Skip to main content
SpringerLink
Log in

Promoting microbial utilization of phenolic substrates from bio-oil

  • Bioenergy/Biofuels/Biochemicals - Original Paper
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

The economic viability of the biorefinery concept is limited by the valorization of lignin. One possible method of lignin valorization is biological upgrading with aromatic-catabolic microbes. In conjunction, lignin monomers can be produced by fast pyrolysis and fractionation. However, biological upgrading of these lignin monomers is limited by low water solubility. Here, we address the problem of low water solubility with an emulsifier blend containing approximately 70 wt% Tween® 20 and 30 wt% Span® 80. Pseudomonas putida KT2440 grew to an optical density (OD600) of 1.0 ± 0.2 when supplied with 1.6 wt% emulsified phenolic monomer-rich product produced by fast pyrolysis of red oak using an emulsifier dose of 0.076 ± 0.002 g emulsifier blend per g of phenolic monomer-rich product. This approach partially mitigated the toxicity of the model phenolic monomer p-coumarate to the microbe, but not benzoate or vanillin. This study provides a proof of concept that processing of biomass-derived phenolics to increase aqueous availability can enhance microbial utilization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Abdelaziz OY, Brink DP, Prothmann J, Ravi K, Sun MZ, Garcia-Hidalgo J, Sandahl M, Hulteberg CP, Turner C, Liden G, Gorwa-Grauslund MF (2016) Biological valorization of low molecular weight lignin. Biotechnol Adv 34:1318–1346. https://doi.org/10.1016/j.biotechadv.2016.10.001

    Article  CAS  PubMed  Google Scholar 

  2. Alwadani N, Fatehi P (2018) Synthetic and lignin-based surfactants: challenges and opportunities. Carbon Resour Convers 1:126–138

    Article  Google Scholar 

  3. Ateş F, Pütün E, Pütün AE (2004) Fast pyrolysis of sesame stalk: yields and structural analysis of bio-oil. J Anal Appl Pyrol 71:779–790. https://doi.org/10.1016/j.jaap.2003.11.001

    Article  CAS  Google Scholar 

  4. Bai X, Kim KH, Brown RC, Dalluge E, Hutchinson C, Lee YJ, Dalluge D (2014) Formation of phenolic oligomers during fast pyrolysis of lignin. Fuel 128:170–179. https://doi.org/10.1016/j.fuel.2014.03.013

    Article  CAS  Google Scholar 

  5. Baker CJ, Mock NM, Whitaker BD, Roberts DP, Rice CP, Deahl KL, Aver’yanov AA (2005) Involvement of acetosyringone in plant-pathogen recognition. Biochem Biophys Res Commun 328:130–136. https://doi.org/10.1016/j.bbrc.2004.12.153

    Article  CAS  PubMed  Google Scholar 

  6. Bar-Even A, Noor E, Flamholz A, Buescher JM, Milo R (2011) Hydrophobicity and charge shape cellular metabolite concentrations. PLoS Comput Biol 7:e1002166. https://doi.org/10.1371/journal.pcbi.1002166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bayly RC, Wigmore GJ (1973) Metabolism of phenol and cresols by mutants of Pseudomonas putida. J Bacteriol 113:1112–1120

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Becker J, Kuhl M, Kohlstedt M, Starck S, Wittmann C (2018) Metabolic engineering of Corynebacterium glutamicum for the production of cis, cis-muconic acid from lignin. Microb Cell Fact 17:115. https://doi.org/10.1186/s12934-018-0963-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Beckham GT, Johnson CW, Karp EM, Salvachúa D, Vardon DR (2016) Opportunities and challenges in biological lignin valorization. Curr Opin Biotechnol 42:40–53

    Article  CAS  Google Scholar 

  10. Calero P, Jensen SI, Bojanovič K, Lennen RM, Koza A, Nielsen AT (2018) Genome-wide identification of tolerance mechanisms toward p-coumaric acid in Pseudomonas putida. Biotechnol Bioeng 115:762–774. https://doi.org/10.1002/bit.26495

