Reaction kinetic analysis of the 3-hydroxypropionate/4-hydroxybutyrate CO2 fixation cycle in extremely thermoacidophilic archaea

Metabolic Engineering

Volumn 38, Issue , 2016, Pages 446-463

  Loder, Andrew J ^a   Han, Yejun ^a   Hawkins, Aaron B ^a   Lian, Hong ^a   Lipscomb, Gina L ^b   Schut, Gerrit J ^b   Keller, Matthew W ^b   Adams, Michael W W ^b   Kelly, Robert M ^a  

^a North Carolina State University   (United States)

^b University of Georgia   (United States)

Author keywords

3 hydroxypropionate; 4 hydroxybutyrate; CO2 fixation; Metallosphaera sedula

Indexed keywords

BIOTECHNOLOGY; CARBON; KINETICS; METABOLIC ENGINEERING; METABOLISM; MICROORGANISMS; REACTION KINETICS;

3-HYDROXYPROPIONATE; 4-HYDROXYBUTYRATE; CARBON FLUXES; CHEMICAL INTERMEDIATES; CONTROL POINT; METALLOSPHAERA SEDULA; REACTION KINETICS MODELS; RELATIVE RATIOS;

CARBON DIOXIDE;

3 HYDROXYPROPIONYL COENZYME A DEHYDRATASE; 3 HYDROXYPROPIONYL COENZYME A SYNTHETASE; 4 HYDROXYBUTYRIC ACID; ACETYL COENZYME A; ACETYL COENZYME A CARBOXYLASE; ACRYLOYLSUCCINYL COENZYME A REDUCTASE; BACTERIAL ENZYME; CARBON DIOXIDE; HYDRACRYLIC ACID; HYDROLYASE; HYDROXYBUTYRYL COENYZME A SYNTHETASE; MALONYL COENZYME A REDUCTASE; OXIDOREDUCTASE; PROPIONYL COENZYME A CARBOXYLASE; SUCCINIC ACID; SUCCINIC SEMIALDEHYDE REDUCTASE; SUCCINYL COENZYME A REDUCTASE; SYNTHETASE; UNCLASSIFIED DRUG; 4-HYDROXYBUTYRIC ACID; HYDROXYBUTYRIC ACID; LACTIC ACID;

ARTICLE; BACTERIAL GROWTH; CARBON DIOXIDE FIXATION; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; KINETIC PARAMETERS; METABOLIC ENGINEERING; METALLOSPHAERA SEDULA; NONHUMAN; PRIORITY JOURNAL; THERMOACIDOPHILIC ARCHAEON; THERMOSTABILITY; ANALOGS AND DERIVATIVES; ARCHAEON; BIOLOGICAL MODEL; EXTREMOPHILE; KINETICS; METABOLIC CLEARANCE RATE; METABOLIC FLUX ANALYSIS; METABOLISM; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; SULFOLOBALES;

ARCHAEA; CARBON DIOXIDE; EXTREMOPHILES; HYDROXYBUTYRATES; KINETICS; LACTIC ACID; METABOLIC CLEARANCE RATE; METABOLIC FLUX ANALYSIS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SULFOLOBACEAE;

EID: 84994806794     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2016.10.009     Document Type: Article

References (56)

