Tracing metabolism from lignocellulosic biomass and gaseous substrates to products with stable-isotopes

Current Opinion in Biotechnology

Volumn 43, Issue , 2017, Pages 86-95

  Gonzalez, Jacqueline E ^a   Antoniewicz, Maciek R ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMASS; CARBON; CARBON DIOXIDE; FEEDSTOCKS; ISOTOPES; METABOLISM; PHYSIOLOGY;

BIOLOGICAL PROCESS; CENTRAL METABOLISMS; ECONOMIC FEASIBILITIES; ISOTOPOMER ANALYSIS; LIGNOCELLULOSIC BIOMASS; METABOLIC FLUX ANALYSIS; PROCESS PERFORMANCE; VALUE ADDED PRODUCTS;

METABOLIC ENGINEERING;

ARABINOSE; CARBON 13; GALACTOSE; GLUCOSE; LIGNOCELLULOSE; MANNOSE; METHANE; XYLOSE; CARBON; GAS; LIGNIN;

BIOMASS; BIOTRANSFORMATION; CARBON SOURCE; CATABOLISM; ESCHERICHIA COLI; HUMAN; ISOTOPE LABELING; ISOTOPE TRACING; METABOLIC ENGINEERING; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; ANALYSIS; GAS; METABOLIC FLUX ANALYSIS; METABOLISM; PROCEDURES; THEORETICAL MODEL;

BIOMASS; CARBON ISOTOPES; GASES; LIGNIN; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; MODELS, THEORETICAL;

EID: 84992401825     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2016.10.002     Document Type: Review

References (83)

