Polysaccharide hydrolysis with engineered Escherichia coli for the production of biocommodities

Review

Abstract

Escherichia coli can ferment a broad range of sugars, including pentoses, hexoses, uronic acids, and polyols. These features make E. coli a suitable microorganism for the development of biocatalysts to be used in the production of biocommodities and biofuels by metabolic engineering. E. coli cannot directly ferment polysaccharides because it does not produce and secrete the necessary saccharolytic enzymes; however, there are many genetic tools that can be used to confer this ability on this prokaryote. The construction of saccharolytic E. coli strains will reduce costs and simplify the production process because the saccharification and fermentation can be conducted in a single reactor with a reduced concentration or absence of additional external saccharolytic enzymes. Recent advances in metabolic engineering, surface display, and excretion of hydrolytic enzymes provide a framework for developing E. coli strains for the so-called consolidated bioprocessing. This review presents the different strategies toward the development of E. coli strains that have the ability to display and secrete saccharolytic enzymes to hydrolyze different sugar-polymeric substrates and reduce the loading of saccharolytic enzymes.

Keywords

Escherichia coli Metabolic engineering Biocommodities Polysaccharides Saccharolytic enzymes secretion 

Notes

Acknowledgments

This work was supported by the Mexican Council of Science and Technology (CONACyT) technological innovation grants: 2010-13879, 2011-154298, and 2012-184417; and from the Universidad Nacional Autónoma de México: grant DGAPA/PAPIIT/UNAM IT200312. The authors wish to thank Drs. Guillermo Gosset and Ricardo Oropeza from the Instituto de Biotecnología and Jaime Ortega from CINVESTAV-IPN for many helpful discussions regarding the topic of this review.