    Article  CAS  PubMed  Google Scholar 

  11. Chi Z, Zhao X, Daugaard T, Rover M, Johnston P, Salazar AM, Santoscoy MC, Smith R, Brown RC, Wen Z, Zabotina O, Jarboe LR (2019) Comparison of product distribution, content and fermentability of biomass in a hybrid thermochemical/biological processing platform. Biomass Bioenerg 120:107–116

    Article  CAS  Google Scholar 

  12. Chiaramonti D, Bonini M, Fratini E, Tondi G, Gartner K, Bridgwater AV, Grimm HP, Soldaini I, Webster A, Baglioni P (2003) Development of emulsions from biomass pyrolysis liquid and diesel and their use in engines—part 1: emulsion production. Biomass Bioenerg 25:85–99. https://doi.org/10.1016/S0961-9534(02)00183-6

    Article  CAS  Google Scholar 

  13. Colombi BL, Zanoni PRS, Tavares LBB (2018) Effect of phenolic compounds on bioconversion of glucose to ethanol by yeast Saccharomyces cerevisiae PE-2. Can J Chem Eng 96:1444–1450. https://doi.org/10.1002/cjce.23114

    Article  CAS  Google Scholar 

  14. Davis KM, Rover MR, Brown RC, Bai X, Wen Z, Jarboe LR (2016) Recovery and utilization of lignin monomers as part of the biorefinery approach. Energies 9:808–831. https://doi.org/10.3390/en9100808

    Article  CAS  Google Scholar 

  15. Davis R, Tao L, Tan ECD, Biddy MJ, Beckham GT, Scarlata C, Jacobson J, Cafferty K, Ross J, Lukas J, Knorr D, Schoen P (2013) Process design and economics for the conversion of lignocellulosic biomass to hydrocarbons: dilute-acid and enzymatic deconstruction of biomass to sugars and biological conversion of sugars to hydrocarbons. National Renewable Energy Laboratory

  16. Donsi F, Annunziata M, Vincensi M, Ferrari G (2012) Design of nanoemulsion-based delivery systems of natural antimicrobials: effect of the emulsifier. J Biotechnol 159:342–350. https://doi.org/10.1016/j.jbiotec.2011.07.001

    Article  CAS  PubMed  Google Scholar 

  17. Doong RA, Lei WG (2003) Solubilization and mineralization of polycyclic aromatic hydrocarbons by Pseudomonas putida in the presence of surfactant. J Hazard Mater 96:15–27. https://doi.org/10.1016/s0304-3894(02)00167-x

    Article  CAS  PubMed  Google Scholar 

  18. Elliott DC, Wang H, Rover M, Whitmer L, Smith R, Brown R (2015) hydrocarbon liquid production via catalytic hydroprocessing of phenolic oils fractionated from fast pyrolysis of red oak and corn stover. ACS Sustain Chem Eng 3:892–902. https://doi.org/10.1021/acssuschemeng.5b00015

    Article  CAS  Google Scholar 

  19. Feist CF, Hegeman GD (1969) Phenol and benzomate metabolism by Pseudomonas putida—regulation of tangential pathways. J Bacteriol 100:869–877

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Flies DB, Chen L (2003) A simple and rapid vortex method for preparing antigen/adjuvant emulsions for immunization. J Immunol Methods 276:239–242. https://doi.org/10.1016/S0022-1759(03)00081-4

    Article  CAS  PubMed  Google Scholar 

  21. Gadhave AD, Waghmare JT (2014) A short review on microemulsion and its application in extraction of vegetable oil. Int J Res Eng Technol 3:147–158

    Google Scholar 

  22. Hou JJ, Qiu Z, Han H, Zhang QZ (2018) Toxicity evaluation of lignocellulose-derived phenolic inhibitors on Saccharomyces cerevisiae growth by using the QSTR method. Chemosphere 201:286–293. https://doi.org/10.1016/j.chemosphere.2018.03.008