1. 1 Himmel, M.E., Bayer, E.A., Lignocellulose conversion to biofuels: current challenges, global perspectives. Curr Opin Biotechnol 20 (2009), 316–317.
2. 2 Elkins, J.G., Raman, B., Keller, M., Engineered microbial systems for enhanced conversion of lignocellulosic biomass. Curr Opin Biotechnol 21 (2010), 657–662.
3. 3 Liao, J.C., Mi, L., Pontrelli, S., Luo, S., Fuelling the future: microbial engineering for the production of sustainable biofuels. Nat Rev Microbiol 14 (2016), 288–304.
4. 4 Munasinghe, P.C., Khanal, S.K., Biomass-derived syngas fermentation into biofuels: opportunities and challenges. Bioresour Technol 101 (2010), 5013–5022.
5. 2 fixation by anaerobic non-photosynthetic mixotrophy for improved carbon conversion. Nat Commun, 7, 2016, 12800, 10.1038/ncomms12800 This study demonstrates that mixotrophic fermentations of sugars and gasses can improve product yields. In this case Clostridium ljungdahlii was engineered to produce acetone with a mass yield that corresponds to 138% of the theoretical heterotrophic maximum yield.
6. 6• Cordova, L.T., Long, C.P., Venkataramanan, K.P., Antoniewicz, M.R., Complete genome sequence, metabolic model construction and phenotypic characterization of Geobacillus LC300, an extremely thermophilic, fast growing, xylose-utilizing bacterium. Metab Eng 32 (2015), 74–81 This paper describes a new extremely thermophilic strain that catabolizes xylose, glucose and other sugars at rates that are several-fold higher than the best engineered mesophilic organisms.
7. 7 Papoutsakis, E.T., Reassessing the progress in the production of advanced biofuels in the current competitive environment and beyond: what are the successes and where progress eludes us and why. Ind Eng Chem Res 54 (2015), 10170–10182.
8. 8 Balderas-Hernandez, V.E., Hernandez-Montalvo, V., Bolivar, F., Gosset, G., Martinez, A., Adaptive evolution of Escherichia coli inactivated in the phosphotransferase system operon improves co-utilization of xylose and glucose under anaerobic conditions. Appl Biochem Biotechnol 163 (2011), 485–496.
9. 13C-metabolic flux analysis study of glucose/xylose co-utilization. Adaptive laboratory evolution was successfully applied to generate a strain that consumes multiple substrates without carbon catabolite repression.
10. 10 Jung, I.Y., Lee, J.W., Min, W.K., Park, Y.C., Seo, J.H., Simultaneous conversion of glucose and xylose to 3-hydroxypropionic acid in engineered Escherichia coli by modulation of sugar transport and glycerol synthesis. Bioresour Technol 198 (2015), 709–716.
11. 11 Aristilde, L., Lewis, I.A., Park, J.O., Rabinowitz, J.D., Hierarchy in pentose sugar metabolism in Clostridium acetobutylicum. Appl Environ Microbiol 81 (2015), 1452–1462.
12. 12 Grimmler, C., Held, C., Liebl, W., Ehrenreich, A., Transcriptional analysis of catabolite repression in Clostridium acetobutylicum growing on mixtures of D-glucose and D-xylose. J Biotechnol 150 (2010), 315–323.
13. 13 Ren, C., Gu, Y., Hu, S., Wu, Y., Wang, P., Yang, Y., Yang, C., Yang, S., Jiang, W., Identification and inactivation of pleiotropic regulator CcpA to eliminate glucose repression of xylose utilization in Clostridium acetobutylicum. Metab Eng 12 (2010), 446–454.
14. 14 Siebers, B., Schonheit, P., Unusual pathways and enzymes of central carbohydrate metabolism in Archaea. Curr Opin Microbiol 8 (2005), 695–705.
15. 15 Henard, C.A., Freed, E.F., Guarnieri, M.T., Phosphoketolase pathway engineering for carbon-efficient biocatalysis. Curr Opin Biotechnol 36 (2015), 183–188.
16. 16 Sund, C.J., Liu, S., Germane, K.L., Servinsky, M.D., Gerlach, E.S., Hurley, M.M., Phosphoketolase flux in Clostridium acetobutylicum during growth on L-arabinose. Microbiology 161 (2015), 430–440.
17. 13C metabolic flux analysis. J Bacteriol 194 (2012), 5413–5422.