References

  1. 1.
    Alvira P, Negro MJ, Ballesteros M (2011) Effect of endoxylanase and α-l-arabinofuranosidase supplementation on the enzymatic hydrolysis of steam exploded wheat straw. Bioresour Technol 102:4552–4558. doi: 10.1016/j.biortech.2010.12.112 PubMedCrossRefGoogle Scholar
  2. 2.
    Arantes V, Saddler JN (2010) Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis. Biotechnol Biofuels 3:4. doi: 10.1186/1754-6834-3-4 PubMedCrossRefGoogle Scholar
  3. 3.
    Ashiuchi M, Nawa C, Kamei T, Song JJ, Hong SP, Sung MH, Soda K, Yagi T, Misono H (2001) Physiological and biochemical characteristics of poly γ-glutamate synthetase complex of Bacillus subtilis. Eur J Biochem 268:5321–5328. doi: 10.1046/j.0014-2956.2001.02475.x PubMedCrossRefGoogle Scholar
  4. 4.
    Ashiuchi M, Soda K, Misono H (1999) A poly-γ-glutamate synthetic system of Bacillus subtilis IFO 3336: gene cloning and biochemical analysis of poly-γ-glutamate produced by Escherichia coli clone cells. Biochem Biophys Res Commun 263:6–12. doi: 10.1006/bbrc.1999.1298 PubMedCrossRefGoogle Scholar
  5. 5.
    Bae W, Mulchandani A, Chen W (2002) Cell surface display of synthetic phytochelatins using ice nucleation protein for enhanced heavy metal bioaccumulation. J Inorg Biochem 88:223–227. doi: 10.1016/S0162-0134(01)00392-0 PubMedCrossRefGoogle Scholar
  6. 6.
    Berlin A, Maximenko V, Gilkes N, Saddler J (2007) Optimization of enzyme complexes for lignocellulose hydrolysis. Biotechnol Bioeng 97:287–296. doi: 10.1002/bit.21238 PubMedCrossRefGoogle Scholar
  7. 7.
    Bio Arquitecture Lab. BAL breaks ground on experimental pilot facility. http://www.ba-lab.com/pdf/BALPilotFacility.pdf. Accessed 21 Jan 2013
  8. 8.
    Bokinsky G, Peralta-Yahya PP, George A, Holmes BM, Steen EJ, Dietrich J, Soon Lee T, Tullman-Ercek D, Voigt CA, Simmons BA, Keasling JD (2011) Synthesis of three advanced biofuels from ionic liquid-pretreated switchgrass using engineered Escherichia coli. Proc Natl Acad Sci USA 108:19949–19954. doi: 10.1073/pnas.1106958108 PubMedCrossRefGoogle Scholar
  9. 9.
    Campbell CJ, Laherrère JH (1998) The end of cheap oil. Sci Am 278:78–83CrossRefGoogle Scholar
  10. 10.
    Chandel AK, Chandrasekhar G, Silva MB, Silvério da Silva S (2012) The realm of cellulases in biorefinery development. Crit Rev Biotechnol 32:187–202. doi: 10.3109/07388551.2011.595385 PubMedCrossRefGoogle Scholar
  11. 11.
    Charbit A, Boulain JC, Ryter A, Hofnung M (1986) Probing the topology of a bacterial membrane protein by genetic insertion of a foreign epitope; expression at the cell surface. EMBO J 5:3029–3037PubMedGoogle Scholar
  12. 12.
    Charbit A, Sobczak E, Michel ML, Molla A, Tiollais P, Hofnung M (1987) Presentation of two epitopes of the preS2 region of hepatitis B virus on live recombinant bacteria. J Immunol 139:1658–1664PubMedGoogle Scholar
  13. 13.
    Chen X, Ishida N, Todaka N, Nakamura R, Maruyama J, Takahashi H, Kitamoto K (2010) Promotion of efficient saccharification of crystalline cellulose by Aspergillus fumigatus Swo1. Appl Environ Microbiol 76:2556–2561. doi: 10.1128/AEM.02499-09 PubMedCrossRefGoogle Scholar
  14. 14.
    Chen Y-P, Hwang I-E, Lin C-J, Wang H-J, Tseng C-P (2012) Enhancing the stability of xylanase from Cellulomonas fimi by cell-surface display on Escherichia coli. J Appl Microbiol 112:455–463. doi: 10.1111/j.1365-2672.2012.05232.x PubMedCrossRefGoogle Scholar
  15. 15.
    Chen Y, Stevens MA, Zhu Y, Holmes J, Moxley G, Xu H (2012) Reducing acid in dilute acid pretreatment and the impact on enzymatic saccharification. J Ind Microbiol Biotechnol 39:691–700. doi: 10.1007/s10295-011-1068-7 PubMedCrossRefGoogle Scholar
  16. 16.
    Clomburg JM, Gonzalez R (2010) Biofuel production in Escherichia coli: the role of metabolic engineering and synthetic biology. Appl Microbiol Biotechnol 86:419–434. doi: 10.1007/s00253-010-2446-1 PubMedCrossRefGoogle Scholar
