Expression of the sub-pathways of the Chloroflexus aurantiacus 3-hydroxypropionate carbon fixation bicycle in E. coli: Toward horizontal transfer of autotrophic growth

Metabolic Engineering

Volumn 16, Issue 1, 2013, Pages 130-139

  Mattozzi, Matthew d ^a,b   Ziesack, Marika ^a,b,c   Voges, Mathias J ^a,b,d   Silver, Pamela A ^a,b   Way, Jeffrey C ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

3 hydroxypropionate; Carbon fixation; Chloroflexus aurantiacus; Diaminopimelic acid; E. coli; Metabolic engineering; Propionate biosensor; Propionate toxicity

Indexed keywords

3-HYDROXYPROPIONATE; CARBON FIXATION; CHLOROFLEXUS AURANTIACUS; DIAMINOPIMELIC ACIDS; E. COLI;

BIOLOGY; BIOSENSORS; CARBON DIOXIDE; ENZYMES; ESCHERICHIA COLI; GENE TRANSFER; METABOLIC ENGINEERING; TOXICITY; VOLATILE FATTY ACIDS;

BICYCLES;

ACETYL COENZYME A; CARBON DIOXIDE; HYDRACRYLIC ACID;

ARTICLE; AUTOTROPHY; AUXOTROPHY; BIOSENSOR; CARBON DIOXIDE FIXATION; CELL GROWTH; CHLOROFLEXUS; CHLOROFLEXUS AURANTIACUS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; NONHUMAN; OPERON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BACTERIAL PROTEINS; CHLOROFLEXUS; ENZYMES; ESCHERICHIA COLI K12; GENE EXPRESSION; LACTIC ACID; RECOMBINANT PROTEINS;

EID: 84874798401     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2013.01.005     Document Type: Article

References (67)