    Article  CAS  PubMed  Google Scholar 

  23. Hu W, Dang Q, Rover M, Brown RC, Wright MM (2016) Comparative techno-economic analysis of advanced biofuels, biochemicals, and hydrocarbon chemicals via the fast pyrolysis platform. Biofuels 7:87–103. https://doi.org/10.1080/17597269.2015.1118780

    Article  CAS  Google Scholar 

  24. Inc IA (1984) The HLB system: a time-saving guide to emulsifier selection. ICI Americas, Wilmington

    Google Scholar 

  25. Jarboe LR, Chi Z (2013) Inhibition of microbial biocatalysts by biomass-derived aldehydes and methods for engineering tolerance. In: Torrioni L, Pescasseroli E (eds) New developments in aldehydes research. Nova Science Publishers, Incorporated

    Google Scholar 

  26. Jarboe LR, Liu P, Royce LA (2011) Engineering inhibitor tolerance for the production of biorenewable fuels and chemicals. Curr Opin Chem Eng 1:38–42. https://doi.org/10.1016/j.coche.2011.08.003

    Article  CAS  Google Scholar 

  27. Jayakody LN, Johnson CW, Whitham JM, Giannone RJ, Black BA, Cleveland NS, Klingeman DM, Michener WE, Olstad JL, Vardon DR, Brown RC, Brown SD, Hettich RL, Guss AM, Beckham GT (2018) Thermochemical wastewater valorization via enhanced microbial toxicity tolerance. Energy Environ Sci 11:1625–1638. https://doi.org/10.1039/c8ee00460a

    Article  CAS  Google Scholar 

  28. Jimenez JI, Minambres B, Garcia JL, Diaz E (2002) Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 4:824–841. https://doi.org/10.1046/j.1462-2920.2002.00370.x

    Article  CAS  PubMed  Google Scholar 

  29. Johnson CW, Beckham GT (2015) Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin. Metab Eng 28:240–247. https://doi.org/10.1016/j.ymben.2015.01.005

    Article  CAS  PubMed  Google Scholar 

  30. Kaczorek E, Olszanowski A (2011) Uptake of hydrocarbon by Pseudomonas fluorencens (P1) and Pseudomonas putida (K1) strains in the presence of surfactants: a cell surface modification. Water Air Soil Pollut 214:451–459

    Article  CAS  Google Scholar 

  31. Kamimura N, Takahashi K, Mori K, Araki T, Fujita M, Higuchi Y, Masai E (2017) Bacterial catabolism of lignin-derived aromatics: new findings in a recent decade: update on bacterial lignin catabolism. Environ Microbiol Rep 9:679–705. https://doi.org/10.1111/1758-2229.12597

    Article  CAS  PubMed  Google Scholar 

  32. Karmakar B, Vohra RM, Nandanwar H, Sharma P, Gupta KG, Sobti RC (2000) Rapid degradation of ferulic acid via 4-vinylguaiacol and vanillin by a newly isolated strain of Bacillus coagulans. J Biotechnol 80:195–202. https://doi.org/10.1016/s0168-1656(00)00248-0

    Article  CAS  PubMed  Google Scholar 

  33. Kim J-S (2015) Production, separation and applications of phenolic-rich bio-oil—a review. Biores Technol 178:90–98. https://doi.org/10.1016/j.biortech.2014.08.121

    Article  CAS  Google Scholar 

  34. Klinke HB, Olsson L, Thomsen AB, Ahring BK (2003) Potential inhibitors from wet oxidation of wheat straw and their effect on ethanol production of Saccharomyces cerevisiae: wet oxidation and fermentation by yeast. Biotechnol Bioeng 81:738–747. https://doi.org/10.1002/bit.10523