  17. 17.
    Dautin N, Bernstein HD (2007) Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61:89–112. doi: 10.1146/annurev.micro.61.080706.093233 PubMedCrossRefGoogle Scholar
  18. 18.
    Dellomonaco C, Clomburg JM, Miller EN, Gonzalez R (2011) Engineered reversal of the β-oxidation cycle for the synthesis of fuels and chemicals. Nature 476:355–359. doi: 10.1038/nature10333 PubMedCrossRefGoogle Scholar
  19. 19.
    Du J, Shao Z, Zhao H (2011) Engineering microbial factories for synthesis of value-added products. J Ind Microbiol Biotechnol 38:873–890. doi: 10.1007/s10295-011-0970-3 PubMedCrossRefGoogle Scholar
  20. 20.
    Edwards MC, Doran-Peterson J (2012) Pectin-rich biomass as feedstock for fuel ethanol production. Appl Microbiol Biotechnol 95:565–575. doi: 10.1007/s00253-012-4173-2 PubMedCrossRefGoogle Scholar
  21. 21.
    Edwards MC, Henriksen ED, Yomano LP, Gardner BC, Sharma LN, Ingram LO, Peterson JD (2011) Addition of genes for cellobiase and pectinolytic activity in Escherichia coli for fuel ethanol production from pectin-rich lignocellulosic biomass. Appl Environ Microbiol 77:5184–5191. doi: 10.1128/AEM.05700-11 PubMedCrossRefGoogle Scholar
  22. 22.
    Fernández-Sandoval MT, Huerta-Beristain G, Trujillo-Martinez B, Bustos P, González V, Bolivar F, Gosset G, Martinez A (2012) Laboratory metabolic evolution improves acetate tolerance and growth on acetate of ethanologenic Escherichia coli under non-aerated conditions in glucose-mineral medium. Appl Microbiol Biotechnol 96:1291–1300. doi: 10.1007/s00253-012-4177-y PubMedCrossRefGoogle Scholar
  23. 23.
    Francisco JA, Earhart CF, Georgiou G (1992) Transport and anchoring of β-lactamase to the external surface of Escherichia coli. Proc Natl Acad Sci U S A 89:2713–2717PubMedCrossRefGoogle Scholar
  24. 24.
    Francisco J, Stathopoulos C, Warren R, Kilburn D, Georgiou G (1993) Specific adhesion and hydrolysis of cellulose by intact Escherichia coli expressing surface anchored cellulase or cellulose binding domains. Bio Technol 11:491–495. doi: 10.1038/nbt0493-491 CrossRefGoogle Scholar
  25. 25.
    Freudl R, MacIntyre S, Degen M, Henning U (1986) Cell surface exposure of the outer membrane protein OmpA of Escherichia coli K-12. J Mol Biol 188:491–494PubMedCrossRefGoogle Scholar
  26. 26.
    Fu C, Mielenz JR, Xiao X, Ge Y, Hamilton CY, Rodriguez M, Chen F, Foston M, Ragauskas A, Bouton J, Dixon RA, Wang Z-Y (2011) Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proc Natl Acad Sci U S A 108:3803–3808. doi: 10.1073/pnas.1100310108 PubMedCrossRefGoogle Scholar
  27. 27.
    Gao D, Uppugundla N, Chundawat SP, Yu X, Hermanson S, Gowda K, Brumm P, Mead D, Balan V, Dale BE (2011) Hemicellulases and auxiliary enzymes for improved conversion of lignocellulosic biomass to monosaccharides. Biotechnol Biofuels 4:5. doi: 10.1186/1754-6834-4-5 PubMedCrossRefGoogle Scholar
  28. 28.
    Garza E, Zhao J, Wang Y, Wang J, Iverson A, Manow R, Finan C, Zhou S (2012) Engineering a homobutanol fermentation pathway in Escherichia coli EG03. J Ind Microbiol Biotechnol 39:1101–1107. doi: 10.1007/s10295-012-1151-8 PubMedCrossRefGoogle Scholar
  29. 29.
    Geddes CC, Mullinnix MT, Nieves IU, Peterson JJ, Hoffman RW, York SW, Yomano LP, Miller EN, Shanmugam KT, Ingram LO (2011) Simplified process for ethanol production from sugarcane bagasse using hydrolysate-resistant Escherichia coli strain MM160. Bioresour Technol 102:2702–2711. doi: 10.1016/j.biortech.2010.10.143 PubMedCrossRefGoogle Scholar
  30. 30.
    Geddes CC, Nieves IU, Ingram LO (2011) Advances in ethanol production. Curr Opin Biotechnol 22:312–319. doi: 10.1016/j.copbio.2011.04.012 PubMedCrossRefGoogle Scholar
  31. 31.
