Conversion of Escherichia coli to Generate All Biomass Carbon from CO2

Cell

Volumn 179, Issue 6, 2019, Pages 1255-1263.e12

  Gleizer, Shmuel ^a   Ben Nissan, Roee ^a   Bar On, Yinon M ^a   Antonovsky, Niv ^a   Noor, Elad ^a   Zohar, Yehudit ^a   Jona, Ghil ^a   Krieger, Eyal ^a   Shamshoum, Melina ^a   Bar Even, Arren ^a   Milo, Ron ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

adaptive laboratory evolution; carbon fixation; Escherichia coli; metabolic rewiring; Rubisco; sustainability; synthetic autotrophy; synthetic biology

Indexed keywords

CARBON; CARBON DIOXIDE; FORMATE DEHYDROGENASE; FORMIC ACID; AMINO ACID; CARBON-13;

ARTICLE; AUTOTROPHY; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BIOMASS CONVERSION; CARBON DIOXIDE FIXATION; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; ELECTROCHEMISTRY; ENERGY; ESCHERICHIA COLI; ISOTOPE LABELING; LABORATORY; NONHUMAN; PRIORITY JOURNAL; REDUCTION (CHEMISTRY); TIME FACTOR; ADAPTATION; BIOMASS; DIRECTED MOLECULAR EVOLUTION; GENETICS; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLISM; MUTATION; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; AMINO ACIDS; AUTOTROPHIC PROCESSES; BIOMASS; CARBON; CARBON DIOXIDE; CARBON ISOTOPES; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; ISOTOPE LABELING; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; MUTATION;

EID: 85075382914     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2019.11.009     Document Type: Article

References (60)