1. 2 fixation. J. Biol. Chem. 2002, 277:12137-12143.
2. Anderson J.C., Dueber J.E., Leguia M., Wu G.C., Goler J.A., Arkin A.P., Keasling J.D. BglBricks: a flexible standard for biological part assembly. J. Biol. Eng. 2010, 4:1.
3. Andreessen B., Steinbüchel A. Biosynthesis and biodegradation of 3-hydroxypropionate-containing polyesters. Appl. Environ. Microbiol. 2010, 76:4919-4925.
4. 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.
5. Bar-Even A., Noor E., Milo R. A survey of carbon fixation pathways through a quantitative lens. J. Exp. Bot. 2011, 63:2325-2342.
6. 2 in plant photosynthesis. Comp. Biochem. Physiol. 1962, 4:187-204.
7. Berg I.A., Kockelkorn D., Buckel W., Fuchs G. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 2007, 318:1782-1786.
8. Boghigian B.A., Zhang H., Pfeifer B.A. Multi-factorial engineering of heterologous polyketide production in Escherichia coli reveals complex pathway interactions. Biotechnol. Bioeng. 2011, 108:1360-1371.
9. Boyle N.R., Morgan J.A. Computation of metabolic fluxes and efficiencies for biological carbon dioxide fixation. Metab. Eng. 2011, 13:150-158.
10. Brock M., Maerker C., Schütz A., Völker U., Buckel W. Oxidation of propionate to pyruvate in Escherichia coli. Eur. J. Biochem. 2002, 269:6184-6194.
11. Buchanan B.B., Arnon D.I. A reverse KREBS cycle in photosynthesis: consensus at last. Photosynth. Res. 1990, 24:47-53.
12. Chuakrut S., Arai H., Ishii M., Igarashi Y. Characterization of a bifunctional archaeal acyl coenzyme A carboxylase. J. Bacteriol. 2003, 185:938-947.
13. Court D.L., Sawitzke J.A., Thomason L.C. Genetic engineering using homologous recombination. Annu. Rev. Genet. 2002, 36:361-388.
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. U.S.A. 2000, 97:6640-6645.
15. Dunlop M.J. Engineering microbes for tolerance to next-generation biofuels. Biotechnol. Biofuels 2011, 4:32.
16. Evans C.T., Sumegi B., Srere P.A., Sherry A.D., Malloy C.R. [13C]propionate oxidation in wild-type and citrate synthase mutant Escherichia coli: evidence for multiple pathways of propionate utilization. Biochem. J. 1993, 291(3):927-932.
17. Foster M.A., Tejerina G., Guest J.R., Woods D.D. Two enzymic mechanisms for the methylation of homocysteine by extracts of Escherichia coli. Biochem. J. 1964, 92:476-488.
18. Friedmann S., Alber B.E., Fuchs G. Properties of R-citramalyl-coenzyme A lyase and its role in the autotrophic 3-hydroxypropionate cycle of Chloroflexus aurantiacus. J. Bacteriol. 2007, 189:2906-2914.
19. Friedmann S., Steindorf A., Alber B.E., Fuchs G. Properties of succinyl-coenzyme A:L-malate coenzyme A transferase and its role in the autotrophic 3-hydroxypropionate cycle of Chloroflexus aurantiacus. J. Bacteriol. 2006, 188:2646-2655.
20. Froese D.S., Dobson C.M., White A.P., Wu X., Padovani D., Banerjee R., Haller T., Gerlt J.A., Surette M.G., Gravel R.A. Sleeping beauty mutase (sbm) is expressed and interacts with ygfd in Escherichia coli. Microbiol. Res. 2009, 164:1-8.
21. Fukui T., Suzuki M., Tsuge T., Nakamura S. Microbial synthesis of poly((R)-3-hydroxybutyrate-co-3-hydroxypropionate) from unrelated carbon sources by engineered Cupriavidus necator. Biomacromolecules 2009, 10:700-706.
22. Gibson D.G. Enzymatic assembly of overlapping DNA fragments. Methods Enzymol. 2011, 498:349-361.
23. Guest J.R., Friedman S., Foster M.A., Tejerina G., Woods D.D. Transfer of the methyl group from N5-methyltetrahydrofolates to homocysteine in Escherichia coli. Biochem. J. 1964, 92:497-504.
24. Haddock B.A., Schairer H.U. Electron-transport chains of Escherichia coli. Reconstitution of respiration in a 5-aminolaevulinic acid-requiring mutant. Eur. J. Biochem. FEBS 1973, 35:34-45.
25. Haller T., Buckel T., Rétey J., Gerlt J.A. Discovering new enzymes and metabolic pathways: conversion of succinate to propionate by Escherichia coli. Biochemistry 2000, 39:4622-4629.
26. +-dependent formate dehydrogenase from Burkholderia stabilis 15516: screening, purification and characterization. Enzyme Microb. Technol. 2010, 46:557-561.
27. 2 fixation. J. Bacteriol. 2002, 184:5999-6006.
28. 2 fixation pathway in Chloroflexus aurantiacus. J. Biol. Chem. 2002, 277:20277-20283.
29. 2 fixation by Chloroflexus aurantiacus. Arch. Microbiol. 1986, 148:292-297.
30. Horswill A.R., Dudding A.R., Escalante-Semerena J.C. Studies of propionate toxicity in Salmonella enterica identify 2-methylcitrate as a potent inhibitor of cell growth. J. Biol. Chem. 2001, 276:19094-19101.
31. Huber H., Gallenberger M., Jahn U., Eylert E., Berg I.A., Kockelkorn D., Eisenreich W., Fuchs G. A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:7851-7856.
32. 2 fixation. J. Bacteriol. 2002, 184:2404-2410.
33. Hügler M., Krieger R.S., Jahn M., Fuchs G. Characterization of acetyl-CoA/propionyl-CoA carboxylase in Metallosphaera sedula: carboxylating enzyme in the 3-hydroxypropionate cycle for autotrophic carbon fixation. Eur. J. Biochem. 2003, 270:736-744.
34. Ishii M., Chuakrut S., Arai H., Igarashi Y. Occurrence, biochemistry and possible biotechnological application of the 3-hydroxypropionate cycle. Appl. Microbiol. Biotechnol. 2004, 64:605-610.
35. Keasling J.D. Manufacturing molecules through metabolic engineering. Science 2010, 330:1355-1358.
36. Lamzin V.S., Aleshin A.E., Strokopytov B.V., Yukhnevich M.G., Popov V.O., Harutyunyan E.H., Wilson K.S. Crystal structure of NAD-dependent formate dehydrogenase. Eur. J. Biochem. 1992, 206:441-452.