    Hahn-Hägerdal B, Galbe M, Gorwa-Grauslund MF, Lidén G, Zacchi G (2006) Bio-ethanol: the fuel of tomorrow from the residues of today. Trends Biotechnol 24:549–556. doi: 10.1016/j.tibtech.2006.10.004 PubMedCrossRefGoogle Scholar
  32. 32.
    He SY, Lindeberg M, Chatterjee AK, Collmer A (1991) Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins to its milieu. Proc Natl Acad Sci USA 88:1079–1083PubMedCrossRefGoogle Scholar
  33. 33.
    Henderson IR, Owen P (1999) The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and oxyR. J Bacteriol 181:2132–2141PubMedGoogle Scholar
  34. 34.
    Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala’Aldeen D (2004) Type V protein secretion pathway: the auto transporter story. Microbiol Mol Biol Rev 68:692–744. doi: 10.1128/MMBR.68.4.692-744.2004 PubMedCrossRefGoogle Scholar
  35. 35.
    Hogsett D, Ahn H, Bernardez T, South C, Lynd L (1992) Direct microbial conversion. Appl Biochem Biotechnol 34(35):527–541. doi: 10.1007/BF02920576 CrossRefGoogle Scholar
  36. 36.
    Horn SJ, Aasen IM, Ostgaard K (2000) Ethanol production from seaweed extract. J Ind Microbiol Biotechnol 25:249–254. doi: 10.1038/sj.jim.7000065 CrossRefGoogle Scholar
  37. 37.
    Huerta-Beristain G, Utrilla J, Hernández-Chávez G, Bolívar F, Gosset G, Martinez A (2008) Specific ethanol production rate in ethanologenic Escherichia coli strain KO11 is limited by pyruvate decarboxylase. J Mol Microbiol Biotechnol 15:55–64. doi: 10.1159/000111993 PubMedCrossRefGoogle Scholar
  38. 38.
    IEA (2007) CO2 Emissions from Fuel Combustion 1971-2005. ParisGoogle Scholar
  39. 39.
    Jarboe LR, Grabar TB, Yomano LP, Shanmugan KT, Ingram LO (2007) Development of ethanologenic bacteria. Adv Biochem Eng Biotechnol 108:237–261. doi: 10.1007/10_2007_068 PubMedGoogle Scholar
  40. 40.
    John RP, Anisha GS, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102:186–193. doi: 10.1016/j.biortech.2010.06.139 PubMedCrossRefGoogle Scholar
  41. 41.
    Jose J, Maas RM, Teese MG (2012) Autodisplay of enzymes-molecular basis and perspectives. J Biotechnol 161:92–103. doi: 10.1016/j.jbiotec.2012.04.001 PubMedCrossRefGoogle Scholar
  42. 42.
    Jose J, Meyer TF (2007) The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol Mol Biol Rev 71:600–619. doi: 10.1128/MMBR.00011-07 PubMedCrossRefGoogle Scholar
  43. 43.
    Jung HC, Park JH, Park SH, Lebeault JM, Pan JG (1998) Expression of carboxymethylcellulase on the surface of Escherichia coli using Pseudomonas syringae ice nucleation protein. Enzyme Microb Technol 22:348–354. doi: 10.1016/S0141-0229(97)00224-X PubMedCrossRefGoogle Scholar
  44. 44.
    Jäger G, Girfoglio M, Dollo F, Rinaldi R, Bongard H, Commandeur U, Fischer R, Spiess AC, Büchs J (2011) How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuels 4:33. doi: 10.1186/1754-6834-4-33 PubMedCrossRefGoogle Scholar
  45. 45.
    Kang SW, Park YS, Lee JS, Hong SI, Kim SW (2004) Production of cellulases and hemicellulases by Aspergillus niger KK2 from lignocellulosic biomass. Bioresour Technol 91:153–156. doi: 10.1016/S0960-8524(03)00172-X PubMedCrossRefGoogle Scholar
  46. 46.
    Kawahara H (2002) The structures and functions of ice crystal-controlling proteins from bacteria. J Biosci Bioeng 94:492–496. doi: 10.1016/S1389-1723(02)80185-2 PubMedGoogle Scholar
  47. 47.
    Kim NJ, Li H, Jung K, Chang HN, Lee PC (2011) Ethanol production from marine algal hydrolysates using Escherichia coli KO11. Bioresour Technol 102:7466–7469. doi: 10.1016/j.biortech.2011.04.071 PubMedCrossRefGoogle Scholar
  48. 48.
    Kim YS, Jung HC, Pan JG (2000) Bacterial cell surface display of an enzyme library for selective screening of improved cellulase variants. Appl Environ Microbiol 66:788–793PubMedCrossRefGoogle Scholar
  49. 49.
