Modular and selective biosynthesis of gasoline-range alkanes

Metabolic Engineering

Volumn 33, Issue , 2016, Pages 28-40

  Sheppard, Micah J ^a,c   Kunjapur, Aditya M ^a,b   Prather, Kristala L J ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c Provivi   (United States)

Author keywords

Alkanes; Biofuel; E. coli; Gasoline; Metabolic engineering; Synthetic biology

Indexed keywords

ALDEHYDES; BIOCHEMISTRY; BIOFUELS; BUTANE; BYPRODUCTS; CARBON; CHAIN LENGTH; CHAINS; ENERGY EFFICIENCY; ESCHERICHIA COLI; FATTY ACIDS; HEPTANE; METABOLIC ENGINEERING; PARAFFINS; PROPANE; REACTION INTERMEDIATES; SYNTHESIS (CHEMICAL);

BROAD SPECIFICITIES; CARBON CHAIN EXTENSION; DIFFERENT MECHANISMS; E. COLI; ENGINEERED ESCHERICHIA COLI; FATTY ACID SYNTHESIS; PRODUCT DISTRIBUTIONS; SYNTHETIC BIOLOGY;

GASOLINE;

ACETYL COENZYME A ACETYLTRANSFERASE; ALDEHYDE REDUCTASE; ALKANE DERIVATIVE; CARBOXYLIC ACID; GASOLINE; THIOL ESTER HYDROLASE; ALKANE; ESCHERICHIA COLI PROTEIN; FATTY ACID; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BIOSYNTHESIS; CARBON SOURCE; CLOSTRIDIUM ACETOBUTYLICUM; CODON; CONTROLLED STUDY; CUPRIAVIDUS NECATOR; ESCHERICHIA COLI; FATTY ACID SYNTHESIS; GAS CHROMATOGRAPHY; GENE DELETION; GENETIC CODE; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; NOSTOC PUNCTIFORME; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDUCTION; WESTERN BLOTTING; GENETICS; ISOLATION AND PURIFICATION; METABOLIC ENGINEERING; METABOLISM; MICROBIOLOGY; PROCEDURES;

ALKANES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FATTY ACIDS, NONESTERIFIED; GASOLINE; METABOLIC ENGINEERING; RECOMBINANT PROTEINS;

EID: 84947714060     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2015.10.010     Document Type: Article

References (71)

