Biofuel metabolic engineering with biosensors

Current Opinion in Chemical Biology

Volumn 35, Issue , 2016, Pages 150-158

  Morgan, Stacy Anne ^a   Nadler, Dana C ^a   Yokoo, Rayka ^a   Savage, David F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFUEL; G PROTEIN COUPLED RECEPTOR; RNA; TRANSCRIPTION FACTOR;

BIOSENSOR; CYTOSOL; METABOLIC ENGINEERING; METABOLITE; MOLECULAR DYNAMICS; PHENOTYPE; REGULATORY MECHANISM; REVIEW; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC PROCEDURES; METABOLISM; PROCEDURES;

BIOFUELS; BIOSENSING TECHNIQUES; FLUORESCENCE RESONANCE ENERGY TRANSFER; METABOLIC ENGINEERING; RNA;

EID: 84992109183     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2016.09.020     Document Type: Review

References (73)

1. 1 Keasling, J.D., Manufacturing molecules through metabolic engineering. Science 330 (2010), 1355–1358.
2. 2 Haimovich, A.D., Muir, P., Isaacs, F.J., Genomes by design. Nat Rev Genet 16 (2015), 501–516.
3. 3 Liu, R., Bassalo, M.C., Zeitoun, R.I., Gill, R.T., Genome scale engineering techniques for metabolic engineering. Metab Eng 32 (2015), 143–154.
4. 4 Hounslow, E., Noirel, J., Gilmour, D.J., Wright, P.C., Lipid quantification techniques for screening oleaginous species of microalgae for biofuel production. Eur J Lipid Sci Technol, 2016, 10.1002/ejlt.201500469.
5. 5 Petzold, C.J., Chan, L.J.G., Nhan, M., Adams, P.D., Analytics for metabolic engineering. Front Bioeng Biotechnol, 3, 2015, 135.
6. 6 Bennett, B.D., Yuan, J., Kimball, E.H., Rabinowitz, J.D., Absolute quantitation of intracellular metabolite concentrations by an isotope ratio-based approach. Nat Protoc 3 (2008), 1299–1311.
7. 7 Vanderporten, E., Frick, L., Turincio, R., Thana, P., Lamarr, W., Liu, Y., Label-free high-throughput assays to screen and characterize novel lactate dehydrogenase inhibitors. Anal Biochem 441 (2013), 115–122.
8. 8 Northen, T.R., Yanes, O., Northen, M.T., Marrinucci, D., Uritboonthai, W., Apon, J., Golledge, S.L., Nordström, A., Siuzdak, G., Clathrate nanostructures for mass spectrometry. Nature 449 (2007), 1033–1036.
9. 9 Heins, R.A., Cheng, X., Nath, S., Deng, K., Bowen, B.P., Chivian, D.C., Datta, S., Friedland, G.D., D'Haeseleer, P., Wu, D., et al. Phylogenomically guided identification of industrially relevant GH1 β-glucosidases through DNA synthesis and nanostructure-initiator mass spectrometry. ACS Chem Biol 9 (2014), 2082–2091.
10. 10 Heim, R., Tsien, R.Y., Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6 (1996), 178–182.
11. 11 Miyawaki, A., Llopis, J., Heim, R., McCaffery, J.M., Adams, J.A., Ikura, M., Tsien, R.Y., Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388 (1997), 882–887.
12. 12 Deuschle, K., Okumoto, S., Fehr, M., Looger, L.L., Kozhukh, L., Frommer, W.B., Construction and optimization of a family of genetically encoded metabolite sensors by semirational protein engineering. Protein Sci 14 (2005), 2304–2314.
13. 13 Baird, G.S., Zacharias, D.A., Tsien, R.Y., Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci U S A 96 (1999), 11241–11246.
14. 14 Berg, J., Hung, Y.P., Yellen, G., A genetically encoded fluorescent reporter of ATP:ADP ratio. Nat Methods 6 (2009), 161–166.
15. + redox state with a genetically encoded fluorescent biosensor. Cell Metab 14 (2011), 545–554.
16. 16•• Ng, C.Y., Farasat, I., Maranas, C.D., Salis, H.M., Rational design of a synthetic Entner–Doudoroff pathway for improved and controllable NADPH regeneration. Metab Eng 29 (2015), 86–96 The authors used MAGE strain engineering to create computationally designed RBS variants of a synthetic Entner–Doudoroff pathway within E. coli and screened for NADPH production in microwell plates with a SFPB. This is the first published example of high-throughput screening using an SFPB.
17. 17 Nadler, D.C., Morgan, S.A., Flamholz, A., Kortright, K.E., Savage, D.F., Rapid construction of metabolite biosensors using domain-insertion profiling. Nat Commun, 7, 2016, 12266.
18. 18 Barrick, J.E., Breaker, R.R., The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol, 8, 2007, R239.