    Klauser T, Pohlner J, Meyer TF (1992) Selective extracellular release of cholera toxin B subunit by Escherichia coli: dissection of Neisseria Iga beta-mediated outer membrane transport. EMBO J 11:2327–2335PubMedGoogle Scholar
  50. 50.
    Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253. doi: 10.1046/j.1365-2958.2000.01983.x PubMedCrossRefGoogle Scholar
  51. 51.
    Korotkov KV, Sandkvist M, Hol WGJ (2012) The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol 10:336–351. doi: 10.1038/nrmicro2762 PubMedGoogle Scholar
  52. 52.
    Kumar R, Singh S, Singh OV (2008) Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J Ind Microbiol Biotechnol 35:377–391. doi: 10.1007/s10295-008-0327-8 PubMedCrossRefGoogle Scholar
  53. 53.
    Lahaye M, Robic A (2007) Structure and functional properties of ulva, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774. doi: 10.1021/bm061185q PubMedCrossRefGoogle Scholar
  54. 54.
    Lee JS, Shin KS, Pan JG, Kim CJ (2000) Surface-displayed viral antigens on Salmonella carrier vaccine. Nat Biotechnol 18:645–648. doi: 10.1038/76494 PubMedCrossRefGoogle Scholar
  55. 55.
    Li H, Foston MB, Kumar R, Samuel R, Gao X, Hu F, Ragauskas AJ, Wyman CE (2012) Chemical composition and characterization of cellulose for Agave as a fast-growing, drought-tolerant biofuels feedstock. RSC Adv 2:4951–4958. doi: 10.1039/c2ra20557b CrossRefGoogle Scholar
  56. 56.
    Liu W, Zhang X-Z, Zhang Z, Zhang Y-HP (2010) Engineering of Clostridium phytofermentans endoglucanase Cel5A for improved thermostability. Appl Environ Microbiol 76:4914–4917. doi: 10.1128/AEM.00958-10 PubMedCrossRefGoogle Scholar
  57. 57.
    Lynd LR (1996) Overview an evaluation of fuel ethanol from cellulosic biomass: technology, economics, the environment, and policy. Annu Rev Energy Environ 21:403–465. doi: 10.1146/annurev.energy.21.1.403 CrossRefGoogle Scholar
  58. 58.
    Martinez A, Grabar TB, Shanmugam KT, Yomano LP, York SW, Ingram LO (2007) Low salt medium for lactate and ethanol production by recombinant Escherichia coli B. Biotechnol Lett 29:397–404. doi: 10.1007/s10529-006-9252-y PubMedCrossRefGoogle Scholar
  59. 59.
    Mills TY, Sandoval NR, Gill RT (2009) Cellulosic hydrolysate toxicity and tolerance mechanisms in Escherichia coli. Biotechnol Biofuels 2:26. doi: 10.1186/1754-6834-2-26 PubMedCrossRefGoogle Scholar
  60. 60.
    Mittal A, Katahira R, Himmel ME, Johnson DK (2011) Effects of alkaline or liquid-ammonia treatment on crystalline cellulose: changes in crystalline structure and effects on enzymatic digestibility. Biotechnol Biofuels 4:41. doi: 10.1186/1754-6834-4-41 PubMedCrossRefGoogle Scholar
  61. 61.
    Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96:673–686. doi: 10.1016/j.biortech.2004.06.025 PubMedCrossRefGoogle Scholar
  62. 62.
    Murphy DJ, Hall CAS (2011) Energy return on investment, peak oil, and the end of economic growth. Ann N Y Acad Sci 1219:52–72. doi: 10.1111/j.1749-6632.2010.05940.x PubMedCrossRefGoogle Scholar
  63. 63.
    Murray J, King D (2012) Climate policy: oil’s tipping point has passed. Nature 481:433–435. doi: 10.1038/481433a PubMedCrossRefGoogle Scholar
  64. 64.
    Muñoz-Gutiérrez I, Oropeza R, Gosset G, Martinez A (2012) Cell surface display of a β-glucosidase employing the type V secretion system on ethanologenic Escherichia coli for the fermentation of cellobiose to ethanol. J Ind Microbiol Biotechnol 39:1141–1152. doi: 10.1007/s10295-012-1122-0 PubMedCrossRefGoogle Scholar
  65. 65.
    Narita J, Okano K, Tateno T, Tanino T, Sewaki T, Sung M-H, Fukuda H, Kondo A (2006) Display of active enzymes on the cell surface of Escherichia coli using PgsA anchor protein and their application to bioconversion. Appl Microbiol Biotechnol 70:564–572. doi: 10.1007/s00253-005-0111-x PubMedCrossRefGoogle Scholar
  66. 66.