1. Alber, B., Olinger, M., Rieder, A., Kockelkorn, D., Jobst, B., Hugler, M., Fuchs, G., Malonyl-coenzyme A reductase in the modified 3-hydroxypropionate cycle for autotrophic carbon fixation in archaeal Metallosphaera and Sulfolobus spp. J. Bacteriol. 188 (2006), 8551-8559.
2. 2 fixation. J. Bacteriol. 190 (2008), 1383-1389.
3. Amend, J.P., Shock, E.L., Energetics of overall metabolic reactions of thermophilic and hyperthermophilic archaea and bacteria. FEMS Microbiol. Rev. 25 (2001), 175-243.
4. Auernik, K.S., Kelly, R.M., Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by transcriptomic analysis of heterotrophic, autotrophic, and mixotrophic growth. Appl. Environ. Microbiol. 76 (2010), 931-935.
5. Bennett, B.D., Kimball, E.H., Gao, M., Osterhout, R., Van Dien, S.J., Rabinowitz, J.D., Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5 (2009), 593-599.
6. 2 fixation pathways. Appl. Environ. Microbiol. 77 (2011), 1925-1936.
7. Berg, I.A., Kockelkorn, D., Buckel, W., Fuchs, G., A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. Science 318 (2007), 1782-1786.
8. 2 fixation cycles in Crenarchaeota. Microbiology 156 (2010), 256-269.
9. Blanch, H.W., Clark, D.S., Biochemical Engineering. 1997, Marcel Dekker, Inc, New York, NY.
10. Carroll, J.J., Slupsky, J.D., Mather, A.E., The solubility of carbon dioxide in water at low pressure. J. Phys. Chem. Ref. Data, 20, 1991, 1201.
11. Chung, H., Yang, J.E., Ha, J.Y., Chae, T.U., Shin, J.H., Gustavsson, M., Lee, S.Y., Bio-based production of monomers and polymers by metabolically engineered microorganisms. Curr. Opin. Biotechnol. 36 (2015), 73-84.
12. Conrado, R.J., Haynes, C.A., Haendler, B.E., Toone, E.J., Electrofuels: a new paradigm for renewable fuels. Lee, J.W., (eds.) Advanced Biofuels and Bioproducts, 2013, Springer, New York, New York, NY, 1037-1064.
13. Cook, P.F., Cleland, W.W., Enzyme Kinetics and Mechanism. 2007, Taylor & Francis, New York, NY.
14. Estelmann, S., Hugler, M., Eisenreich, W., Werner, K., Berg, I.A., Ramos-Vera, W.H., Say, R.F., Kockelkorn, D., Gad'on, N., Fuchs, G., Labeling and enzyme studies of the central carbon metabolism in Metallosphaera sedula. J. Bacteriol. 193 (2011), 1191-1200.
15. 2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals. Curr. Opin. Chem. Eng. 1 (2012), 380-395.
16. Fell, D., Understanding the Control of Metabolism. 1997, Portland Press, London, UK.
17. Flamholz, A., Noor, E., Bar-Even, A., Milo, R., eQuilibrator - the biochemical thermodynamics calculator. Nucleic Acids Res. 40 (2012), D770-D775.
18. Han, Y., Hawkins, A.S., Adams, M.W., Kelly, R.M., Epimerase (Msed_0639) and mutase (Msed_0638 and Msed_2055) convert (S)-methylmalonyl-coenzyme A (CoA) to succinyl-CoA in the Metallosphaera sedula 3-hydroxypropionate/4-hydroxybutyrate cycle. Appl. Environ. Microbiol. 78 (2012), 6194-6202.
19. Hawkins, A.B., Adams, M.W., Kelly, R.M., Conversion of 4-hydroxybutyrate to acetyl-coenzyme A and its anapleurosis in the Metallosphaera sedula 3-hydroxypropionate/4-hydroxybutyrate carbon fixation pathway. Appl. Environ. Microbiol. 80 (2014), 2536-2545.
20. 2-based 3-hydroxypropionate production. Biotechnol. Bioeng. 112 (2015), 1533-1543.
21. 2 fixation cycle in thermoacidophilic archaea. J. Biol. Chem. 288 (2013), 4012-4022.
22. 2 fixation pathway in Chloroflexus aurantiacus. J. Biol. Chem. 277 (2002), 20277-20283.