19. 19 McKeague, M., Derosa, M.C., Challenges and opportunities for small molecule aptamer development. J Nucleic Acids, 2012, 2012, 748913.
20. 20 Michener, J.K., Smolke, C.D., High-throughput enzyme evolution in Saccharomyces cerevisiae using a synthetic RNA switch. Metab Eng 14 (2012), 306–316.
21. 21 Meyer, A., Pellaux, R., Potot, S., Becker, K., Hohmann, H.-P., Panke, S., Held, M., Optimization of a whole-cell biocatalyst by employing genetically encoded product sensors inside nanolitre reactors. Nat Chem 7 (2015), 673–678.
22. 22 Lee, S.-W., Oh, M.-K., A synthetic suicide riboswitch for the high-throughput screening of metabolite production in Saccharomyces cerevisiae. Metab Eng 28 (2015), 143–150.
23. 23 Gu, M.B., Mitchell, R.J., Kim, B.C., Whole-cell-based biosensors for environmental biomonitoring and application. Adv Biochem Eng Biotechnol 87 (2004), 269–305.
24. 24 Dietrich, J.A., Shis, D.L., Alikhani, A., Keasling, J.D., Transcription factor-based screens and synthetic selections for microbial small-molecule biosynthesis. ACS Synth Biol 2 (2013), 47–58.
25. 25 Li, S., Si, T., Wang, M., Zhao, H., Development of a synthetic malonyl-CoA sensor in Saccharomyces cerevisiae for intracellular metabolite monitoring and genetic screening. ACS Synth Biol 4 (2015), 1308–1315.
26. 26 Raman, S., Rogers, J.K., Taylor, N.D., Church, G.M., Evolution-guided optimization of biosynthetic pathways. Proc Natl Acad Sci U S A 111 (2014), 17803–17808.
27. 27• Chou, H.H., Keasling, J.D., Programming adaptive control to evolve increased metabolite production. Nat Commun, 4, 2013, 2595 This paper used a synthetic-TF biosensor to repress the expression of a mutator polymerase (broken proof-reading exonuclease). This system increases mutations and explores genetic diversity while ligand levels were low, then ‘locks in’ the genotype as metabolite levels rise.
28. 28 Farmer, W.R., Liao, J.C., Improving lycopene production in Escherichia coli by engineering metabolic control. Nat Biotechnol 18 (2000), 533–537.
29. 29 Scalcinati, G., Partow, S., Siewers, V., Schalk, M., Daviet, L., Nielsen, J., Combined metabolic engineering of precursor and co-factor supply to increase α-santalene production by Saccharomyces cerevisiae. Microb Cell Factories, 11, 2012, 117.
30. 30 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.
31. 31•• Xu, P., Li, L., Zhang, F., Stephanopoulos, G., Koffas, M., Improving fatty acids production by engineering dynamic pathway regulation and metabolic control. Proc Natl Acad Sci U S A 111 (2014), 11299–11304 Using a TF, the authors engineered both up-regulation and down-regulation of genes within a fatty acid pathway in response to malonyl-CoA concentration. This unique example of one TF providing both types of pathway control improved fatty acid production greater than threefold.
32. 32 Alon, U., An Introduction to Systems Biology: Design Principles of Biological Circuits. 2007.
33. 33 Erickson, J.P., Wu, J.J., Goddard, J.G., Tigyi, G., Kawanishi, K., Tomei, L.D., Kiefer, M.C., Edg-2/Vzg-1 couples to the yeast pheromone response pathway selectively in response to lysophosphatidic acid. J Biol Chem 273 (1998), 1506–1510.
34. 34 Radhika, V., Proikas-Cezanne, T., Jayaraman, M., Onesime, D., Ha, J.H., Dhanasekaran, D.N., Chemical sensing of DNT by engineered olfactory yeast strain. Nat Chem Biol 3 (2007), 325–330.
35. 35 Mukherjee, K., Bhattacharyya, S., Peralta-Yahya, P., GPCR-based chemical biosensors for medium-chain fatty acids. ACS Synth Biol 4 (2015), 1261–1269.
36. 36 Mombaerts, P., Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5 (2004), 263–278.
37. 37 Levskaya, A., Chevalier, A.A., Tabor, J.J., Simpson, Z.B., Lavery, L.A., Levy, M., Davidson, E.A., Scouras, A., Ellington, A.D., Marcotte, E.M., et al. Synthetic biology: engineering Escherichia coli to see light. Nat Cell Biol 438 (2005), 441–442.