37. Lee S.K., Keasling J.D. A propionate-inducible expression system for enteric bacteria. Appl. Environ. Microbiol. 2005, 71:6856-6862.
38. Lee S.K., Keasling J.D. A Salmonella-based, propionate-inducible, expression system for Salmonella enterica. Gene 2006, 377:6-11.
39. Lee S.K., Keasling J.D. Propionate-regulated high-yield protein production in Escherichia coli. Biotechnol. Bioeng. 2006, 93:912-918.
40. Lee S.K., Keasling J.D. Heterologous protein production in Escherichia coli using the propionate-inducible pPro system by conventional and auto-induction methods. Protein Expression Purif. 2008, 61:197-203.
41. 2. I. Co-methylcobyric acid and CO-(methyl)-5-methoxybenzimidazolylcobamide as intermediates with Clostridium thermoaceticum. Biochemistry 1965, 4:2771-2780.
42. Man W.-J., Li Y., Connor C.D., Wilton D.C. Biochim. Biophys. Acta 1995, 1250:69-75.
43. Marx C.J., Lidstrom M.E. Development of improved versatile broad-host-range vectors for use in methylotrophs and other Gram-negative bacteria. Microbiology (Reading, England) 2001, 147:2065-2075.
44. Mattozzi M.D.L.P., Keasling J.D. Rationally engineered biotransformation of p-nitrophenol. Biotechnol. Prog. 2010, 26:616-621.
45. Menendez C., Bauer Z., Huber H., Gad'on N., Stetter K.O., Fuchs G. Presence of acetyl coenzyme A (CoA) carboxylase and propionyl-CoA carboxylase in autotrophic Crenarchaeota and indication for operation of a 3-hydroxypropionate cycle in autotrophic carbon fixation. J. Bacteriol. 1999, 181:1088-1098.
46. Meng D.C., Shi Z.Y., Wu L.P., Zhou Q., Wu Q., Chen J.C., Chen G.Q. Production and characterization of poly(3-hydroxypropionate-co-4-hydroxybutyrate) with fully controllable structures by recombinant Escherichia coli containing an engineered pathway. Metab. Eng. 2012, 14:317-324.
47. Miller J. Experiments in Molecular Genetics 1972, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
48. Murphy K.C. Use of bacteriophage lambda recombination functions to promote gene replacement in Escherichia coli. J. Bacteriol. 1998, 180:2063-2071.
49. Pfeifer B.A., Admiraal S.J., Gramajo H., Cane D.E., Khosla C. Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science (New York, N.Y.) 2001, 291:1790-1792.
50. Psencík J., Collins A.M., Liljeroos L., Torkkeli M., Laurinmäki P., Ansink H.M., Ikonen T.P., Serimaa R.E., Blankenship R.E., Tuma R., Butcher S.J. Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus. J. Bacteriol. 2009, 191:6701-6708.
51. Rathnasingh C., Raj S.M., Lee Y., Catherine C., Ashok S., Park S. Production of 3-hydroxypropionic acid via malonyl-CoA pathway using recombinant Escherichia coli strains. J. Biotechnol. 2011, 157:633-640.
52. Roy I., Leadlay P.F. Physical map location of the new Escherichia coli gene sbm. J. Bacteriol. 1992, 174:5763-5764.
53. cat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J. Exp. Bot. 2001, 53:609-620.
54. 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 3rd ed. J. Sambrook, D.W. Russell (Eds.).
55. 2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle. Eur. J. Biochem. FEBS 1993, 215:633-643.
56. Tang K.-H., Barry K., Chertkov O., Dalin E., Han C.S., Hauser L.J., Honchak B.M., Karbach L.E., Land M.L., Lapidus A., Larimer F.W., Mikhailova N., Pitluck S., Pierson B.K., Blankenship R.E. Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genomics 2011, 12:334.
57. Thomason L., Court D.L., Bubunenko M., Costantino N., Wilson H., Datta S., Oppenheim A. Recombineering: genetic engineering in bacteria using homologous recombination. Current Protocols in Molecular Biology 2007, F.M. Ausubel (Ed.).
58. Wang R.Y., Shi Z.Y., Chen J.C., Wu Q., Chen G.C. Enhanced co-production of hydrogen and poly-(R)-3-hydroxybutyrate by recombinant PHB producing E. coli over-expressing hydrogenase 3 and acetyl-CoA synthetase. Metab. Eng. 2012, 14:496-503.
59. Wang Q., Liu C., Xian M., Zhang Y., Zhao G. Biosynthetic pathway for poly(3-Hydroxypropionate) in recombinant Escherichia coli. J. Microbiol. 2012, 50:693-697.
60. Weiss, R., Kelly, J., Bryant, R., Rubin, A., 2008. Registry of Standard Biological Parts Ribosome Binding Sites Community Collection [www Document]. URL http://partsregistry.org/Ribosome_Binding_Sites/Prokaryotic/Constitutive/Community_Collection.
61. Yu B.J., Sung B.H., Lee J.Y., Son S.H., Kim M.S., Kim S.C. sucAB and sucCD are mutually essential genes in Escherichia coli. FEMS Microbiol. Lett. 2006, 254:245-250.
62. Zarzycki J., Brecht V., Müller M., Fuchs G. Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:21317-21322.
63. Zarzycki J., Fuchs G. Co-assimilation of organic substrates via the autotrophic 3-hydroxypropionate bi-cycle in Chloroflexus aurantiacus. Appl. Environ. Microbiol. 2011, 77:6181-6188.
64. Zhang F., Rodriguez S., Keasling J.D. Metabolic engineering of microbial pathways for advanced biofuels production. Curr. Opin. Biotechnol. 2011, 22:775-783.
65. Zhang H., Boghigian B.A., Pfeifer B.A. Investigating the role of native propionyl-CoA and methylmalonyl-CoA metabolism on heterologous polyketide production in Escherichia coli. Biotechnol. Bioeng. 2010, 105:567-573.
66. Zhang H., Wang Y., Boghigian B.A., Pfeifer B.A. Probing the heterologous metabolism supporting 6-deoxyerythronolide B biosynthesis in Escherichia coli. Microbiol. Biotechnol. 2009, 2:390-394.
67. Zhou Q., Shi Z.-Y., Meng D.C., Wu Q., Chen J.C., Chen G.C. Production of 3-hydroxypropionate homopolymer and poly(3-hydroxypropionate-co-4-hydroxybutyrate) copolymer by recombinant Escherichia coli. Metab. Eng. 2011, 13:777-785.