18. 18 Xiong, W., Lee, T.C., Rommelfanger, S., Gjersing, E., Cano, M., Maness, P.C., Ghirardi, M., Yu, J., Phosphoketolase pathway contributes to carbon metabolism in cyanobacteria. Nat Plants, 2, 2015, 15187.
19. 2 emission. J Biosci Bioeng 103 (2007), 262–269.
20. 20 Bogorad, I.W., Lin, T.S., Liao, J.C., Synthetic non-oxidative glycolysis enables complete carbon conservation. Nature 502 (2013), 693–697.
21. 21 Yang, X., Yuan, Q., Zheng, Y., Ma, H., Chen, T., Zhao, X., An engineered non-oxidative glycolysis pathway for acetone production in Escherichia coli. Biotechnol Lett 38 (2016), 1359–1365.
22. 22 Sonderegger, M., Schumperli, M., Sauer, U., Metabolic engineering of a phosphoketolase pathway for pentose catabolism in Saccharomyces cerevisiae. Appl Environ Microbiol 70 (2004), 2892–2897.
23. 23 de Jong, B.W., Shi, S., Siewers, V., Nielsen, J., Improved production of fatty acid ethyl esters in Saccharomyces cerevisiae through up-regulation of the ethanol degradation pathway and expression of the heterologous phosphoketolase pathway. Microb Cell Fact, 13, 2014, 39.
24. 24•• Cam, Y., Alkim, C., Trichez, D., Trebosc, V., Vax, A., Bartolo, F., Besse, P., Francois, J.M., Walther, T., Engineering of a synthetic metabolic pathway for the assimilation of D-xylose into value-added chemicals. ACS Synth Biol 5 (2016), 607–618 In this work a novel metabolic pathway was engineered in E. coli to convert xylose into products including ethylene glycol and glycolic acid at high yields.
25. 25•• Choi, S.Y., Park, S.J., Kim, W.J., Yang, J.E., Lee, H., Shin, J., Lee, S.Y., One-step fermentative production of poly(lactate-co-glycolate) from carbohydrates in Escherichia coli. Nat Biotechnol 34 (2016), 435–440 In this work E. coli was engineered to produce a wide range of biodegradable and biocompatible synthetic polymers from glucose and xylose. This was achieved by introducing the Dahms pathway to produce glycolate from xylose, and by eliminating carbon catabolite repression.
26. 26• Tai, Y.S., Xiong, M., Jambunathan, P., Wang, J., Wang, J., Stapleton, C., Zhang, K., Engineering nonphosphorylative metabolism to generate lignocellulose-derived products. Nat Chem Biol 12 (2016), 247–253 In this work the authors introduced the Weimberg pathway into E. coli and constructed an artificial biosynthetic pathways to 1,4-butanediol (BDO) that could achieve a high theoretical molar yield from D-xylose, L-arabinose and D-galacturonate. The titers, rates and yields were higher than those previously reported using conventional pathways.
27. 27 Radek, A., Krumbach, K., Gatgens, J., Wendisch, V.F., Wiechert, W., Bott, M., Noack, S., Marienhagen, J., Engineering of Corynebacterium glutamicum for minimized carbon loss during utilization of D-xylose containing substrates. J Biotechnol 192:Pt A (2014), 156–160.
28. 28 Kohler, K.A., Blank, L.M., Frick, O., Schmid, A., D-Xylose assimilation via the Weimberg pathway by solvent-tolerant Pseudomonas taiwanensis VLB120. Environ Microbiol 17 (2015), 156–170.
29. 29 Pereira, B., Li, Z.J., De Mey, M., Lim, C.G., Zhang, H., Hoeltgen, C., Stephanopoulos, G., Efficient utilization of pentoses for bioproduction of the renewable two-carbon compounds ethylene glycol and glycolate. Metab Eng 34 (2016), 80–87.
30. 30 Pereira, B., Zhang, H., De Mey, M., Lim, C.G., Li, Z.J., Stephanopoulos, G., Engineering a novel biosynthetic pathway in Escherichia coli for production of renewable ethylene glycol. Biotechnol Bioeng 113 (2016), 376–383.
31. 31 Fast, A.G., Schmidt, E.D., Jones, S.W., Tracy, B.P., Acetogenic mixotrophy: novel options for yield improvement in biofuels and biochemicals production. Curr Opin Biotechnol 33 (2015), 60–72.
32. 32 Hu, P., Chakraborty, S., Kumar, A., Woolston, B., Liu, H., Emerson, D., Stephanopoulos, G., Integrated bioprocess for conversion of gaseous substrates to liquids. Proc Natl Acad Sci U S A 113 (2016), 3773–3778.