    Article  CAS  PubMed  Google Scholar 

  35. Kohlstedt M, Starck S, Barton N, Stolzenberger J, Selzer M, Mehlmann K, Schneider R, Pleissner D, Rinkel J, Dickschat JS, Venus J, van Duuren J, Wittmann C (2018) From lignin to nylon: cascaded chemical and biochemical conversion using metabolically engineered Pseudomonas putida. Metab Eng 47:279–293. https://doi.org/10.1016/j.ymben.2018.03.003

    Article  CAS  PubMed  Google Scholar 

  36. Linger JG, Vardon DR, Guarnieri MT, Karp EM, Hunsinger GB, Franden MA, Johnson CW, Chupka G, Strathmann TJ, Pienkos PT, Beckham GT (2014) Lignin valorization through integrated biological funneling and chemical catalysis. Proc Natl Acad Sci 111:12013–12018. https://doi.org/10.1073/pnas.1410657111

    Article  CAS  PubMed  Google Scholar 

  37. Liu Y, Liu Z, Zeng G, Chen M, Jiang Y, Shao B, Li Z, Liu Y (2018) Effect of surfactants on the interaction of phenol with laccase: molecular docking and molecular dynamics simulation studies. J Hazard Mater 357:10–18. https://doi.org/10.1016/j.jhazmat.2018.05.042

    Article  CAS  PubMed  Google Scholar 

  38. Liu ZH, Xie SX, Lin FR, Jin MJ, Yuan JS (2018) Combinatorial pretreatment and fermentation optimization enabled a record yield on lignin bioconversion. Biotechnol Biofuels 11:21. https://doi.org/10.1186/s13068-018-1021-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lv G, Wang F, Cai W, Zhang X (2014) Characterization of the emulsions formed by catastrophic phase inversion. Colloids Surf A 450:141–147. https://doi.org/10.1016/j.colsurfa.2014.03.023

    Article  CAS  Google Scholar 

  40. Michinobu T, Hishida M, Sato M, Katayama Y, Masai E, Nakamura M, Otsuka Y, Ohara S, Shigehara K (2008) Polyesters of 2-pyrone-4,6-dicarboxylic acid (PDC) obtained from a metabolic intermediate of lignin. Polym J 40:68–75. https://doi.org/10.1295/polymj.PJ2007158

    Article  CAS  Google Scholar 

  41. Mycroft Z, Gomis M, Mines P, Law P, Bugg TDH (2015) Biocatalytic conversion of lignin to aromatic dicarboxylic acids in Rhodococcus jostii RHA1 by re-routing aromatic degradation pathways. Green Chem 17:4974–4979. https://doi.org/10.1039/c5gc01347j

    Article  CAS  Google Scholar 

  42. Nikel PDV (2018) Pseudomonas putida as a functional chassis for industrial biocatalysis: from native biochemistry to trans-metabolism. Metab Eng 50:142–155

    Article  CAS  Google Scholar 

  43. Oconnor K, Buckley CM, Hartmans S, Dobson ADW (1995) Possible regulatory role for nonaromatic carbon sources in styrene degradation by Pseudomonas putida CA-3. Appl Environ Microbiol 61:544–548

    CAS  Google Scholar 

  44. Oleskowicz-Popiel P, Klein-Marcuschamer D, Simmons BA, Blanch HW (2014) Lignocellulosic ethanol production without enzymes—technoeconomic analysis of ionic liquid pretreatment followed by acidolysis. Biores Technol 158:294–299. https://doi.org/10.1016/j.biortech.2014.02.016

    Article  CAS  Google Scholar 

  45. Pollard AS, Rover MR, Brown RC (2012) Characterization of bio-oil recovered as stage fractions with unique chemical and physical properties. J Anal Appl Pyrol 93:129–138

    Article  CAS  Google Scholar 

  46. Porras M, Solans C, González C, Gutiérrez JM (2008) Properties of water-in-oil (W/O) nano-emulsions prepared by a low-energy emulsification method. Colloids Surf A 324:181–188. https://doi.org/10.1016/j.colsurfa.2008.04.012