23. Huang, Y., Li, Z., Shimizu, K., Ye, Q., Co-production of 3-hydroxypropionic acid and 1,3-propanediol by Klebseilla pneumoniae expressing aldH under microaerobic conditions. Bioresour. Technol. 128 (2013), 505-512.
24. 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. USA 105 (2008), 7851-7856.
25. Hugler, M., Krieger, R.S., Jahn, M., Fuchs, G., Characterization of acetyl-CoA/propionyl-CoA carboxylase in Metallosphaera sedula. Eur. J. Biochem. 270 (2003), 736-744.
26. Keller, M., Loder, A., Basen, M., Izquierdo, J., Kelly, R.M., Adams, M.W.W., Production of lignofuels and electrofuels by extremely thermophilic microbes. Biofuels 5 (2015), 499-515.
27. Keller, M.W., Schut, G.J., Lipscomb, G.L., Menon, A.L., Iwuchukwu, I.J., Leuko, T.T., Thorgersen, M.P., Nixon, W.J., Hawkins, A.S., Kelly, R.M., Adams, M.W.W., Exploiting microbial hyperthermophilicity to produce an industrial chemical, using hydrogen and carbon dioxide. Proc. Natl. Acad. Sci. USA 110 (2013), 5840-5845.
28. Kerkhoven, E.J., Lahtvee, P.-J., Nielsen, J., Applications of computational modeling in metabolic engineering of yeast. FEMS Yeast Res., 15, 2014.
29. Kockelkorn, D., Fuchs, G., Malonic semialdehyde reductase, succinic semialdehyde reductase, and succinyl-coenzyme A reductase from Metallosphaera sedula: enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in Sulfolobales. J. Bacteriol. 191 (2009), 6352-6362.
30. Kumar, V., Ashok, S., Park, S., Recent advances in biological production of 3-hydroxypropionic acid. Biotechnol. Adv. 31 (2013), 945-961.
31. Leyn, S.A., Rodionova, I.A., Li, X., Rodionov, D.A., Novel transcriptional regulons for autotrophic cycle genes in Crenarchaeota. J. Bacteriol. 197 (2015), 2383-2391.
32. 2 to higher alcohols. Science, 335, 2012, 1596.
33. 2 incorporation into 3-hydroxypropionate by metabolically engineered Pyrococcus furiosus. Biotechnol. Bioeng., 2016, 10.1002/bit.26033.
34. Liebermeister, W., Klipp, E., Bringing metabolic networks to life: convenience rate law and thermodynamic constraints. Theor. Biol. Med. Model., 3, 2006, 41.
35. Lipscomb, G.L., Stirrett, K., Schut, G.J., Yang, F., Jenney, F.E., Scott, R.A., Adams, M.W.W., Westpheling, J., Natural competence in the hyperthermophilic archaeon Pyrococcus furiosus facilitates genetic manipulation: construction of markerless deletions of genes encoding the two cytoplasmic hydrogenases. Appl. Environ. Microbiol. 77 (2011), 2232-2238.
36. Loder, A.J., Zeldes, B.M., Garrison, G.D. 2nd, Lipscomb, G.L., Adams, M.W., Kelly, R.M., Alcohol selectivity in a synthetic thermophilic n-butanol pathway is driven by biocatalytic and thermostability characteristics of constituent enzymes. Appl. Environ. Microbiol. 81 (2015), 7187-7200.
37. Maezato, Y., Johnson, T., McCarthy, S., Dana, K., Blum, P., Metal resistance and lithoautotrophy in the extreme thermoacidophile Metallosphaera sedula. J. Bacteriol. 194 (2012), 6856-6863.
38. Marcheschi, R.J., Li, H., Zhang, K., Noey, E.L., Kim, S., Chaubey, A., Houk, K.N., Liao, J.C., A synthetic recursive “+1″ pathway for carbon chain elongation. ACS Chem. Biol. 7 (2012), 689-697.
39. Mattozzi, M., Ziesack, M., Voges, M.J., Silver, P.A., Way, J.C., Expression of the sub-pathways of the Chloroflexus aurantiacus 3-hydroxypropionate carbon fixation bicycle in E. coli: toward horizontal transfer of autotrophic growth. Metab. Eng. 16 (2013), 130-139.
