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Bioprocess and Biosystems Engineering

, Volume 38, Issue 1, pp 165–174 | Cite as

Comparing in situ removal strategies for improving styrene bioproduction

  • Rebekah McKenna
  • Luis Moya
  • Matthew McDaniel
  • David R. NielsenEmail author
Original Paper

Abstract

As an important conventional monomer compound, the biological production of styrene carries significant promise with respect to creating novel sustainable materials. Since end-product toxicity presently limits styrene production by previously engineered Escherichia coli, in situ product removal by both solvent extraction and gas stripping were explored as process-based strategies for circumventing its inhibitory effects. In solvent extraction, the addition of bis(2-ethylhexyl)phthalate offered the greatest productivity enhancement, allowing net volumetric production of 836 ± 64 mg/L to be reached, representing a 320 % improvement over single-phase cultures. Gas stripping rates, meanwhile, were controlled by rates of bioreactor agitation and, to a greater extent, aeration. A periodic gas stripping protocol ultimately enabled up to 561 ± 15 mg/L styrene to be attained. Lastly, by relieving the effects of styrene toxicity, new insight was gained regarding subsequent factors limiting its biosynthesis in E. coli and strategies for future strain improvement are discussed.

Keywords

Styrene In situ product recovery Gas stripping Solvent extraction 

Notes

Acknowledgments

This work was supported by start-up funds from Arizona State University. M.M. was supported by funding from the Fulton Undergraduate Research Initiative (FURI) at Arizona State University. R.M. was supported by Fellowships from ARCS and PEO International.

Supplementary material

449_2014_1255_MOESM1_ESM.docx (151 kb)
Supplementary material 1 (DOCX 151 kb)