1. International Energy Statistics, 2014. United States Energy Information Administration. Energy Information Administration, U.S. Department of Energy.
2. Akhtar M.K., Turner N.J., Jones P.R. Carboxylic acid reductase is a versatile enzyme for the conversion of fatty acids into fuels and chemical commodities. Proc. Natl. Acad. Sci. USA 2013, 110:87-92.
3. Anderson A.J., Dawes E.A. Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol. Rev. 1990, 54:450-472.
4. 2. Proc. Natl. Acad. Sci. USA 2013, 110:3191-3196.
5. Aukema K.G., Makris T.M., Stoian S.A., Richman J.E., Münck E., Lipscomb J.D., Wackett L.P. Cyanobacterial aldehyde deformylase oxygenation of aldehydes yields n-1 aldehydes and alcohols in addition to alkanes. ACS Catal. 2013, 3:2228-2238.
6. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol .Syst. Biol. 2006, 2(2006):0008.
7. Berríos-Rivera S.J., Bennett G.N., San K.-Y. Metabolic engineering of Escherichia coli: increase of NADH availability by overexpressing an NAD+-dependent formate dehydrogenase. Metab. Eng. 2002, 4:217-229.
8. Burgess, D.R. Thermochemical Data. NIST Chemistry WebBook, NIST Standard Reference Database Number 69. In: P.J. Linstrom and W.G. Mallard (Eds). National Institute of Standards and Technology, Gaithersburg, MD, 2009.
9. Byers D.M., Gong H. Acyl carrier protein: structure-function relationships in a conserved multifunctional protein family. Biochem. Cell Biol. 2007, 85:649-662.
10. Caspi R., Altman T., Billington R., Dreher K., Foerster H., Fulcher C.A., Holland T.A., Keseler I.M., Kothari A., Kubo A., Krummenacker M., Latendresse M., Mueller L.A., Ong Q., Paley S., Subhraveti P., Weaver D.S., Weerasinghe D., Zhang P., Karp P.D. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 2014, 42:D459-D471.
11. Chemler J.A., Fowler Z.L., McHugh K.P., Koffas M.A.G. Improving NADPH availability for natural product biosynthesis in Escherichia coli by metabolic engineering. Metab. Eng. 2010, 12:96-104.
12. Choi Y.J., Lee S.Y. Microbial production of short-chain alkanes. Nature 2013, 502:571.
13. Cline P.V., Delfino J.J., Rao P.S.C. Partitioning of aromatic constituents into water from gasoline and other complex solvent mixtures. Environ. Sci. Technol. 1991, 25:914-920.
14. Datsenko K.A., Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 2000, 97:6640-6645.
15. Davis M.S., Solbiati J., Cronan J.E. Overproduction of Acetyl-Coa carboxylase activity increases the rate of fatty acid biosynthesis in Escherichia coli. J. Biol. Chem. 2000, 275:28593-28598.
16. De Lay N.R., Cronan J.E. In vivo functional analyses of the type II acyl carrier proteins of fatty acid biosynthesis. J. Biol. Chem. 2007, 282:20319-20328.
17. Dehesh K., Jones A., Knutzon D.S., Voelker T.A. Production of high levels of 8:0 and 10:0 fatty acids in transgenic canola by overexpression of Ch FatB2, a thioesterase cDNA from Cuphea hookeriana. Plant J. 1996, 9:167-172.
18. Dekishima Y., Lan E.I., Shen C.R., Cho K.M., Liao J.C. Extending carbon chain length of 1-butanol pathway for 1-hexanol synthesis from glucose by engineered Escherichia coli. J. Am. Chem. Soc. 2013, 133:11399-11401.
19. Dellomonaco C., Clomburg J.M., Miller E.N., Gonzalez R. Engineered reversal of the β-oxidation cycle for the synthesis of fuels and chemicals. Nature 2011, 476:355-359.
20. Dugar D., Stephanopoulos G. Relative potential of biosynthetic pathways for biofuels and bio-based products. Nat. Biotechnol. 2011, 29:1074-1078.
21. Fichman, B. T., Repice, R., Adler, R., Berry, J., Michaels, J., Grape, S. G., Paduano, N., Bonnar, D., Namovicz, C. R., Barrick, J., Anderson, M., Sweeney, A., Young, P., Wirman, C., Mobilia, M., Bredehoeft, G., Lindstrom, P., Ko, N., 2012. Annual Energy Review 2011, United States Energy Information Administration Energy. U. S. D. o. (Ed.). United States Energy Information Administration, Washington, D.C.
22. Fortman J.L., Chhabra S., Mukhopadhyay A., Chou H., Lee T.S., Steen E., Keasling J.D. Biofuel alternatives to ethanol: pumping the microbial well. Trends Biotechnol. 2008, 26:375-381.
23. Gul-Karaguler N., Sessions R., Clarke A., Holbrook J.J. A single mutation in the NAD-specific formate dehydrogenase from Candida methylica allows the enzyme to use NADP. Biotechnol. Lett. 2001, 23:283-287.
24. Hall M., Stueckler C., Hauer B., Stuermer R., Friedrich T., Breuer M., Kroutil W., Faber K. Asymmetric bioreduction of activated C=C bonds using Zymomonas mobilis NCR enoate reductase and old yellow enzymes OYE 1-3 from yeasts. Eur. J. Org. Chem. 2008, 2008:1511-1516.