40. McCloskey, D., Palsson, B.O., Feist, A.M., Basic and applied uses of genome-scale metabolic network reconstructions of Escherichia coli. Mol. Syst. Biol., 9, 2013, 661.
41. Muller, J., MacEachran, D., Burd, H., Sathitsuksanoh, N., Bi, C., Yeh, Y.C., Lee, T.S., Hillson, N.J., Chhabra, S.R., Singer, S.W., Beller, H.R., Engineering of Ralstonia eutropha H16 for autotrophic and heterotrophic production of methyl ketones. Appl. Environ. Microbiol. 79 (2013), 4433-4439.
42. Noor, E., Bar-Even, A., Flamholz, A., Reznik, E., Liebermeister, W., Milo, R., Pathway thermodynamics highlights kinetic obstacles in central metabolism. PLoS Comput. Biol., 10, 2014, e1003483.
43. Nybo, S.E., Khan, N.E., Woolston, B.M., Curtis, W.R., Metabolic engineering in chemolithoautotrophic hosts for the production of fuels and chemicals. Metab. Eng. 30 (2015), 105-120.
44. Okino, S., Noburyu, R., Suda, M., Jojima, T., Inui, M., Yukawa, H., An efficient succinic acid production process in a metabolically engineered Corynebacterium glutamicum strain. Appl. Microbiol. Biotechnol. 81 (2008), 459-464.
45. Peeples, T.L., Kelly, R.M., Bioenergetic response of the extreme thermoacidophile Metallosphaera sedula to thermal and nutritional stresses. Appl. Environ. Microbiol. 61 (1995), 2314-2321.
46. Ramos-Vera, W.H., Weiss, M., Strittmatter, E., Kockelkorn, D., Fuchs, G., Identification of missing genes and enzymes for autotrophic carbon fixation in crenarchaeota. J. Bacteriol. 193 (2011), 1201-1211.
47. 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. 157 (2012), 633-640.
48. Teufel, R., Kung, J.W., Kockelkorn, D., Alber, B.E., Fuchs, G., 3-hydroxypropionyl-coenzyme A dehydratase and acryloyl-coenzyme A reductase, enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in the Sulfolobales. J. Bacteriol. 191 (2009), 4572-4581.
49. Thorgersen, M.P., Lipscomb, G.L., Schut, G.J., Kelly, R.M., Adams, M.W.W., Deletion of acetyl-CoA synthetases I and II increases production of 3-hydroxypropionate by the metabolically-engineered hyperthermophile Pyrococcus furiosus. Metab. Eng. 22 (2014), 83-88.
50. Ueki, T., Nevin, K.P., Woodard, T.L., Lovley, D.R., Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii. mBio, 5, 2014 (e01636-14).
51. Wagner, M., van Wolferen, M., Wagner, A., Lassak, K., Meyer, B.H., Reimann, J., Albers, S.V., Versatile genetic tool box for the crenarchaeote Sulfolobus acidocaldarius. Front. Microbiol., 3, 2012, 214.
52. Wheaton, G., Counts, J., Mukherjee, A., Kruh, J., Kelly, R., The confluence of heavy metal biooxidation and heavy metal resistance: implications for bioleaching by extreme thermoacidophiles. Minerals 5 (2015), 397-451.
53. Yuzawa, S., Chiba, N., Katz, L., Keasling, J.D., Construction of a part of a 3-hydroxypropionate cycle for heterologous polyketide biosynthesis in Escherichia coli. Biochemistry 51 (2012), 9779-9781.
54. Zeldes, B.M., Keller, M.W., Loder, A.J., Straub, C.T., Adams, M.W., Kelly, R.M., Extremely thermophilic microorganisms as metabolic engineering platforms for production of fuels and industrial chemicals. Front. Microbiol., 6, 2015, 1209.
55. Zhang, F., Carothers, J.M., Keasling, J.D., Design of a dynamic sensor-regulator system for production of chemicals and fuels derived from fatty acids. Nat. Biotechnol. 30 (2012), 354-359.
56. Zhang, Y.H., Substrate channeling and enzyme complexes for biotechnological applications. Biotechnol. Adv. 29 (2011), 715-725.