References

  1. 1.
    Song H, Lee SY (2006) Production of succinic acid by bacterial fermentation. Enzyme Microb Technol 39:352–361CrossRefGoogle Scholar
  2. 2.
    Abdel-Rahman MA, Tashiro Y, Sonomoto K (2013) Recent advances in lactic acid production by microbial fermentation processes. Biotechnol Adv 31:877–902CrossRefGoogle Scholar
  3. 3.
    Ezeji TC, Qureshi N, Blaschek HP (2007) Bioproduction of butanol from biomass: from genes to bioreactors. Curr Opin Biotechnol 18:220–227CrossRefGoogle Scholar
  4. 4.
    Lee JW, Na D, Park JM, Lee J, Choi S, Lee SY (2012) Systems metabolic engineering of microorganisms for natural and non-natural chemicals. Nat Chem Biol 8:536–546CrossRefGoogle Scholar
  5. 5.
    Yim H, Haselbeck R, Niu W, Pujol-Baxley C, Burgard A, Boldt J, Khandurina J, Trawick JD, Osterhout RE, Stephen R, Estadilla J, Teisan S, Schreyer HB, Andrae S, Yang TH, Lee SY, Burk MJ, Van Dien S (2011) Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol. Nat Chem Biol 7:445–452CrossRefGoogle Scholar
  6. 6.
    Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB (2010) Microbial biosynthesis of alkanes. Science 329:559–562CrossRefGoogle Scholar
  7. 7.
    Atsumi S, Hanai T, Liao JC (2008) Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451:86–89CrossRefGoogle Scholar
  8. 8.
    Tseng HC, Prather KL (2012) Controlled biosynthesis of odd-chain fuels and chemicals via engineered modular metabolic pathways. Proc Natl Acad Sci USA 109:17925–17930CrossRefGoogle Scholar
  9. 9.
    Lu XF, Vora H, Khosla C (2008) Overproduction of free fatty acids in E. coli: implications for biodiesel production. Metab Eng 10:333–339CrossRefGoogle Scholar
  10. 10.
    Steen EJ, Kang Y, Bokinsky G, Hu Z, Schirmer A, McClure A, Del Cardayre SB, Keasling JD (2010) Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature 463:559–562CrossRefGoogle Scholar
  11. 11.
    Dunlop MJ (2011) Engineering microbes for tolerance to next-generation biofuels. Biotechnol Biofuels 4:32CrossRefGoogle Scholar
  12. 12.
    James DH, Castor WM (2011) Styrene. Ullmann’s Encyclopedia of Industrial Chemistry. Wiley-VCH, New YorkGoogle Scholar
  13. 13.
    SRI (2010) Styrene. Access Intelligence LLC Inc, RockwilleGoogle Scholar
  14. 14.
    McKenna R, Nielsen DR (2011) Styrene biosynthesis from glucose by engineered E. coli. Metab Eng 13:544–554CrossRefGoogle Scholar
  15. 15.
    Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A (2011) Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7:487CrossRefGoogle Scholar
  16. 16.
    Lennen RM, Pfleger BF (2013) Modulating membrane composition alters free fatty acid tolerance in Escherichia coli. PLoS ONE 8:e54031CrossRefGoogle Scholar
  17. 17.
    Patnaik R, Louie S, Gavrilovic V, Perry K, Stemmer WP, Ryan CM, del Cardayre S (2002) Genome shuffling of Lactobacillus for improved acid tolerance. Nat Biotechnol 20:707–712CrossRefGoogle Scholar
  18. 18.
    Ghiaci P, Norbeck J, Larsson C (2013) Physiological adaptations of Saccharomyces cerevisiae evolved for improved butanol tolerance. Biotechnol Biofuels 6:101CrossRefGoogle Scholar
  19. 19.
    Daugulis AJ (1988) Integrated reaction and product recovery in bioreactor systems. Biotechnol Prog 4:113–122CrossRefGoogle Scholar
  20. 20.
    Malinowski JJ (2001) Two-phase partitioning bioreactors in fermentation technology. Biotechnol Adv 19:525–538CrossRefGoogle Scholar
  21. 21.
    Vertes AA, Qureshi N, Blaschek HP, Yukawa H, Ezeji TC, Li Y (2010) Advanced product recovery technologies. In: Vertes AA, Qureshi N, Blaschek HP, Yukawa H (eds) Biomass to biofuels: strategies for global industries. Blackwell Publishing Ltd, OxfordCrossRefGoogle Scholar
  22. 22.
    Dafoe JT, Daugulis AJ (2014) In situ product removal in fermentation systems: improved process performance and rational extractant selection. Biotechnol Lett 36:443–460CrossRefGoogle Scholar
  23. 23.
    Gyamerah M, Glover J (1996) Production of ethanol by continuous fermentation and liquid–liquid extraction. J Chem Technol Biotechnol 66:145–152CrossRefGoogle Scholar
  24. 24.
    Weilnhammer C, Blass E (1994) Continuous fermentation with product recovery by in-situ extraction. Chem Eng Technol 17:365–373CrossRefGoogle Scholar
  25. 25.
    Rude MA, Baron TS, Brubaker S, Alibhai M, Del Cardayre SB, Schirmer A (2011) Terminal olefin (1-alkene) biosynthesis by a novel p450 fatty acid decarboxylase from Jeotgalicoccus species. Appl Environ Microbiol 77:1718–1727CrossRefGoogle Scholar
  26. 26.
    Oudshoorn A, van der Wielen LAM, Straathof AJJ (2009) Adsorption equilibria of bio-based butanol solutions using zeolite. Biochem Eng J 48:99–103CrossRefGoogle Scholar
  27. 27.
    Nielsen DR, Prather KJ (2009) In situ product recovery of n-butanol using polymeric resins. Biotechnol Bioeng 102:811–821CrossRefGoogle Scholar
  28. 28.
    Inokuma K, Liao JC, Okamoto M, Hanai T (2010) Improvement of isopropanol production by metabolically engineered Escherichia coli using gas stripping. J Biosci Bioeng 110:696–701CrossRefGoogle Scholar
  29. 29.
    Loser C, Schroder A, Deponte S, Bley T (2005) Balancing the ethanol formation in continuous bioreactors with ethanol stripping. Eng Life Sci 5:325–332CrossRefGoogle Scholar
  30. 30.
    Vane LM (2005) A review of pervaporation for product recovery from biomass fermentation processes. J Chem Technol Biotechnol 80:603–629CrossRefGoogle Scholar
  31. 31.
    Ikegami T, Yanagishita H, Kitamoto D, Haraya K, Nakane T, Matsuda H, Koura N, Sano T (1997) Production of highly concentrated ethanol in a coupled fermentation/pervaporation process using silicalite membranes. Biotechnol Tech 11:921–924CrossRefGoogle Scholar