1. Aigner, H., Wilson, R.H., Bracher, A., Calisse, L., Bhat, J.Y., Hartl, F.U., Hayer-Hartl, M., Plant RuBisCo assembly in E. coli with five chloroplast chaperones including BSD2. Science 358 (2017), 1272–1278.
2. Antonovsky, N., Gleizer, S., Noor, E., Zohar, Y., Herz, E., Barenholz, U., Zelcbuch, L., Amram, S., Wides, A., Tepper, N., et al. Sugar Synthesis from CO2 in Escherichia coli. Cell 166 (2016), 115–125.
3. 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., 2, 2006, 2006.0008.
4. Bar-On, Y.M., Phillips, R., Milo, R., The biomass distribution on Earth. Proc. Natl. Acad. Sci. USA 115 (2018), 6506–6511.
5. Barenholz, U., Davidi, D., Reznik, E., Bar-On, Y., Antonovsky, N., Noor, E., Milo, R., Design principles of autocatalytic cycles constrain enzyme kinetics and force low substrate saturation at flux branch points. eLife, 6, 2017, e20667.
6. Barrick, J.E., Colburn, G., Deatherage, D.E., Traverse, C.C., Strand, M.D., Borges, J.J., Knoester, D.B., Reba, A., Meyer, A.G., Identifying structural variation in haploid microbial genomes from short-read resequencing data using breseq. BMC Genomics, 15, 2014, 1039.
7. 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.
8. 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. 4 (2002), 217–229.
9. Blount, Z.D., Barrick, J.E., Davidson, C.J., Lenski, R.E., Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489 (2012), 513–518.
10. Braatsch, S., Helmark, S., Kranz, H., Koebmann, B., Jensen, P.R., Escherichia coli strains with promoter libraries constructed by Red/ET recombination pave the way for transcriptional fine-tuning. Biotechniques 45 (2008), 335–337.
11. Cherepanov, P.P., Wackernagel, W., Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158 (1995), 9–14.
12. Claassens, N.J., Sánchez-Andrea, I., Sousa, D.Z., Bar-Even, A., Towards sustainable feedstocks: A guide to electron donors for microbial carbon fixation. Curr. Opin. Biotechnol. 50 (2018), 195–205.
13. Clasquin, M.F., Melamud, E., Rabinowitz, J.D., LC-MS data processing with MAVEN: a metabolomic analysis and visualization engine. Curr. Protoc. Bioinformatics, Chapter 14, 2012, Unit14.11.
14. Crowther, T.W., Glick, H.B., Covey, K.R., Bettigole, C., Maynard, D.S., Thomas, S.M., Smith, J.R., Hintler, G., Duguid, M.C., Amatulli, G., et al. Mapping tree density at a global scale. Nature 525 (2015), 201–205.
15. Ebrahim, A., Lerman, J.A., Palsson, B.O., Hyduke, D.R., COBRApy: COnstraints-Based Reconstruction and Analysis for Python. BMC Syst. Biol., 7, 2013, 74.
16. Edwards, J.S., Ibarra, R.U., Palsson, B.O., In silico predictions of Escherichia coli metabolic capabilities are consistent with experimental data. Nat. Biotechnol. 19 (2001), 125–130.
17. Egorov, A.M., Popov, V.O., Berezin, I.V., Rodionov, U.V., Kinetic and structural properties of Nad-Dependent bacterial formate dehydrogenase. J. Solid-Phase Biochem. 5 (1980), 19–33.
18. Folsom, J.P., Carlson, R.P., Physiological, biomass elemental composition and proteomic analyses of Escherichia coli ammonium-limited chemostat growth, and comparison with iron- and glucose-limited chemostat growth. Microbiology 161 (2015), 1659–1670.
19. French, K.E., Harnessing synthetic biology for sustainable development. Nat. Sustain. 2 (2019), 250–252.
20. Glazyrina, J., Materne, E.M., Dreher, T., Storm, D., Junne, S., Adams, T., Greller, G., Neubauer, P., High cell density cultivation and recombinant protein production with Escherichia coli in a rocking-motion-type bioreactor. Microb. Cell Fact., 9, 2010, 42.
21. Grenier, F., Matteau, D., Baby, V., Rodrigue, S., Complete Genome Sequence of Escherichia coli BW25113. Genome Announc., 2, 2014, e01038-14.
22. Gresham, D., Hong, J., The functional basis of adaptive evolution in chemostats. FEMS Microbiol. Rev. 39 (2015), 2–16.
23. Grunwald, S., Mottet, A., Grousseau, E., Plassmeier, J.K., Popović, M.K., Uribelarrea, J.L., Gorret, N., Guillouet, S.E., Sinskey, A., Kinetic and stoichiometric characterization of organoautotrophic growth of Ralstonia eutropha on formic acid in fed-batch and continuous cultures. Microb. Biotechnol. 8 (2015), 155–163.
24. Herz, E., Antonovsky, N., Bar-On, Y., Davidi, D., Gleizer, S., Prywes, N., Noda-Garcia, L., Frisch, K.L., Zohar, Y., Wernick, D.G., et al. The genetic basis for the adaptation of E. coli to sugar synthesis from CO2. Nat. Commun., 8, 2017, 1705.
25. Holzhütter, H.-G., The principle of flux minimization and its application to estimate stationary fluxes in metabolic networks. Eur. J. Biochem. 271 (2004), 2905–2922.
26. Huang, H., Wang, S., Moll, J., Thauer, R.K., Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J. Bacteriol. 194 (2012), 3689–3699.
27. Innocent, B., Liaigre, D., Pasquier, D., Francois, R., Leger, J.-M., Kokoh, K., Electro-reduction of carbon dioxide to formate on lead electrode in aqueous medium. J. Appl. Electrochem. 39 (2009), 227–232.
28. 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., Exploiting microbial hyperthermophilicity to produce an industrial chemical, using hydrogen and carbon dioxide. Proc. Natl. Acad. Sci. USA 110 (2013), 5840–5845.
29. Kromdijk, J., Głowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K., Long, S.P., Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354 (2016), 857–861.
30. Kubis, A., Bar-Even, A., Synthetic biology approaches for improving photosynthesis. J. Exp. Bot. 70 (2019), 1425–1433.