    Nhan NT, Gonzalez de Valdivia E, Gustavsson M, Hai TN, Larsson G (2011) Surface display of Salmonella epitopes in Escherichia coli and Staphylococcus carnosus. Microb Cell Fact 10:22. doi: 10.1186/1475-2859-10-22 PubMedCrossRefGoogle Scholar
  67. 67.
    Nobe R, Sakakibara Y, Fukuda N, Yoshida N, Ogawa K, Suiko M (2003) Purification and characterization of laminaran hydrolases from Trichoderma viride. Biosci Biotechnol Biochem 67:1349–1357. doi: 10.1271/bbb.67.1349 PubMedCrossRefGoogle Scholar
  68. 68.
    Olson DG, McBride JE, Shaw AJ, Lynd LR (2012) Recent progress in consolidated bioprocessing. Curr Opin Biotechnol 23:396–405. doi: 10.1016/j.copbio.2011.11.026 PubMedCrossRefGoogle Scholar
  69. 69.
    Orencio-Trejo M, Utrilla J, Fernández-Sandoval MT, Huerta-Beristain G, Gosset G, Martinez A (2010) Engineering the Escherichia coli fermentative metabolism. Adv Biochem Eng Biotechnol 121:71–107. doi: 10.1007/10_2009_61 PubMedGoogle Scholar
  70. 70.
    Orencio-Trejo M, Flores N, Escalante A, Hernández-Chávez G, Bolívar F, Gosset G, Martinez A (2008) Metabolic regulation analysis of an ethanologenic Escherichia coli strain based on RT-PCR and enzymatic activities. Biotechnol Biofuels 1:8. doi: 10.1186/1754-6834-1-8 PubMedCrossRefGoogle Scholar
  71. 71.
    Orser C, Staskawicz BJ, Panopoulos NJ, Dahlbeck D, Lindow SE (1985) Cloning and expression of bacterial ice nucleation genes in Escherichia coli. J Bacteriol 164:359–366PubMedGoogle Scholar
  72. 72.
    Owen NA, Inderwildi OR, King DA (2010) The status of conventional world oil reserves—Hype or cause for concern? Energy Policy 38:4743–4749. doi: 10.1016/j.enpol.2010.02.026 CrossRefGoogle Scholar
  73. 73.
    Park J, Rodríguez-Moyá M, Li M, Pichersky E, San K-Y, Gonzalez R (2012) Synthesis of methyl ketones by metabolically engineered Escherichia coli. J Ind Microbiol Biotechnol 39:1703–1712. doi: 10.1007/s10295-012-1178-x PubMedCrossRefGoogle Scholar
  74. 74.
    Percival E (1979) The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. Br Phycol J 14:103–117. doi: 10.1080/00071617900650121 CrossRefGoogle Scholar
  75. 75.
    Peterson R, Nevalainen H (2012) Trichoderma reesei RUT-C30: thirty years of strain improvement. Microbiology 158:58–68. doi: 10.1099/mic.0.054031-0 PubMedCrossRefGoogle Scholar
  76. 76.
    Pohlner J, Halter R, Beyreuther K, Meyer TF (1987) Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458–462. doi: 10.1038/325458a0 PubMedCrossRefGoogle Scholar
  77. 77.
    Qian Z-G, Xia X-X, Choi JH, Lee SY (2008) Proteome-based identification of fusion partner for high-level extracellular production of recombinant proteins in Escherichia coli. Biotechnol Bioeng 101:587–601. doi: 10.1002/bit.21898 PubMedCrossRefGoogle Scholar
  78. 78.
    Rubin EM (2008) Genomics of cellulosic biofuels. Nature 454:841–845. doi: 10.1038/nature07190 PubMedCrossRefGoogle Scholar
  79. 79.
    Ryu S, Karim MN (2011) A whole cell biocatalyst for cellulosic ethanol production from dilute acid-pretreated corn stover hydrolyzates. Appl Microbiol Biotechnol 91:529–542. doi: 10.1007/s00253-011-3261-z PubMedCrossRefGoogle Scholar
  80. 80.
    Shin H-D, Chen RR (2008) Extracellular recombinant protein production from an Escherichia coli lpp deletion mutant. Biotechnol Bioeng 101:1288–1296. doi: 10.1002/bit.22013 PubMedCrossRefGoogle Scholar
  81. 81.
    Soma Y, Inokuma K, Tanaka T, Ogino C, Kondo A, Okamoto M, Hanai T (2012) Direct isopropanol production from cellobiose by engineered Escherichia coli using a synthetic pathway and a cell surface display system. J Biosci Bioeng 114:80–85. doi: 10.1016/j.jbiosc.2012.02.019 PubMedCrossRefGoogle Scholar
  82. 82.
    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 463:559–562. doi: 10.1038/nature08721 PubMedCrossRefGoogle Scholar
  83. 83.