    Article  CAS  Google Scholar 

  47. Pradilla D, Vargas W, Alvarez O (2015) The application of a multi-scale approach to the manufacture of concentrated and highly concentrated emulsions. Chem Eng Res Des 95:162–172. https://doi.org/10.1016/j.cherd.2014.10.016

    Article  CAS  Google Scholar 

  48. Rabenhorst J (1996) Production of methoxyphenol-type natural aroma chemicals by biotransformation of eugenol with a new Pseudomonas sp. Appl Microbiol Biotechnol 46:470–474. https://doi.org/10.1007/s002530050846

    Article  CAS  Google Scholar 

  49. Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F, Davis MF, Davison BH, Dixon RA, Gilna P, Keller M, Langan P, Naskar AK, Saddler JN, Tschaplinski TJ, Tuskan GA, Wyman CE (2014) Lignin valorization: improving lignin processing in the biorefinery. Science 334:709–720

    Google Scholar 

  50. Rahate AR, Nagarkar JM (2007) Emulsification of vegetable oils using a blend of nonionic surfactants for cosmetic applications. J Dispersion Sci Technol 28:1077–1080

    Article  CAS  Google Scholar 

  51. Ramos JL, Duque E, Gallegos M-T, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in Gram negative bacteria. Annu Rev Microbiol 56:743–768

    Article  CAS  Google Scholar 

  52. Ravi K, Garcia-Hidalgo J, Gorwa-Grauslund MF, Liden G (2017) Conversion of lignin model compounds by Pseudomonas putida KT2440 and isolates from compost. Appl Microbiol Biotechnol 101:5059–5070. https://doi.org/10.1007/s00253-017-8211-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Reva ON, Weinel C, Weinel M, Böhm K, Stjepandic D, Hoheisel JD, Tümmler B (2006) Functional genomics of stress response in Pseudomonas putida KT2440. J Bacteriol 188:4079–4092

    Article  CAS  Google Scholar 

  54. Rinaldi R, Jastrzebski R, Clough MT, Ralph J, Kennema M, Bruijnincx PCA, Weckhuysen BM (2016) Paving the way for lignin valorisation: recent advances in bioengineering, biorefining and catalysis. Angew Chem Int Ed 55:8164–8215. https://doi.org/10.1002/anie.201510351

    Article  CAS  Google Scholar 

  55. Rogers JG, Brammer JG (2012) Estimation of the production cost of fast pyrolysis bio-oil. Biomass Bioenerg 36:208–217. https://doi.org/10.1016/j.biombioe.2011.10.028

    Article  CAS  Google Scholar 

  56. Rojo MC, Lopez FNA, Lerena MC, Mercado L, Torres A, Combina M (2015) Evaluation of different chemical preservatives to control Zygosaccharomyces rouxii growth in high sugar culture media. Food Control 50:349–355. https://doi.org/10.1016/j.foodcont.2014.09.014

    Article  CAS  Google Scholar 

  57. Rover MR (2013) Analysis of sugars and phenolic compounds in bio-oil. Iowa State University, Ames

    Book  Google Scholar 

  58. Rover MR, Brown RC (2013) Quantification of total phenols in bio-oil using the Folin–Ciocalteu method. J Anal Appl Pyrol 104:366–371. https://doi.org/10.1016/j.jaap.2013.06.011

    Article  CAS  Google Scholar 

  59. Rover MR, Friend AJ, Smith RG, Brown RC (2018) Enabling biomass combustion and co-firing through the use of Lignocol. Fuel 211:312–317. https://doi.org/10.1016/j.fuel.2017.09.076

    Article  CAS  Google Scholar 

  60. Rover MR, Hall PH, Johnston PA, Smith RG, Brown RC (2015) Stabilization of bio-oils using low temperature, low pressure hydrogenation. Fuel 153:224–230. https://doi.org/10.1016/j.fuel.2015.02.054