31. Malhotra, A., Severinova, E., Darst, S.A., Crystal structure of a σ 70 subunit fragment from E. coli RNA polymerase. Cell 87 (1996), 127–136.
32. Marlière, P., Patrouix, J., Döring, V., Herdewijn, P., Tricot, S., Cruveiller, S., Bouzon, M., Mutzel, R., Chemical evolution of a bacterium's genome. Angew. Chem. Int. Ed. Engl. 50 (2011), 7109–7114.
33. Masters, M., Colloms, M.D., Oliver, I.R., He, L., Macnaughton, E.J., Charters, Y., The pcnB gene of Escherichia coli, which is required for ColE1 copy number maintenance, is dispensable. J. Bacteriol. 175 (1993), 4405–4413.
34. Mattozzi, M.D., 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.
35. Nielsen, J., Keasling, J.D., Engineering Cellular Metabolism. Cell 164 (2016), 1185–1197.
36. Ort, D.R., Merchant, S.S., Alric, J., Barkan, A., Blankenship, R.E., Bock, R., Croce, R., Hanson, M.R., Hibberd, J.M., Long, S.P., et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. USA 112 (2015), 8529–8536.
37. Orth, J.D., Fleming, R.M.T., Palsson, B.Ø., Reconstruction and Use of Microbial Metabolic Networks: the Core Escherichia coli Metabolic Model as an Educational Guide. Ecosal Plus, 4, 2010.
38. Orth, J.D., Thiele, I., Palsson, B.Ø., What is flux balance analysis?. Nat. Biotechnol., 28, 2010, 245.
39. Phaneuf, P.V., Gosting, D., Palsson, B.O., Feist, A.M., ALEdb 1.0: a database of mutations from adaptive laboratory evolution experimentation. Nucleic Acids Res. 47:D1 (2019), D1164–D1171.
40. Pontrelli, S., Fricke, R.C.B., Sakurai, S.S.M., Putri, S.P., Fitz-Gibbon, S., Chung, M., Wu, H.Y., Chen, Y.J., Pellegrini, M., Fukusaki, E., Liao, J.C., Directed strain evolution restructures metabolism for 1-butanol production in minimal media. Metab. Eng. 49 (2018), 153–163.
41. Pontrelli, S., Chiu, T.-Y., Lan, E.I., Chen, F.Y., Chang, P., Liao, J.C., Escherichia coli as a host for metabolic engineering. Metab. Eng. 50 (2018), 16–46.
42. Popov, V.O., Lamzin, V.S., NAD(+)-dependent formate dehydrogenase. Biochem. J. 301 (1994), 625–643.
43. Pronk, J.T., Meijer, W.M., Hazeu, W., van Dijken, J.P., Bos, P., Kuenen, J.G., Growth of Thiobacillus ferrooxidans on Formic Acid. Appl. Environ. Microbiol. 57 (1991), 2057–2062.
44. Quandt, E.M., Deatherage, D.E., Ellington, A.D., Georgiou, G., Barrick, J.E., Recursive genomewide recombination and sequencing reveals a key refinement step in the evolution of a metabolic innovation in Escherichia coli. Proc. Natl. Acad. Sci. USA 111 (2014), 2217–2222.
45. Reeder, T., Schleif, R., Mapping, sequence, and apparent lack of function of araJ, a gene of the Escherichia coli arabinose regulon. J. Bacteriol. 173 (1991), 7765–7771.
46. Sauer, U., Evolutionary engineering of industrially important microbial phenotypes. Adv. Biochem. Eng. Biotechnol. 73 (2001), 129–169.
47. Schada von Borzyskowski, L., Carrillo, M., Leupold, S., Glatter, T., Kiefer, P., Weishaupt, R., Heinemann, M., Erb, T.J., An engineered Calvin-Benson-Bassham cycle for carbon dioxide fixation in Methylobacterium extorquens AM1. Metab. Eng. 47 (2018), 423–433.
48. Schwander, T., Schada von Borzyskowski, L., Burgener, S., Cortina, N.S., Erb, T.J., A synthetic pathway for the fixation of carbon dioxide in vitro. Science 354 (2016), 900–904.
49. Smith, A.M., Stitt, M., Coordination of carbon supply and plant growth. Plant Cell Environ. 30 (2007), 1126–1149.
50. Sonderegger, M., Sauer, U., Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl. Environ. Microbiol. 69 (2003), 1990–1998.
51. Song, S., Park, C., Organization and regulation of the D-xylose operons in Escherichia coli K-12: XylR acts as a transcriptional activator. J. Bacteriol. 179 (1997), 7025–7032.
52. South, P.F., Cavanagh, A.P., Liu, H.W., Ort, D.R., Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science, 363, 2019, eaat9077.
53. Thomason, L.C., Costantino, N., Court, D.L., E. coli genome manipulation by P1 transduction. Curr. Protoc. Mol. Biol., Chapter 1, 2007, Unit 1.17.
54. Totir, M., Echols, N., Nanao, M., Gee, C.L., Moskaleva, A., Gradia, S., Iavarone, A.T., Berger, J.M., May, A.P., Zubieta, C., Alber, T., Macro-to-micro structural proteomics: native source proteins for high-throughput crystallization. PLoS ONE, 7, 2012, e32498.
55. Utrilla, J., O'Brien, E.J., Chen, K., McCloskey, D., Cheung, J., Wang, H., Armenta-Medina, D., Feist, A.M., Palsson, B.O., Global Rebalancing of Cellular Resources by Pleiotropic Point Mutations Illustrates a Multi-scale Mechanism of Adaptive Evolution. Cell Syst. 2 (2016), 260–271.
56. Volpers, M., Claassens, N.J., Noor, E., van der Oost, J., de Vos, W.M., Kengen, S.W., Martins Dos Santos, V.A., Integrated In Silico Analysis of Pathway Designs for Synthetic Photo-Electro-Autotrophy. PLoS ONE, 11, 2016, e0157851.
57. Wides, A., Milo, R., Understanding the Dynamics and Optimizing the Performance of Chemostat Selection Experiments. arXiv, 2018 arXiv:1806.00272 https://arxiv.org/abs/1806.00272.
58. Yishai, O., Lindner, S.N., Gonzalez de la Cruz, J., Tenenboim, H., Bar-Even, A., The formate bio-economy. Curr. Opin. Chem. Biol. 35 (2016), 1–9.
59. Zamboni, N., Sauer, U., Novel biological insights through metabolomics and 13C-flux analysis. Curr. Opin. Microbiol. 12 (2009), 553–558.
60. Zelcbuch, L., Antonovsky, N., Bar-Even, A., Levin-Karp, A., Barenholz, U., Dayagi, M., Liebermeister, W., Flamholz, A., Noor, E., Amram, S., et al. Spanning high-dimensional expression space using ribosome-binding site combinatorics. Nucleic Acids Res., 41, 2013, e98.