  32. 32.
    Etschmann MM, Schrader J (2006) An aqueous-organic two-phase bioprocess for efficient production of the natural aroma chemicals 2-phenylethanol and 2-phenylethylacetate with yeast. Appl Microbiol Biotechnol 71:440–443CrossRefGoogle Scholar
  33. 33.
    Etschmann MM, Sell D, Schrader J (2005) Production of 2-phenylethanol and 2-phenylethylacetate from l-phenylalanine by coupling whole-cell biocatalysis with organophilic pervaporation. Biotechnol Bioeng 92:624–634CrossRefGoogle Scholar
  34. 34.
    Jain AN, Khan TR, Daugulis AJ (2010) Bioproduction of benzaldehyde in a solid-liquid two-phase partitioning bioreactor using Pichia pastoris. Biotechnol Lett 32:1649–1654CrossRefGoogle Scholar
  35. 35.
    Khan TR, Daugulis AJ (2010) Application of solid–liquid TPPBs to the production of l-phenylacetylcarbinol from benzaldehyde using Candida utilis. Biotechnol Bioeng 107:633–641CrossRefGoogle Scholar
  36. 36.
    Verhoef S, Wierckx N, Westerhof RG, de Winde JH, Ruijssenaars HJ (2009) Bioproduction of p-hydroxystyrene from glucose by the solvent-tolerant bacterium Pseudomonas putida S12 in a two-phase water-decanol fermentation. Appl Environ Microbiol 75:931–936CrossRefGoogle Scholar
  37. 37.
    Julsing MK, Kuhn D, Schmid A, Buhler B (2012) Resting cells of recombinant E. coli show high epoxidation yields on energy source and high sensitivity to product inhibition. Biotechnol Bioeng 109:1109–1119CrossRefGoogle Scholar
  38. 38.
    Nielsen JH, Villadsen J, Lidén G (2003) Bioreaction engineering principles, 2nd edn. Kluwer Academic/Plenum Publishers, New YorkCrossRefGoogle Scholar
  39. 39.
    Nienow AW (1990) Gas dispersion performance in fermenter operation. Chem Eng Prog 86:61–71Google Scholar
  40. 40.
    Bailey JE, Ollis DF (1986) Biochemical engineering fundamentals, 2nd edn. McGraw-Hill, New YorkGoogle Scholar
  41. 41.
    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 80:33–41CrossRefGoogle Scholar
  42. 42.
    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 65:2324–2332Google Scholar
  43. 43.
    Buhler 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 81:683–694CrossRefGoogle Scholar
  44. 44.
    Buhler B, Witholt B, Hauer B, Schmid A (2002) Characterization and application of xylene monooxygenase for multistep biocatalysis. Appl Environ Microbiol 68:560–568CrossRefGoogle Scholar
  45. 45.
    Prpich GP, Daugulis AJ (2007) Solvent selection for enhanced bioproduction of 3-methylcatechol in a two-phase partitioning bioreactor. Biotechnol Bioeng 97:536–543CrossRefGoogle Scholar
  46. 46.
    Newman JD, Marshall J, Chang M, Nowroozi F, Paradise E, Pitera D, Newman KL, Keasling JD (2006) High-level production of amorpha-4,11-diene in a two-phase partitioning bioreactor of metabolically engineered Escherichia coli. Biotechnol Bioeng 95:684–691CrossRefGoogle Scholar
  47. 47.
    Bruce LJ, Daugulis AJ (1991) Solvent selection strategies for extractive biocatalysis. Biotechnol Prog 7:116–124CrossRefGoogle Scholar
  48. 48.
    Ramos J-L (2004) Pseudomonas. Biosynthesis of macromolecules and molecular metabolism, vol 3. Springer, DordrechtGoogle Scholar
  49. 49.
    Tribe DE (1987) Novel microorganism and method. US Patent 4,681,852Google Scholar
  50. 50.
    Jang HJ, Yoon SH, Ryu HK, Kim JH, Wang CL, Kim JY, Oh DK, Kim SW (2011) Retinoid production using metabolically engineered Escherichia coli with a two-phase culture system. Microb Cell Fact 10:59CrossRefGoogle Scholar
  51. 51.
    Rodriguez GM, Tashiro Y, Atsumi S (2014) Expanding ester biosynthesis in Escherichia coli. Nat Chem Biol 10:259–265CrossRefGoogle Scholar
  52. 52.
    Olaofe OA, Fenner CJ, Gudiminchi RK, Smit MS, Harrison STL (2013) The influence of microbial physiology on biocatalyst activity and efficiency in the terminal hydroxylation of n-octane using Escherichia coli expressing the alkane hydroxylase, CYP153A6. Microb Cell Factories 12Google Scholar
  53. 53.
    U.S. Environmental Protection Agency, EPA on-line tools for site assessment calculation. http://www.epa.gov/athens/learn2model/part-two/onsite/esthenry.html
  54. 54.
    Nielsen DR, Daugulis AJ, McLellan PJ (2007) Dynamic simulation of benzene vapor treatment by a two-phase partitioning bioscrubber. Part I: model development, parameter estimation, and parametric sensitivity. Biochem Eng J 36:239–249CrossRefGoogle Scholar
  55. 55.
    Nielsen DR, Daugulis AJ, McLellan PJ (2007) Dynamic simulation of benzene vapor treatment by a two-phase partitioning bioscrubber. Part II: model calibration, validation, and predictions. Biochem Eng J 36:250–261CrossRefGoogle Scholar
  56. 56.
    McKenna R, Pugh S, Thompson B, Nielsen DR (2013) Microbial production of the aromatic building-blocks (S)-styrene oxide and (R)-1,2-phenylethanediol from renewable resources. Biotechnol J 8:1465–1475CrossRefGoogle Scholar
  57. 57.
    Powell JT, Morrison JF (1978) The purification and properties of the aspartate aminotransferase and aromatic-amino-acid aminotransferase from Escherichia coli. Eur J Biochem/FEBS 87:391–400CrossRefGoogle Scholar
  58. 58.
    Tewari YB, Kishore N, Goldberg RN, Luong TN (1998) An equilibrium and calorimetric study of some transamination reactions. J Chem Thermodyn 30:777–793CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Rebekah McKenna
    • 1
  • Luis Moya
    • 1
  • Matthew McDaniel
    • 1
  • David R. Nielsen
    • 1
    Email author
  1. 1.Department of Chemical Engineering, School for Engineering of Matter, Transport, and EnergyArizona State UniversityTempeUSA

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