Pathway design using de novo steps through uncharted biochemical spaces

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Kumar, Akhil ^a   Wang, Lin ^b   Ng, Chiam Yu ^b   Maranas, Costas D ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b The Pennsylvania State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 BUTANEDIOL; BENZO[A]PYRENE; CATECHOL; PHENYLEPHRINE; ORGANIC COMPOUND;

ALGORITHM; BIOCHEMISTRY; BIODEGRADATION; BIOTRANSFORMATION; COMPLEXITY; DESIGN METHOD; DETECTION METHOD; DRUG; ENZYME; ENZYME ACTIVITY; METABOLITE; MICROBIAL ACTIVITY; THERMODYNAMICS; XENOBIOTICS;

ARTICLE; BIOTRANSFORMATION; CHEMICAL REACTION; CHEMICAL STRUCTURE; INFORMATION PROCESSING; NOVOSTOIC PROCEDURE; OXIDATION; REPRIME PROCEDURE; SYNTHESIS; ALGORITHM; BIOLOGY; CHEMICAL MODEL; CHEMISTRY; METABOLISM; PROCEDURES; THERMODYNAMICS;

ALGORITHMS; COMPUTATIONAL BIOLOGY; METABOLIC NETWORKS AND PATHWAYS; MODELS, CHEMICAL; MOLECULAR STRUCTURE; ORGANIC CHEMICALS; THERMODYNAMICS;

EID: 85043307792     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-02362-x     Document Type: Article

References (70)