25. Handke P., Lynch S.A., Gill R.T. Application and engineering of fatty acid biosynthesis in Escherichia coli for advanced fuels and chemicals. Metab. Eng. 2011, 13:28-37.
26. Harger M., Zheng L., Moon A., Ager C., An J.H., Choe C., Lai Y.-L., Mo B., Zong D., Smith M.D., Egbert R.G., Mills J.H., Baker D., Pultz I.S., Siegel J.B. Expanding the Product profile of a microbial alkane biosynthetic pathway. ACS Synth. Biol. 2012, 2:59-62.
27. Heath R.J., Rock C.O. Enoyl-acyl carrier protein reductase (fabI) plays a determinant role in completing cycles of fatty acid elongation in Escherichia coli. J. Biol. Chem. 1995, 270:26538-26542.
28. Hoffmeister M., Piotrowski M., Nowitzki U., Martin W. Mitochondrial trans-2-Enoyl-CoA reductase of wax ester fermentation from Euglena gracilis defines a new family of enzymes involved in lipid synthesis. J. Biol. Chem. 2005, 280:4329-4338.
29. Howard T.P., Middelhaufe S., Moore K., Edner C., Kolak D.M., Taylor G.N., Parker D.A., Lee R., Smirnoff N., Aves S.J., Love J. Synthesis of customized petroleum-replica fuel molecules by targeted modification of free fatty acid pools in Escherichia coli. Proc. Natl. Acad. Sci. USA 2013, 110:7636-7641.
30. Inui M., Suda M., Kimura S., Yasuda K., Suzuki H., Toda H., Yamamoto S., Okino S., Suzuki N., Yukawa H. Expression of Clostridium acetobutylicum butanol synthetic genes in Escherichia coli. Appl. Microbiol. Biotechnol. 2008, 77:1305-1316.
31. Javidpour P., Pereira J.H., Goh E.-B., McAndrew R.P., Ma S.M., Friedland G.D., Keasling J.D., Chhabra S.R., Adams P.D., Beller H.R. Biochemical and structural studies of NADH-dependent FabG used to increase the bacterial production of fatty acids under anaerobic conditions. Appl. Environ. Microbiol. 2014, 80:497-505.
32. Jing F., Cantu D.C., Tvaruzkova J., Chipman J.P., Nikolau B.J., Yandeau-Nelson M.D., Reilly P.J. Phylogenetic and experimental characterization of an acyl-ACP thioesterase family reveals significant diversity in enzymatic specificity and activity. BMC Biochem. 2011, 12. 44-44.
33. Johansen N.G., Ettre L.S., Miller R.L. Quantitative analysis of hydrocarbons by structural group type in gasolines and distillates : I. gas chromatography. J. Chromatogr. A 1983, 256:393-417.
34. Jones A., Davies H.M., Voelker T.A. Palmitoyl-acyl carrier protein (ACP) thioesterase and the evolutionary origin of plant acyl-ACP thioesterases. Plant Cell 1995, 7:359-371.
35. Kallio P., Pásztor A., Thiel K., Akhtar M.K., Jones P.R. An engineered pathway for the biosynthesis of renewable propane. Nat. Commun. 2014, 5.
36. Kameda K., Nunn W.D. Purification and characterization of acyl coenzyme A synthetase from Escherichia coli. J. Biol. Chem. 1981, 256:5702-5707.
37. Khara B., Menon N., Levy C., Mansell D., Das D., Marsh E.N.G., Leys D., Scrutton N.S. Production of propane and other short-chain alkanes by structure-based engineering of ligand specificity in aldehyde-deformylating oxygenase. ChemBioChem 2013, 14:1204-1208.
38. Klock H.E., Lesley S.A. The polymerase incomplete primer extension (PIPE) method applied to high-throughput cloning and site-directed mutagenesis. High Throughput Protein Expression and Purification. 2009, vol. 498:91-103. Humana Press.
39. Koebmann B.J., Westerhoff H.V., Snoep J.L., Nilsson D., Jensen P.R. The glycolytic flux in Escherichia coli is controlled by the demand for ATP. J. Bacteriol. 2002, 184:3909-3916.
40. Kunau W.-H., Dommes V., Schulz H. β-oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog. Lipid Res. 1995, 34:267-342.
41. Kunjapur A.M., Prather K.L.J. Microbial engineering for aldehyde synthesis. Appl. Environ. Microbiol. 2015, 81:1892-1901.
42. Kunjapur A.M., Tarasova Y., Prather K.L.J. Synthesis and accumulation of aromatic aldehydes in an engineered strain of Escherichia coli. J. Am. Chem. Soc. 2014, 136:11644-11654.
43. Lennen R.M., Pfleger B.F. Engineering Escherichia coli to synthesize free fatty acids. Trends Biotechnol. 2012, 30:659-667.
44. Liu X., Sheng J., Curtiss R. Fatty acid production in genetically modified cyanobacteria. Proc. Natl. Acad. Sci. USA 2011, 108:6899-6904.
45. Lütke-Eversloh T., Bahl H. Metabolic engineering of Clostridium acetobutylicum: recent advances to improve butanol production. Curr. Opin. Biotechnol. 2011, 22:634-647.
46. Nielsen D.R., Leonard E., Yoon S.-H., Tseng H.-C., Yuan C., Prather K.L.J. Engineering alternative butanol production platforms in heterologous bacteria. Metab. Eng. 2009, 11:262-273.