38. 38 Baumgartner, J.W., Kim, C., Brissette, R.E., Inouye, M., Park, C., Hazelbauer, G.L., Transmembrane signalling by a hybrid protein: communication from the domain of chemoreceptor Trg that recognizes sugar-binding proteins to the kinase/phosphatase domain of osmosensor EnvZ. J Bacteriol 176 (1994), 1157–1163.
39. 39 Ninfa, A.J., Use of two-component signal transduction systems in the construction of synthetic genetic networks. Curr Opin Microbiol 13 (2010), 240–245.
40. 40 Ganesh, I., Ravikumar, S., Yoo, I.-K., Hong, S.H., Construction of malate-sensing Escherichia coli by introduction of a novel chimeric two-component system. Bioprocess Biosyst Eng 38 (2015), 797–804.
41. 41 Liu, D., Xiao, Y., Evans, B.S., Zhang, F., Negative feedback regulation of fatty acid production based on a malonyl-CoA sensor-actuator. ACS Synth Biol 4 (2015), 132–140.
42. 42 Voigt, C.A., Genetic parts to program bacteria. Curr Opin Biotechnol 17 (2006), 548–557.
43. 43 David, F., Nielsen, J., Siewers, V., Flux control at the malonyl-CoA node through hierarchical dynamic pathway regulation in Saccharomyces cerevisiae. ACS Synth Biol 5 (2016), 224–233.
44. 44 Siedler, S., Schendzielorz, G., Binder, S., Eggeling, L., Bringer, S., Bott, M., SoxR as a single-cell biosensor for NADPH-consuming enzymes in Escherichia coli. ACS Synth Biol 3 (2014), 41–47.
45. 45 Feng, J., Jester, B.W., Tinberg, C.E., Mandell, D.J., Antunes, M.S., Chari, R., Morey, K.J., Rios, X., Medford, J.I., Church, G.M., et al. A general strategy to construct small molecule biosensors in eukaryotes. eLife, 2015, 4.
46. 46 Santos, C.N.S., Stephanopoulos, G., Melanin-based high-throughput screen for L-tyrosine production in Escherichia coli. Appl Environ Microbiol 74 (2008), 1190–1197.
47. 47• DeLoache, W.C., Russ, Z.N., Narcross, L., Gonzales, A.M., Martin, V.J.J., Dueber, J.E., An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose. Nat Chem Biol 11 (2015), 465–471 This paper developed an enzyme-based biosensor for L-DOPA, transforming it into a fluorescent pigment for efficient screening of tyrosine to L-DOPA conversion. This approach shows future promise for detecting biofuel-related molecules as pathways toward other fluorescent products, such as polyenes, are elucidated.
48. 48 Rogers, J.K., Church, G.M., Genetically encoded sensors enable real-time observation of metabolite production. Proc Natl Acad Sci U S A 113 (2016), 2388–2393.
49. 49• Delépine, B., Libis, V., Carbonell, P., Faulon, J.-L., SensiPath: computer-aided design of sensing-enabling metabolic pathways. Nucleic Acids Res, 2016, 10.1093/nar/gkw305 This work reports SensiPath ( http://sensipath.micalis.fr), an informative, web-based tool for the computer-aided design of metabolic pathways that can convert a non-detectable target metabolite to one that can be detected.
50. 50 Ferrell, J.E., Tsai, T.Y.-C., Yang, Q., Modeling the cell cycle: why do certain circuits oscillate?. Cell 144 (2011), 874–885.
51. 51 Lindsley, J.E., Rutter, J., Whence cometh the allosterome?. Proc Natl Acad Sci U S A 103 (2006), 1053–10535.
52. 52•• Vetting, M.W., Al-Obaidi, N., Zhao, S., San Francisco, B., Kim, J., Wichelecki, D.J., Bouvier, J.T., Solbiati, J.O., Vu, H., Zhang, X., et al. Experimental strategies for functional annotation and metabolism discovery: targeted screening of solute binding proteins and unbiased panning of metabolomes. Biochem 54 (2015), 909–931 This paper used computational and high-throughput experimental approaches to determine ligands and functional annotations for members of a family of solute binding proteins. Such approaches may be useful in mining novel LBDs from putative protein sequences found in genome and metagenome sequencing projects.
53. 53 Uchiyama, T., Abe, T., Ikemura, T., Watanabe, K., Substrate-induced gene-expression screening of environmental metagenome libraries for isolation of catabolic genes. Nat Biotechnol 23 (2005), 88–93.
54. 54 Tinberg, C.E., Khare, S.D., Dou, J., Doyle, L., Nelson, J.W., Schena, A., Jankowski, W., Kalodimos, C.G., Johnsson, K., Stoddard, B.L., et al. Computational design of ligand-binding proteins with high affinity and selectivity. Nature 501 (2013), 212–216.
