; Solvent tolerance

Indexed keywords

OXYGENASE; SOLVENT; STYRENE; STYRENE MONOOXYGENASE; XYLENE MONOOXYGENASE;

BIOCATALYSIS; BIOTRANSFORMATION; CLASSIFICATION; DRUG EFFECTS; ESCHERICHIA COLI; GENETICS; HYDROXYLATION; METABOLISM; PHENOTYPE; PSEUDOMONAS; REPRODUCIBILITY;

BIOCATALYSIS; BIOTRANSFORMATION; ESCHERICHIA COLI; HYDROXYLATION; OXYGENASES; PHENOTYPE; PSEUDOMONAS; REPRODUCIBILITY OF RESULTS; SOLVENTS; STYRENE;

EID: 84937758990     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-015-1615-8     Document Type: Article

References (61)

1. Alonso S, Rendueles M, Diaz M (2012) Physiological heterogeneity of Pseudomonas taetrolens during lactobionic acid production. Appl Microbiol Biotechnol 96(6):1465–1477. doi:10.1007/s00253-012-4254-2
2. Amanullah A, Hewitt CJ, Nienow AW, Lee C, Chartrain M, Buckland BC, Drew SW, Woodley JM (2003) Measurement of strain-dependent toxicity in the indene bioconversion using multiparameter flow cytometry. Biotechnol Bioeng 81(4):405–420. doi:10.1002/Bit.10479
3. Andersson DI, Hughes D (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 8(4):260–271. doi:10.1038/nrmicro2319
4. Avery SV (2006) Microbial cell individuality and the underlying sources of heterogeneity. Nat Rev Microbiol 4(8):577–587. doi:10.1038/nrmicro1460
5. Bagdasarian M, Lurz R, Ruckert B, Franklin FCH, Bagdasarian MM, Frey J, Timmis KN (1981) Specific-purpose plasmid cloning vectors II. Broad host range, high copy number, Rsf 1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas. Gene 16(1–3):237–247. doi:10.1016/0378-1119(81)90080-9
6. Beaumont HJ, Gallie J, Kost C, Ferguson GC, Rainey PB (2009) Experimental evolution of bet hedging. Nature 462(7269):90–93. doi:10.1038/nature08504
7. Birnbaum S, Bailey JE (1991) Plasmid presence changes the relative levels of many host cell proteins and ribosome components in recombinant Escherichia coli. Biotechnol Bioeng 37(8):736–745. doi:10.1002/bit.260370808
8. Blank LM, Ionidis G, Ebert BE, Bühler B, Schmid A (2008) Metabolic response of Pseudomonas putida during redox biocatalysis in the presence of a second octanol phase. FEBS J 275(20):5173–5190. doi:10.1111/j.1742-4658.2008.06648.x
9. Bühler B, Bollhalder I, Hauer B, Witholt B, Schmid A (2003) Use of the two-liquid phase concept to exploit kinetically controlled multistep biocatalysis. Biotechnol Bioeng 81(6):683–694. doi:10.1002/Bit.10512
10. Bühler B, Schmid A, Hauer B, Witholt B (2000) Xylene monooxygenase catalyzes the multistep oxygenation of toluene and pseudocumene to corresponding alcohols, aldehydes, and acids in Escherichia coli JM101. J Biol Chem 275(14):10085–10092. doi:10.1074/jbc.275.14.10085
11. Bühler B, Witholt B, Hauer B, Schmid A (2002) Characterization and application of xylene monooxygenase for multistep biocatalysis. Appl Environ Microbiol 68(2):560–568. doi:10.1128/Aem.68.2.560-568.2002
12. Canosa I, Sanchez-Romero JM, Yuste L, Rojo F (2000) A positive feedback mechanism controls expression of AlkS, the transcriptional regulator of the Pseudomonas oleovorans alkane degradation pathway. Mol Microbiol 35(4):791–799
13. Carneiro S, Ferreira EC, Rocha I (2013) Metabolic responses to recombinant bioprocesses in Escherichia coli. J Biotechnol 164(3):396–408. doi:10.1016/j.jbiotec.2012.08.026
14. Choi KH, Kumar A, Schweizer HP (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64(3):391–397. doi:10.1016/j.mimet.2005.06.001
15. Delvigne F, Goffin P (2014) Microbial heterogeneity affects bioprocess robustness: dynamic single-cell analysis contributes to understanding of microbial populations. Biotechnol J 9(1):61–72. doi:10.1002/biot.201300119
16. Durfee T, Nelson R, Baldwin S, Plunkett G 3rd, Burland V, Mau B, Petrosino JF, Qin X, Muzny DM, Ayele M, Gibbs RA, Csorgo B, Posfai G, Weinstock GM, Blattner FR (2008) The complete genome sequence of Escherichia coli DH10B: insights into the biology of a laboratory workhorse. J Bacteriol 190(7):2597–2606. doi:10.1128/JB.01695-07
17. Ebert BE, Kurth F, Grund M, Blank LM, Schmid A (2011) Response of Pseudomonas putida KT2440 to increased NADH and ATP demand. Appl Environ Microbiol 77(18):6597–6605. doi:10.1128/AEM.05588-11
18. Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002) Stochastic gene expression in a single cell. Science 297(5584):1183–1186. doi:10.1126/science.1070919
19. Grand View Research MRC (2014) Biotechnology market (Biopharmacy, Bioservices, Bioagriculture, Bioindustrial, Fermentation, DNA sequencing, Tissue Engineering, Regeneration) analysis and segment forecasts to 2020. http://www.grandviewresearch.com/industry-analysis/biotechnology-market
20. Gross R, Lang K, Bühler K, Schmid A (2010) Characterization of a biofilm membrane reactor and its prospects for fine chemical synthesis. Biotechnol Bioeng 105(4):705–717. doi:10.1002/Bit.22584
21. Halan B, Schmid A, Buehler K (2010) Maximizing the productivity of catalytic biofilms on solid supports in membrane aerated reactors. Biotechnol Bioeng 106(4):516–527. doi:10.1002/bit.22732
22. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166(4):557–580. doi:10.1016/S0022-2836(83)80284-8
23. Hartmans S, van der Werf MJ, de Bont JA (1990) Bacterial degradation of styrene involving a novel flavin adenine dinucleotide-dependent styrene monooxygenase. Appl Environ Microbiol 56(5):1347–1351
24. Heipieper HJ, de Bont JA (1994) Adaptation of Pseudomonas putida S12 to ethanol and toluene at the level of fatty acid composition of membranes. Appl Environ Microbiol 60(12):4440–4444
25. Heipieper HJ, Neumann G, Cornelissen S, Meinhardt F (2007) Solvent-tolerant bacteria for biotransformations in two-phase fermentation systems. Appl Microbiol Biotechnol 74(5):961–973. doi:10.1007/s00253-006-0833-4
26. Hewitt CJ, Caron GNV, Nienow AW, McFarlane CM (1999) The use of multi-parameter flow cytometry to compare the physiological response of Escherichia coli W3110 to glucose limitation during batch, fed-batch and continuous culture cultivations. J Biotechnol 75(2–3):251–264. doi:10.1016/S0168-1656(99)00168-6
27. Jahn M, Seifert J, von Bergen M, Schmid A, Bühler B, Müller S (2012) Subpopulation-proteomics in prokaryotic populations. Curr Opin Biotechnol 24(1):79–87. doi:10.1016/j.copbio.2012.10.017
28. Jahn M, Vorpahl C, Turkowsky D, Lindmeyer M, Bühler B, Harms H, Müller S (2014) Accurate determination of plasmid copy number of flow-sorted cells using droplet digital PCR. Anal Chem 86(12):5969–5976. doi:10.1021/ac501118v
29. Julsing MK, Kuhn D, Schmid A, Bühler B (2012) Resting cells of recombinant E. coli show high epoxidation yields on energy source and high sensitivity to product inhibition. Biotechnol Bioeng 109(5):1109–1119. doi:10.1002/bit.24404
30. Junker F, Ramos JL (1999) Involvement of the cis/trans isomerase Cti in solvent resistance of Pseudomonas putida DOT-T1E. J Bacteriol 181(18):5693–5700
31. Kaern M, Elston TC, Blake WJ, Collins JJ (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6(6):451–464. doi:10.1038/nrg1615
32. Kieboom J, Dennis JJ, Zylstra GJ, de Bont JA (1998) Active efflux of organic solvents by Pseudomonas putida S12 is induced by solvents. J Bacteriol 180(24):6769–6772
33. Köhler KA, Rückert C, Schatschneider S, Vorhölter FJ, Szczepanowski R, Blank LM, Niehaus K, Goesmann A, Pühler A, Kalinowski J, Schmid A (2013) Complete genome sequence of Pseudomonas sp. strain VLB120 a solvent tolerant, styrene degrading bacterium, isolated from forest soil. J Biotechnol 168(4):729–730. doi:10.1016/j.jbiotec.2013.10.016
34. Kuhn D, Bühler B, Schmid A (2012) Production host selection for asymmetric styrene epoxidation: Escherichia coli vs. solvent-tolerant Pseudomonas. J Ind Microbiol Biotechnol 39(8):1125–1133. doi:10.1007/s10295-012-1126-9
35. Kuhn D, Kholiq MA, Heinzle E, Bühler B, Schmid A (2010) Intensification and economic and ecological assessment of a biocatalytic oxyfunctionalization process. Green Chem 12(5):815–827. doi:10.1039/b921896c
36. Leak DJ, Sheldon RA, Woodley JM, Adlercreutz P (2009) Biocatalysts for selective introduction of oxygen. Biocatal Biotransform 27(1):1–26. doi:10.1080/10242420802393519
37. Messing J (1979) A multipurpose cloning system based on the single-stranded DNA bacteriophage M13. Recomb DNA Tech Bull 3(2):43–49
38. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VA, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen JA, Timmis KN, Dusterhoft A, Tummler B, Fraser CM (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4(12):799–808. doi:10.1046/j.1462-2920.2002.00366.x