1. Rodriguez, G. M., Tashiro, Y. &Atsumi, S. Expanding ester biosynthesis in Escherichia coli. Nat. Chem. Biol. 10, 259-265 (2014).
2. Atsumi, S., Hanai, T. &Liao, J. C. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451, 86-89 (2008).
3. Khersonsky, O., Roodveldt, C. &Tawfik, D. S. Enzyme promiscuity: evolutionary and mechanistic aspects. Curr. Opin. Chem. Biol. 10, 498-508 (2006).
4. Nam, H. et al. Network context and selection in the evolution to enzyme specificity. Science 337, 1101-1104 (2012).
5. Coelho, P. S., Brustad, E. M., Kannan, A. &Arnold, F. H. Olefin cyclopropanation via carbene transfer catalyzed by engineered cytochrome P450 enzymes. Science 339, 307-310 (2013).
6. Young, E. M., Tong, A., Bui, H., Spofford, C. &Alper, H. S. Rewiring yeast sugar transporter preference through modifying a conserved protein motif. Proc. Natl Acad. Sci. USA 111, 131-136 (2014).
7. Huisman, G. W., Liang, J. &Krebber, A. Practical chiral alcohol manufacture using ketoreductases. Curr. Opin. Chem. Biol. 14, 122-129 (2010).
8. Savile, C. K. et al. Biocatalytic asymmetric synthesis of chiral amines from ketones applied to sitagliptin manufacture. Science 329, 305-309 (2010).
9. Saraf, M. C., Moore, G. L., Goodey, N. M. &Cao, V. Y. IPRO: an iterative computational protein library redesign and optimization procedure. Biophys. J. 90, 4167-4180 (2006).
10. Liu, Y. &Kuhlman, B. RosettaDesign server for protein design. Nucleic Acids Res. 34, W235-W238 (2006).
11. Siegel, J. B. et al. Computational protein design enables a novel one-carbon assimilation pathway. Proc. Natl Acad. Sci. USA 112, 3704-3709 (2015).
12. Khersonsky, O. et al. Bridging the gaps in design methodologies by evolutionary optimization of the stability and proficiency of designed Kemp eliminase KE59. Proc. Natl Acad. Sci. USA 109, 10358-10363 (2012).
13. Ogata, H. et al. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 27, 29-34 (1999).
14. Rahman, S. A., Advani, P., Schunk, R., Schrader, R. &Schomburg, D. Metabolic pathway analysis web service (Pathway Hunter Tool at CUBIC). Bioinformatics 21, 1189-1193 (2005).
15. Blum, T. &Kohlbacher, O. MetaRoute: fast search for relevant metabolic routes for interactive network navigation and visualization. Bioinformatics 24, 2108-2109 (2008).
16. Pey, J., Prada, J., Beasley, J. E. &Planes, F. J. Path finding methods accounting for stoichiometry in metabolic networks. Genome Biol. 12, R49 (2011).
17. de Figueiredo, L., Podhorski, A. &Rubio, A. Computing the shortest elementary flux modes in genome-scale metabolic networks. Bioinformatics 25, 3158-3165 (2009).
18. Chowdhury, A. &Maranas, C. D. Designing overall stoichiometric conversions and intervening metabolic reactions. Sci. Rep. 5, 16009 (2015).
19. Kumar, A., Suthers, P. F. &Maranas, C. D. MetRxn: a knowledgebase of metabolites and reactions spanning metabolic models and databases. BMC Bioinformatics 13, 6 (2012).
20. Kanehisa, M., Goto, S. &Sato, Y. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199-D205 (2014).
21. Schomburg, I., Chang, A. &Placzek, S. BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Res. 41, D764-D772 (2013).
22. Caspi, R. et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 40, D742-D753 (2012).
23. Dugundji Ivar, J. U. An algebraic model of constitutional chemistry as a basis for chemical computer programs. Comput. Chem. 39, 19-64 (1973).
24. Yamanishi, Y., Hattori, M., Kotera, M., Goto, S. &Kanehisa, M. Enzyme: predicting potential EC numbers from the chemical transformation pattern of substrate-product pairs. Bioinformatics 25, i179-i186 (2009).
25. Weininger, D., Weininger, A. &Weininger, J. L. SMILES. 2. Algorithm for generation of unique SMILES notation. J. Chem. Inf. Model. 29, 97-101 (1989).
26. Finley, S. D., Broadbelt, L. J. &Hatzimanikatis, V. Computational framework for predictive biodegradation. Biotechnol. Bioeng. 104, 1086-1097 (2009).
27. Carbonell, P., Parutto, P., Herisson, J., Pandit, S. B. &Faulon, J.-L. XTMS: pathway design in an eXTended metabolic space. Nucleic Acids Res. 42, W389-W394 (2014).
28. Fenner, K., Gao, J., Kramer, S., Ellis, L. &Wackett, L. Data-driven extraction of relative reasoning rules to limit combinatorial explosion in biodegradation pathway prediction. Bioinformatics 24, 2079-2085 (2008).
29. Moriya, Y. et al. PathPred: an enzyme-catalyzed metabolic pathway prediction server. Nucleic Acids Res. 38, 1-6 (2010).
30. Law, J. et al. Route Designer: a retrosynthetic analysis tool utilizing automated retrosynthetic rule generation. J. Chem. Inf. Model. 49, 593-602 (2009).
31. Campodonico, M. A., Andrews, B. A., Asenjo, J. A., Palsson, B. O. &Feist, A. M. Generation of an atlas for commodity chemical production in Escherichia coli and a novel pathway prediction algorithm, GEM-Path. Metab. Eng. 25, 140-158 (2014).
32. Henry, C. S., Broadbelt, L. J. &Hatzimanikatis, V. Thermodynamics-based metabolic flux analysis. Biophys. J. 92, 1792-1805 (2007).
33. Boghigian, B. A., Shi, H., Lee, K. &Pfeifer, B. A. Utilizing elementary mode analysis, pathway thermodynamics, and a genetic algorithm for metabolic flux determination and optimal metabolic network design. BMC Syst. Biol. 4, 49 (2010).
34. Kumar, A. &Maranas, C. D. CLCA: maximum common molecular substructure queries within the MetRxn database. J. Chem. Inf. Model. 54, 3417-3438 (2014).
35. Yim, H. et al. Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol. Nat. Chem. Biol. 7, 445-452 (2011).
36. 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 110, 87-92 (2013).