55. 55 Taylor, N.D., Garruss, A.S., Moretti, R., Chan, S., Arbing, M.A., Cascio, D., Rogers, J.K., Isaacs, F.J., Kosuri, S., Baker, D., et al. Engineering an allosteric transcription factor to respond to new ligands. Nat Methods 13 (2015), 177–183.
56. 56 Deuschle, K., Chaudhuri, B., Okumoto, S., Lager, I., Lalonde, S., Frommer, W.B., Rapid metabolism of glucose detected with FRET glucose nanosensors in epidermal cells and intact roots of Arabidopsis RNA-silencing mutants. Plant Cell 18 (2006), 2314–2325.
57. 57 Guntas, G., Mansell, T.J., Kim, J.R., Ostermeier, M., Directed evolution of protein switches and their application to the creation of ligand-binding proteins. Proc Natl Acad Sci U S A 102 (2005), 11224–11229.
58. 58 Oakes, B.L., Nadler, D.C., Flamholz, A., Fellmann, C., Staahl, B.T., Doudna, J.A., Savage, D.F., Profiling of engineering hotspots identifies an allosteric CRISPR-Cas9 switch. Nat Biotechnol 34 (2016), 646–651.
59. 59 Reynolds, K.A., McLaughlin, R.N., Ranganathan, R., Hot spots for allosteric regulation on protein surfaces. Cell 147 (2011), 1564–1575.
60. + redox visualized in brain slices by two-photon fluorescence lifetime biosensor imaging. Antioxid Redox Signal, 2016, 10.1089/ars.2015.6593.
61. 61 Zhang, D., He, Y., Wang, Y., Wang, H., Wu, L., Aries, E., Huang, W.E., Whole-cell bacterial bioreporter for actively searching and sensing of alkanes and oil spills. Microbial Biotechnol 5 (2012), 87–97.
62. 62 Sticher, P., Jaspers, M.C., Stemmler, K., Harms, H., Zehnder, A.J., van der Meer, J.R., Development and characterization of a whole-cell bioluminescent sensor for bioavailable middle-chain alkanes in contaminated groundwater samples. Appl Environ Microbiol 63 (1997), 4053–4060.
63. 63 Tang, S.-Y., Cirino, P.C., Design and application of a mevalonate-responsive regulatory protein. Angew Chem Int Ed Engl 50 (2011), 1084–1086.
64. 64 Zhang, Y.-M., Rock, C.O., A rainbow coalition of lipid transcriptional regulators. Mol Microbiol 78 (2010), 5–8.
65. 65 Imamura, H., Nhat, K.P.H., Togawa, H., Saito, K., Iino, R., Kato-Yamada, Y., Nagai, T., Noji, H., Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc Natl Acad Sci U S A 106 (2009), 15651–15656.
66. 66 San Martín, A., Ceballo, S., Ruminot, I., Lerchundi, R., Frommer, W.B., Barros, L.F., A genetically encoded FRET lactate sensor and its use to detect the Warburg effect in single cancer cells. PLoS ONE, 8, 2013, e57712.
67. 67 Fehr, M., Lalonde, S., Lager, I., Wolff, M.W., Frommer, W.B., In vivo imaging of the dynamics of glucose uptake in the cytosol of COS-7 cells by fluorescent nanosensors. J Biol Chem 278 (2003), 19127–19133.
68. 68 San Martín, A., Ceballo, S., Baeza-Lehnert, F., Lerchundi, R., Valdebenito, R., Contreras-Baeza, Y., Alegría, K., Barros, L.F., Imaging mitochondrial flux in single cells with a FRET sensor for pyruvate. PLoS ONE, 9, 2014, e85780.
69. 69 Dahl, R.H., Zhang, F., Alonso-Gutierrez, J., Baidoo, E., Batth, T.S., Redding-Johanson, A.M., Petzold, C.J., Mukhopadhyay, A., Lee, T.S., Adams, P.D., et al. Engineering dynamic pathway regulation using stress-response promoters. Nat Biotechnol 31 (2013), 1039–1046.
70. 70 Knudsen, J.D., Carlquist, M., Gorwa-Grauslund, M., NADH-dependent biosensor in Saccharomyces cerevisiae: principle and validation at the single cell level. AMB Express, 4, 2014, 81.
71. 71 Scalcinati, G., Knuf, C., Partow, S., Chen, Y., Maury, J., Schalk, M., Daviet, L., Nielsen, J., Siewers, V., Dynamic control of gene expression in Saccharomyces cerevisiae engineered for the production of plant sesquiterpene α-santalene in a fed-batch mode. Metab Eng 14 (2012), 91–103.
72. 72 Østergaard, H., Henriksen, A., Hansen, F.G., Winther, J.R., Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J 20 (2001), 5853–5862.
73. 73 Akiyama, N., Takeda, K., Miki, K., Crystal structure of a periplasmic substrate-binding protein in complex with calcium lactate. J Mol Biol 392 (2009), 559–565.