39. Neumann G, Kabelitz N, Zehnsdorf A, Miltner A, Lippold H, Meyer D, Schmid A, Heipieper HJ (2005) Prediction of the adaptability of Pseudomonas putida DOT-T1E to a second phase of a solvent for economically sound two-phase biotransformations. Appl Environ Microbiol 71(11):6606–6612. doi:10.1128/Aem.71.11.6606-6612.2005
40. Nikolic N, Barner T, Ackermann M (2013) Analysis of fluorescent reporters indicates heterogeneity in glucose uptake and utilization in clonal bacterial populations. BMC Microbiol 13:258. doi:10.1186/1471-2180-13-258
41. Otto K, Hofstetter K, Rothlisberger M, Witholt B, Schmid A (2004) Biochemical characterization of StyAB from Pseudomonas sp. strain VLB120 as a two-component flavin-diffusible monooxygenase. J Bacteriol 186(16):5292–5302. doi:10.1128/JB.186.16.5292-5302.2004
42. Panke S, Held M, Wubbolts MG, Witholt B, Schmid A (2002) Pilot-scale production of (S)-styrene oxide from styrene by recombinant Escherichia coli synthesizing styrene monooxygenase. Biotechnol Bioeng 80(1):33–41. doi:10.1002/Bit.10346
43. Panke S, Meyer A, Huber CM, Witholt B, Wubbolts MG (1999) An alkane-responsive expression system for the production of fine chemicals. Appl Environ Microbiol 65(6):2324–2332
44. Panke S, Wubbolts MG, Schmid A, Witholt B (2000) Production of enantiopure styrene oxide by recombinant Escherichia coli synthesizing a two-component styrene monooxygenase. Biotechnol Bioeng 69(1):91–100. doi:10.1002/(SICI)1097-0290(20000705)69:1<91:AID-BIT11>3.0.CO;2-X
45. Pedraza JM, van Oudenaarden A (2005) Noise propagation in gene networks. Science 307(5717):1965–1969. doi:10.1126/science.1109090
46. Ramos JL, Duque E, Huertas MJ, Haidour A (1995) Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high-concentrations of aromatic-hydrocarbons. J Bacteriol 177(14):3911–3916
47. Rausenberger J, Fleck C, Timmer J, Kollmann M (2009) Signatures of gene expression noise in cellular systems. Prog Biophys Mol Biol 100(1–3):57–66. doi:10.1016/j.pbiomolbio.2009.06.003
48. Rojas A, Duque E, Mosqueda G, Golden G, Hurtado A, Ramos JL, Segura A (2001) Three efflux pumps are required to provide efficient tolerance to toluene in Pseudomonas putida DOT-T1E. J Bacteriol 183(13):3967–3973. doi:10.1128/JB.183.13.3967-3973.2001
49. Rojo F, Dinamarca MA (2004) Catabolite repression and physiological control. In: Ramos JL, Filloux A (eds) Pseudomonas, virulence and gene regulation, vol 2. Springer, New York, pp 365–387
50. Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, Band 1. New York
51. Sanchez-Romero MA, Casadesus J (2014) Contribution of phenotypic heterogeneity to adaptive antibiotic resistance. Proc Natl Acad Sci USA 111(1):355–360. doi:10.1073/pnas.1316084111
52. Schrewe M, Julsing MK, Bühler B, Schmid A (2013) Whole-cell biocatalysis for selective and productive C-O functional group introduction and modification. Chem Soc Rev 42(15):6346–6377. doi:10.1039/c3cs60011d
53. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52(3–4):591–611. doi:10.2307/2333709
54. Siegele DA, Hu JC (1997) Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc Natl Acad Sci USA 94(15):8168–8172
55. Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59(2):201–222
56. Silva-Rocha R, de Lorenzo V (2010) Noise and robustness in prokaryotic regulatory networks. Annu Rev Microbiol 64:257–275. doi:10.1146/annurev.micro.091208.073229
57. Smits TH, Seeger MA, Witholt B, van Beilen JB (2001) New alkane-responsive expression vectors for Escherichia coli and Pseudomonas. Plasmid 46(1):16–24. doi:10.1006/plas.2001.1522
58. + recombinants. J Bacteriol 181(5):1610–1616
59. Suzuki M, Hayakawa T, Shaw JP, Rekik M, Harayama S (1991) Primary structure of xylene monooxygenase: similarities to and differences from the alkane hydroxylation system. J Bacteriol 173(5):1690–1695
60. Timmis KN (2002) Pseudomonas putida: a cosmopolitan opportunist par excellence. Environ Microbiol 4(12):779–781. doi:10.1046/j.1462-2920.2002.00365.x
61. Woodley JM (2006) Microbial biocatalytic processes and their development. Adv Appl Microbiol 60:1–15. doi:10.1016/S0065-2164(06)60001-4