37. Morgat, A., Lombardot, T., Axelsen, K. B. &Aimo, L. Updates in rhea-an expert curated resource of biochemical reactions. Nucleic Acids Res. 45, 4279 (2016).
38. Baison, W., Teerawutgulrag, A., Puangsombat, P. &Rakariyatham, N. An alternative synthesis of (+/-)-phenylephrine hydrochloride. Maejo Int. J. Sci. Technol. 8, 41-47 (2014).
39. Zhang, W., Ames, B. D. &Walsh, C. T. Identification of phenylalanine 3-hydroxylase for meta-tyrosine biosynthesis. Biochemistry 50, 5401-5403 (2011).
40. Hagel, J. M., Krizevski, R., Marsolais, F., Lewinsohn, E. &Facchini, P. J. Biosynthesis of amphetamine analogs in plants. Trends Plant. Sci. 17, 404-412 (2012).
41. Lenders, J. W. M. et al. Specific genetic deficiencies of the A and B isoenzymes of monoamine oxidase are characterized by distinct neurochemical and clinical phenotypes. J. Clin. Invest. 97, 1010-1019 (1996).
42. McClymont, K. &Soyer, O. S. Metabolic tinker: an online tool for guiding the design of synthetic metabolic pathways. Nucleic Acids Res. 41, e113 (2013).
43. Pandey, R. K., Upadhyay, P. K. &Kumar, P. Enantioselective synthesis of (R)-phenylephrine hydrochloride. Tetrahedron Lett. 44, 6245-6246 (2003).
44. Russell, P. B. &Childress, S. J. New route to phenylephrine. J. Pharm. Sci. 50, 713-771 (1961).
45. Gurjar, M. K., Krishna, L. M., Sarma, B. V. N. B. S. &Chorghade, M. S. A practical synthesis of (R)-(-)-phenylephrine hydrochloride. Org. Proc. Res. Dev. 2, 422-424 (1998).
46. Shobayashi, M., Mukai, N., Iwashita, K., Hiraga, Y. &Iefuji, H. A new method for isolation of S-adenosylmethionine (SAM)-accumulating yeast. Appl. Microbiol. Biotechnol. 69, 704-710 (2006).
47. Chen, H. et al. Intracellular expression of Vitreoscilla hemoglobin improves Sadenosylmethionine production in a recombinant Pichia pastoris. Appl. Microbiol. Biotechnol. 74, 1205-1212 (2007).
48. Yu, H. Environmental carcinogenic polycyclic aromatic hydrocarbons: photochemistry and phototoxicity. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev. 20, 149-183 (2002).
49. Mueller, J. G. et al. Phylogenetic and physiological comparisons of PAHdegrading bacteria from geographically diverse soils. Antonie Van Leeuwenhoek 71, 329-343 (1997).
50. Habe, H. &Omori, T. Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci. Biotechnol. Biochem. 67, 225-243 (2003).
51. Gadd, G. M. Fungi in Bioremediation (Cambridge University Press, Cambridge, UK, 2001).
52. Haritash, A. K. &Kaushik, C. P. Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J. Hazard. Mater. 169, 1-15 (2009).
53. Yang, Y., Chen, R. F. &Shiaris, M. P. Metabolism of naphthalene, fluorene, and phenanthrene: preliminary characterization of a cloned gene cluster from Pseudomonas putida NCIB 9816. J. Bacteriol. 176, 2158-2164 (1994).
54. Zhang, K., Sawaya, M. R., Eisenberg, D. S. &Liao, J. C. Expanding metabolism for biosynthesis of nonnatural alcohols. Proc. Natl Acad. Sci. USA 105, 20653-20658 (2008).
55. Currin, A., Swainston, N., Day, P. J. &Kell, D. B. Synthetic biology for the directed evolution of protein biocatalysts: navigating sequence space intelligently. Chem. Soc. Rev. 44, 1172-1239 (2015).
56. Jessen, H. J., Liao, H. H., Gort, S. J. &Selifonova, O. V. Beta-alanine/alphaketoglutarate aminotransferase for 3-hydroxypropionic acid production. US patent application US20090291480 A1 (2014).
57. Liao, H. H., Gokarn, R. R., Gort, S. J. &Jessen, H. J. Alanine 2, 3-aminomutase. US patent application US20080124785 A1 (2007).
58. Renata, H., Wang, Z. J. &Arnold, F. H. Expanding the enzyme universe: accessing non-natural reactions by mechanism-guided directed evolution. Angew. Chem. Int. Ed. 54, 3351-3367 (2015).
59. France, S. P., Hepworth, L. J., Turner, N. J. &Flitsch, S. L. Constructing biocatalytic cascades: in vitro and in vivo approaches to de novo multi-enzyme pathways. ACS Catal. 7, 710-724 (2017).
60. Moretti, S. et al. MetaNetX/MNXref-reconciliation of metabolites and biochemical reactions to bring together genome-scale metabolic networks. Nucleic Acids Res. 44, D523-D526 (2016).
61. Lang, M., Stelzer, M. &Schomburg, D. BKM-react, an integrated biochemical reaction database. BMC Biochem. 12, 42 (2011).
62. Poux, S. et al. On expert curation and scalability: UniProtKB/Swiss-Prot as a case study. Bioinformatics 33, 3454-3460 (2017).
63. Burgard, A. P., Pharkya, P. &Maranas, C. D. OptKnock: a bilevel programming framework for identifying gene knockout strategies for microbial strain optimization. Biotechnol. Bioeng. 84, 647-657 (2003).
64. Ranganathan, S., Suthers, P. F. &Maranas, C. D. OptForce: an optimization procedure for identifying all genetic manipulations leading to targeted overproductions. PLoS Comput. Biol. 6, e1000744 (2010).
65. Mahadevan, R., Kamp, von, A. &Klamt, S. Genome-scale strain designs based on regulatory minimal cut sets. Bioinformatics 31, 2844-2851 (2015).
66. Mellor, J., Grigoras, I., Carbonell, P. &Faulon, J.-L. Semisupervised Gaussian process for automated enzyme search. ACS Synth. Biol. 5, 518-528 (2016).
67. Richard, A. M. et al. ToxCast chemical landscape: paving the road to 21st century toxicology. Chem. Res. Toxicol. 29, 1225-1251 (2016).
68. Pandit, A. V., Srinivasan, S. &Mahadevan, R. Redesigning metabolism based on orthogonality principles. Nat. Commun. 8, 15188 (2017).
69. Noor, E., Haraldsdóttir, H. S., Milo, R. &Fleming, R. M. T. Consistent estimation of Gibbs energy using component contributions. PLoS Comput. Biol. 9, e1003098 (2013).
70. Flamholz, A., Noor, E., Bar-Even, A. &Milo, R. eQuilibrator\-The biochemical thermodynamics calculator. Nucleic Acids Res. 40, D770-D775 (2012).