    Tanaka T, Kawabata H, Ogino C, Kondo A (2011) Creation of a cello oligosaccharide-assimilating Escherichia coli strain by displaying active beta-glucosidase on the cell surface via a novel anchor protein. Appl Environ Microbiol 77:6265–6270. doi: 10.1128/AEM.00459-11 PubMedCrossRefGoogle Scholar
  84. 84.
    Utrilla J, Gosset G, Martinez A (2009) ATP limitation in a pyruvate formate lyase mutant of Escherichia coli MG1655 increases glycolytic flux to d-lactate. J Ind Microbiol Biotechnol 36:1057–1062. doi: 10.1007/s10295-009-0589-9 PubMedCrossRefGoogle Scholar
  85. 85.
    Utrilla J, Licona-Cassani C, Marcellin E, Gosset G, Nielsen LK, Martinez A (2012) Engineering and adaptive evolution of Escherichia coli for d-lactate fermentation reveals GatC as a xylose transporter. Metab Eng 14:469–476. doi: 10.1016/j.ymben.2012.07.007 PubMedCrossRefGoogle Scholar
  86. 86.
    van Bloois E, Winter RT, Kolmar H, Fraaije MW (2011) Decorating microbes: surface display of proteins on Escherichia coli. Trends Biotechnol 29:79–86. doi: 10.1016/j.tibtech.2010.11.003 PubMedCrossRefGoogle Scholar
  87. 87.
    van der Woude MW, Henderson IR (2008) Regulation and function of Ag43 (Flu). Annu Rev Microbiol 62:153–169. doi: 10.1146/annurev.micro.62.081307.162938 PubMedCrossRefGoogle Scholar
  88. 88.
    Veldhuis MK, Christensen LM, Fulmer EI (1936) Production of ethanol: by thermophilic fermentation of cellulose. Ind Eng Chem 28:430–433. doi: 10.1021/ie50316a015 CrossRefGoogle Scholar
  89. 89.
    Wang X, Liu X, Wang G (2011) Two-stage hydrolysis of invasive algal feedstock for ethanol fermentation. J Integr Plant Biol 53:246–252. doi: 10.1111/j.1744-7909.2010.01024.x PubMedCrossRefGoogle Scholar
  90. 90.
    Wargacki AJ, Leonard E, Win MN, Regitsky DD, Santos CNS, Kim PB, Cooper SR, Raisner RM, Herman A, Sivitz AB, Lakshmanaswamy A, Kashiyama Y, Baker D, Yoshikuni Y (2012) An engineered microbial platform for direct biofuel production from brown macroalgae. Science 335:308–313. doi: 10.1126/science.1214547 PubMedCrossRefGoogle Scholar
  91. 91.
    Xiong H, von Weymarn N, Turunen O, Leisola M, Pastinen O (2005) Xylanase production by Trichoderma reesei Rut C-30 grown on l-arabinose-rich plant hydrolysates. Bioresour Technol 96:753–759. doi: 10.1016/j.biortech.2004.08.007 PubMedCrossRefGoogle Scholar
  92. 92.
    Yang C, Freudl R, Qiao C, Mulchandani A (2010) Cotranslocation of methyl parathion hydrolase to the periplasm and of organophosphorus hydrolase to the cell surface of Escherichia coli by the Tat pathway and ice nucleation protein display system. Appl Environ Microbiol 76:434–440. doi: 10.1128/AEM.02162-09 PubMedCrossRefGoogle Scholar
  93. 93.
    Zhang G, Brokx S, Weiner JH (2006) Extracellular accumulation of recombinant proteins fused to the carrier protein YebF in Escherichia coli. Nat Biotechnol 24:100–104. doi: 10.1038/nbt1174 PubMedCrossRefGoogle Scholar
  94. 94.
    Zhang Y-HP (2008) Reviving the carbohydrate economy via multi-product lignocellulose biorefineries. J Ind Microbiol Biotechnol 35:367–375. doi: 10.1007/s10295-007-0293-6 PubMedCrossRefGoogle Scholar
  95. 95.
    Zheng Z, Chen T, Zhao M, Wang Z, Zhao X (2012) Engineering Escherichia coli for succinate production from hemicellulose via consolidated bioprocessing. Microb Cell Fact 11:37. doi: 10.1186/1475-2859-11-37 PubMedCrossRefGoogle Scholar
  96. 96.
    Zhou S, Yomano LP, Saleh AZ, Davis FC, Aldrich HC, Ingram LO (1999) Enhancement of expression and apparent secretion of Erwinia chrysanthemi endoglucanase (encoded by celZ) in Escherichia coli B. Appl Environ Microbiol 65:2439–2445PubMedGoogle Scholar

Copyright information

© Society for Industrial Microbiology and Biotechnology 2013

Authors and Affiliations

  1. 1.Departamento de Ingeniería Celular y Biocatálisis, Instituto de BiotecnologíaUniversidad Nacional Autónoma de MéxicoCuernavacaMexico

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