    Article  CAS  Google Scholar 

  61. Rover MR, Johnston PA, Jin T, Smith RG, Brown RC, Jarboe L (2014) Production of clean pyrolytic sugars for fermentation. Chemsuschem 7:1662–1668. https://doi.org/10.1002/cssc.201301259

    Article  CAS  PubMed  Google Scholar 

  62. Rover MR, Johnston PA, Whitmer LE, Smith RG, Brown RC (2014) The effect of pyrolysis temperature on recovery of bio-oil as distinctive stage fractions. J Anal Appl Pyrol 105:262–268. https://doi.org/10.1016/j.jaap.2013.11.012

    Article  CAS  Google Scholar 

  63. Sainsbury PD, Hardiman EM, Ahmad M, Otani H, Seghezzi N, Eltis LD, Bugg TDH (2013) Breaking down lignin to high-value chemicals: the conversion of lignocellulose to vanillin in a gene deletion mutant of Rhodococcus jostii RHA1. ACS Chem Biol 8:2151–2156. https://doi.org/10.1021/cb400505a

    Article  CAS  PubMed  Google Scholar 

  64. Salvachua D, Johnson CW, Singer CA, Rohrer H, Peterson DJ, Black BA, Knapp A, Beckham GT (2018) Bioprocess development for muconic acid production from aromatic compounds and lignin. Green Chem 20:5007–5019. https://doi.org/10.1039/c8gc02519c

    Article  CAS  Google Scholar 

  65. Salvachúa D, Karp EM, Nimlos CT, Vardon DR, Beckham GT (2015) Towards lignin consolidated bioprocessing: simultaneous lignin depolymerization and product generation by bacteria. Green Chem 17:4951–4967

    Article  Google Scholar 

  66. Shen Y, Jarboe L, Brown R, Wen Z (2015) A thermochemical–biochemical hybrid processing of lignocellulosic biomass for producing fuels and chemicals. Biotechnol Adv 33:1799–1813. https://doi.org/10.1016/j.biotechadv.2015.10.006

    Article  CAS  PubMed  Google Scholar 

  67. Shim H, Yang ST (1999) Biodegradation of benzene, toluene, ethylbenzene, and o-xylene by a coculture of Pseudomonas putida and Pseudomonas fluorescens immobilized in a fibrous-bed bioreactor. J Biotechnol 67:99–112. https://doi.org/10.1016/s0168-1656(98)00166-7

    Article  CAS  PubMed  Google Scholar 

  68. Shingler V, Powlowski J, Marklund U (1992) Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas SP Strain-CF600. J Bacteriol 174:711–724. https://doi.org/10.1128/jb.174.3.711-724.1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Sonoki T, Takahashi K, Sugita H, Hatamura M, Azuma Y, Sato T, Suzuki S, Kamimura N, Masai E (2018) Glucose-free cis, cis-muconic acid production via new metabolic designs corresponding to the heterogeneity of lignin. ACS Sustain Chem Eng 6:1256–1264. https://doi.org/10.1021/acssuschemeng.7b03597

    Article  CAS  Google Scholar 

  70. Vardon DR, Franden MA, Johnson CW, Karp EM, Guarnieri MT, Linger JG, Salm MJ, Strathmann TJ, Beckham GT (2015) Adipic acid production from lignin. Energy Environ Sci 8:617–628. https://doi.org/10.1039/c4ee03230f

    Article  CAS  Google Scholar 

  71. Wang L, Zhang R, Li J, Guo L, Yang HP, Ma FY, Yu HB (2018) Comparative study of the fast pyrolysis behavior of ginkgo, poplar, and wheat straw lignin at different temperatures. Ind Crops Prod 122:465–472. https://doi.org/10.1016/j.indcrop.2018.06.038