33. 2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals. Curr Opin Chem Eng 1 (2012), 380–395.
34. 34 Berg, I.A., Kockelkorn, D., Ramos-Vera, W.H., Say, R.F., Zarzycki, J., Hugler, M., Alber, B.E., Fuchs, G., Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8 (2010), 447–460.
35. 35 Ducat, D.C., Way, J.C., Silver, P.A., Engineering cyanobacteria to generate high-value products. Trends Biotechnol 29 (2011), 95–103.
36. 2.
37. 2 fixation. Biotechnol Biofuels, 8, 2015, 86.
38. 38 Li, Y.H., Ou-Yang, F.Y., Yang, C.H., Li, S.Y., The coupling of glycolysis and the Rubisco-based pathway through the non-oxidative pentose phosphate pathway to achieve low carbon dioxide emission fermentation. Bioresour Technol 187 (2015), 189–197.
39. 39 Guadalupe-Medina, V., Wisselink, H.W., Luttik, M.A., de Hulster, E., Daran, J.M., Pronk, J.T., van Maris, A.J., Carbon dioxide fixation by Calvin-Cycle enzymes improves ethanol yield in yeast. Biotechnol Biofuels, 6, 2013, 125.
40. 40 Abubackar, H.N., Veiga, M.C., Kennes, C., Carbon monoxide fermentation to ethanol by Clostridium autoethanogenum in a bioreactor with no accumulation of acetic acid. Bioresour Technol 186 (2015), 122–127.
41. 41 Kopke, M., Held, C., Hujer, S., Liesegang, H., Wiezer, A., Wollherr, A., Ehrenreich, A., Liebl, W., Gottschalk, G., Durre, P., Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci U S A 107 (2010), 13087–13092.
42. 42 Fei, Q., Guarnieri, M.T., Tao, L., Laurens, L.M., Dowe, N., Pienkos, P.T., Bioconversion of natural gas to liquid fuel: opportunities and challenges. Biotechnol Adv 32 (2014), 596–614.
43. 43 Haynes, C.A., Gonzalez, R., Rethinking biological activation of methane and conversion to liquid fuels. Nat Chem Biol 10 (2014), 331–339.
44. 44 Whitaker, W.B., Jones, J.A., Bennett, K., Gonzalez, J.E., Vernacchio, V.R., Collins, S.M., Palmer, M.A., Schmidt, S., Antoniewicz, M.R., Koffas, M.A., et al. Engineering the biological conversion of methanol to specialty chemicals in Escherichia coli. Metab Eng, 2016.
45. 45 Lessmeier, L., Pfeifenschneider, J., Carnicer, M., Heux, S., Portais, J.C., Wendisch, V.F., Production of carbon-13-labeled cadaverine by engineered Corynebacterium glutamicum using carbon-13-labeled methanol as co-substrate. Appl Microbiol Biotechnol 99 (2015), 10163–10176.
46. 13C flux analysis. BMC Syst Biol, 7, 2013, 17.
47. 13C-metabolic flux analysis of co-cultures: a novel approach. Metab Eng 31 (2015), 132–139.
48. 48 Antoniewicz, M.R., Methods and advances in metabolic flux analysis: a mini-review. J Ind Microbiol Biotechnol 42 (2015), 317–325.
49. 49 Iwatani, S., Van Dien, S., Shimbo, K., Kubota, K., Kageyama, N., Iwahata, D., Miyano, H., Hirayama, K., Usuda, Y., Shimizu, K., et al. Determination of metabolic flux changes during fed-batch cultivation from measurements of intracellular amino acids by LC–MS/MS. J Biotechnol 128 (2007), 93–111.
50. 50 Antoniewicz, M.R., Tandem mass spectrometry for measuring stable-isotope labeling. Curr Opin Biotechnol 24 (2013), 48–53.
51. 51 McCloskey, D., Young, J.D., Xu, S., Palsson, B.O., Feist, A.M., MID max LC–MS/MS method for measuring the precursor and product mass isotopomer distributions of metabolic intermediates and cofactors for metabolic flux analysis applications. Anal Chem 88 (2016), 1362–1370.
52. 52 McConnell, B.O., Antoniewicz, M.R., Measuring the composition and stable-isotope labeling of algal biomass carbohydrates via gas chromatography/mass spectrometry. Anal Chem 88 (2016), 4624–4628.
53. 53 Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Measuring deuterium enrichment of glucose hydrogen atoms by gas chromatography/mass spectrometry. Anal Chem 83 (2011), 3211–3216.
54. 54 Choi, J., Grossbach, M.T., Antoniewicz, M.R., Measuring complete isotopomer distribution of aspartate using gas chromatography/tandem mass spectrometry. Anal Chem 84 (2012), 4628–4632.