47. Parikh S., Moynihan D.P., Xiao G., Tonge P.J. Roles of tyrosine 158 and lysine 165 in the catalytic mechanism of InhA, the Enoyl-ACP reductase from Mycobacterium tuberculosis. Biochemistry 1999, 38:13623-13634.
48. Peralta-Yahya P.P., Zhang F., del Cardayre S.B., Keasling J.D. Microbial engineering for the production of advanced biofuels. Nature 2012, 488:320-328.
49. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
50. Pick A., Rühmann B., Schmid J., Sieber V. Novel CAD-like enzymes from Escherichia coli K-12 as additional tools in chemical production. Appl. Microbiol. Biotechnol. 2013, 97(13):5815-5824.
51. Pieper U., Webb B.M., Barkan D.T., Schneidman-Duhovny D., Schlessinger A., Braberg H., Yang Z., Meng E.C., Pettersen E.F., Huang C.C., Datta R.S., Sampathkumar P., Madhusudhan M.S., Sjölander K., Ferrin T.E., Burley S.K., Sali A. ModBase, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res. 2011, 39:D465-D474.
52. Piškur J., Rozpedowska E., Polakova S., Merico A., Compagno C. How did Saccharomyces evolve to become a good brewer?. Trends Genet. 2006, 22:183-186.
53. Postma E., Verduyn C., Scheffers W.A., Van Dijken J.P. Enzymic analysis of the crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 1989, 55:468-477.
54. Ratledge C. Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie 2004, 86:807-815.
55. Richter N., Gröger H., Hummel W. Asymmetric reduction of activated alkenes using an enoate reductase from Gluconobacter oxydans. Appl. Microbiol. Biotechnol. 2011, 89:79-89.
56. Rodriguez G.M., Atsumi S. Toward aldehyde and alkane production by removing aldehyde reductase activity in Escherichia coli. Metab. Eng. 2014, 25:227-237.
57. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Sanders W.N., Maynard J.B. Capillary gas chromatographic method for determining the C3-C12 hydrocarbons in full-range motor gasolines. Anal. Chem. 1968, 40:527-535.
59. Schirmer A., Rude M.A., Li X., Popova E., del Cardayre S.B. Microbial biosynthesis of alkanes. Science 2010, 329:559-562.
60. Schulz H. Beta oxidation of fatty acids. Biochim. Biophys. Acta - Lipids Lipid Metab. 1991, 1081:109-120.
61. Schweizer E., Hofmann J. Microbial type I fatty acid synthases (FAS): major players in a network of cellular FAS systems. Microbiol. Mol. Biol. Rev. 2004, 68:501-517.
62. Seelbach K., Riebel B., Hummel W., Kula M.-R., Tishkov V.I., Egorov A.M., Wandrey C., Kragl U. A novel, efficient regenerating method of NADPH using a new formate dehydrogenase. Tetrahedron Lett. 1996, 37:1377-1380.
63. Sheppard M.J., Kunjapur A.M., Wenck S.J., Prather K.L.J. Retro-biosynthetic screening of a modular pathway design achieves selective route for microbial synthesis of 4-methyl-pentanol. Nat. Commun. 2014, 5:5031.
64. Slater S., Houmiel K.L., Tran M., Mitsky T.A., Taylor N.B., Padgette S.R., Gruys K.J. Multiple β-ketothiolases mediate poly(β-Hydroxyalkanoate) copolymer synthesis in Ralstonia eutropha. J. Bacteriol. 1998, 180:1979-1987.
65. Steinbüchel A., Lütke-Eversloh T. Metabolic engineering and pathway construction for biotechnological production of relevant polyhydroxyalkanoates in microorganisms. Biochem. Eng. J. 2003, 16:81-96.
66. Strogen B., Horvath A. Greenhouse Gas Emissions from the Construction, Manufacturing, Operation, and Maintenance of U.S Distribution Infrastructure for Petroleum and Biofuels. J. Infrastruct. Syst. 2013, 19:371-383.
67. Thomason, L. C., Costantino, N., Court, D. L., 2001. E. coli genome manipulation by P1 transduction current protocols in molecular biology. John Wiley & Sons, Inc.
68. Tseng H.-C., Harwell C., Martin C., Prather K. Biosynthesis of chiral 3-hydroxyvalerate from single propionate-unrelated carbon sources in metabolically engineered E. coli. Microb. Cell Factories 2010, 9:96.
69. Tseng H.-C., Prather K.L.J. Controlled biosynthesis of odd-chain fuels and chemicals via engineered modular metabolic pathways. Proc. Natl. Acad. Sci. USA 2012, 109:17925-17930.
70. Vemuri G.N., Altman E., Sangurdekar D.P., Khodursky A.B., Eiteman M.A. Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Appl. Environ. Microbiol. 2006, 72:3653-3661.
71. Wells J.E., Hylemon P.B. Identification and characterization of a bile acid 7α-dehydroxylation operon in Clostridium sp. strain TO-931, a highly active 7α-dehydroxylating strain isolated from human feces. Appl. Environ. Microbiol. 2000, 66:1107-1113.