    Article  CAS  Google Scholar 

  72. Wang S, Wang Y, Cai Q, Wang X, Jin H, Luo Z (2014) Multi-step separation of monophenols and pyrolytic lignins from the water-insoluble phase of bio-oil. Sep Purif Technol 122:248–255. https://doi.org/10.1016/j.seppur.2013.11.017

    Article  CAS  Google Scholar 

  73. Wright MM, Daugaard DE, Satrio JA, Brown RC (2010) Techno-economic analysis of biomass fast pyrolysis to transportation fuels. Fuel 89. Supplement 1:S2–S10. https://doi.org/10.1016/j.fuel.2010.07.029

    Article  CAS  Google Scholar 

  74. Yang S, Long Y, Yan H, Cai HW, Li YD, Wang XG (2017) Gene cloning, identification, and characterization of the multicopper oxidase CumA from Pseudomonas sp 593. Biotechnol Appl Biochem 64:347–355. https://doi.org/10.1002/bab.1501

    Article  CAS  PubMed  Google Scholar 

  75. Zaldivar J, Ingram LO (1999) Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnol Bioeng 66:203–210. https://doi.org/10.1002/(sici)1097-0290(1999)66:4%3c203:Aid-bit1%3e3.3.Co;2-r

    Article  CAS  PubMed  Google Scholar 

  76. Zaldivar J, Martinez A, Ingram LO (1999) Effect of selected aldehydes on the growth and fermentation of ethanologenic Escherichia coli. Biotechnol Bioeng 65:24–33. https://doi.org/10.1002/(sici)1097-0290(19991005)65:1%3c24:Aid-bit4%3e3.0.Co;2-2

    Article  CAS  PubMed  Google Scholar 

  77. Zhang N, Zhang L, Sun D (2015) Influence of Emulsification Process on the Properties of Pickering Emulsions Stabilized by Layered Double Hydroxide Particles. Langmuir 31:4619–4626. https://doi.org/10.1021/la505003w

    Article  CAS  PubMed  Google Scholar 

  78. Zhao C, Xie SX, Pu YQ, Zhang R, Huang F, Ragauskas AJ, Yuan JS (2016) Synergistic enzymatic and microbial lignin conversion. Green Chem 18:1306–1312. https://doi.org/10.1039/c5gc01955a

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funding for this research was provided by Iowa State University’s Bioeconomy Institute, and NSF Energy for Sustainability, award number CBET-1605034. This work was also authored in part by Alliance for Sustainable Energy, LLC, the manager and operator of the National Renewable Energy Laboratory for the U.S. Department of Energy (DOE) under Contract no. DE-AC36-08GO28308. Funding to DS and GTB was provided by the U.S. Department of Energy Office of Energy Efficiency and Renewable Energy Technologies Office.

Author information

Authors and Affiliations

  1. Chemical and Biological Engineering, 4134 Biorenewable Research Laboratory, Iowa State University, Ames, IA, 50011, USA

    Kirsten Davis & Laura R. Jarboe

  2. Bioeconomy Institute, Iowa State University, 1140 BRL Building, 617 Bissell Road, Ames, IA, 50011, USA

    Marjorie R. Rover, Ryan G. Smith & Robert C. Brown

  3. National Bioenergy Center, National Renewable Energy Laboratory, Golden, CO, 80401, USA

    Davinia Salvachúa & Gregg T. Beckham

  4. Department of Food Science and Human Nutrition, Iowa State University, Ames, IA, 50011, USA

    Zhiyou Wen

Authors
  1. Kirsten Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marjorie R. Rover
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Davinia Salvachúa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ryan G. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gregg T. Beckham
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhiyou Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Robert C. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Laura R. Jarboe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura R. Jarboe.

Ethics declarations

Conflict of interest

There are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 236 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Davis, K., Rover, M.R., Salvachúa, D. et al. Promoting microbial utilization of phenolic substrates from bio-oil. J Ind Microbiol Biotechnol 46, 1531–1545 (2019). https://doi.org/10.1007/s10295-019-02208-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10295-019-02208-z

Keywords

Search

Navigation