55. 55 Long, C.P., Antoniewicz, M.R., Metabolic flux analysis of Escherichia coli knockouts: lessons from the Keio collection and future outlook. Curr Opin Biotechnol 28 (2014), 127–133.
56. 56• Khodayari, A., Zomorrodi, A.R., Liao, J.C., Maranas, C.D., A kinetic model of Escherichia coli core metabolism satisfying multiple sets of mutant flux data. Metab Eng 25 (2014), 50–62 This paper describes a detailed ensemble kinetic model of E. coli core metabolism that encompasses 138 reactions, 93 metabolites and 60 substrate-level regulatory interactions. The described model construction pipeline provides a systematic approach for future improvements as more flux data becomes available.
57. 57 Long, C.P., Gonzalez, J.E., Sandoval, N.R., Antoniewicz, M.R., Characterization of physiological responses to 22 gene knockouts in Escherichia coli central carbon metabolism. Metab Eng 37 (2016), 102–113.
58. 13C-MFA for high-resolution flux analysis. In this work, 14 parallel labeling experiments were successfully integrated to generate the most accurate and precise flux map measured thus far for E. coli.
59. 13C metabolic flux analysis. Curr Opin Biotechnol 36 (2015), 91–97.
60. 60 Au, J., Choi, J., Jones, S.W., Venkataramanan, K.P., Antoniewicz, M.R., Parallel labeling experiments validate Clostridium acetobutylicum metabolic network model for C metabolic flux analysis. Metab Eng 26 (2014), 23–33.
61. 13C metabolic flux analysis of the extremely thermophilic, fast growing, xylose-utilizing Geobacillus strain LC300. Metab Eng 33 (2016), 148–157.
62. 62 Crown, S.B., Marze, N., Antoniewicz, M.R., Catabolism of branched chain amino acids contributes significantly to synthesis of odd-chain and even-chain fatty acids in 3T3-L1 adipocytes. PLOS ONE, 10, 2015, e0145850.
63. 13C]glutamine provide new insights into CHO cell metabolism. Metab Eng 15 (2013), 34–47.
64. 13C-metabolic flux analysis. Metab Eng 37 (2016), 72–78.
65. 13C-isotopomer data sets to study metabolism in perfused working hearts. Am J Physiol Heart Circ Physiol 311 (2016), H881–H891.
66. 13C-metabolic flux analysis using elementary metabolite units (EMU) basis vector methodology. Metab Eng 14 (2012), 150–161.
67. 13C-MFA. The study demonstrates that flux precision can be dramatically improved when multiple tracers are used in parallel labeling experiments.
68. 68 David, H., Krogh, A.M., Roca, C., Akesson, M., Nielsen, J., CreA influences the metabolic fluxes of Aspergillus nidulas during growth on glucose and xylose. Microbiology 151 (2005), 2209–2221.
69. 69 Grotkjaer, T., Christakopoulos, P., Nielsen, J., Olsson, L., Comparative metabolic network analysis of two xylose fermenting recombinant Saccharomyces cerevisiae strains. Metab Eng 7 (2005), 437–444.
70. 13C metabolic flux analysis of microbial and mammalian systems is enhanced with GC–MS measurements of glycogen and RNA labeling. Metab Eng 38 (2016), 65–72.
71. 13C nuclear magnetic resonance spectroscopy to elucidate L-arabinose metabolism in yeasts. Appl Environ Microbiol 74 (2008), 1845–1855.
72. 72 Fendt, S.M., Sauer, U., Transcriptional regulation of respiration in yeast metabolizing differently repressive carbon substrates. BMC Syst Biol, 4, 2010, 12.
73. 13C NMR study of glucose and cellobiose metabolism by four cellulolytic strains of the genus Fibrobacter. Biodegradation 9 (1998), 451–461.
74. 74 Benisch, F., Boles, E., The bacterial Entner-Doudoroff pathway does not replace glycolysis in Saccharomyces cerevisiae due to the lack of activity of iron-sulfur cluster enzyme 6-phosphogluconate dehydratase. J Biotechnol 171 (2014), 45–55.
75. 13C flux profiling reveals conservation of the Entner-Doudoroff pathway as a glycolytic strategy among marine bacteria that use glucose. Appl Environ Microbiol 81 (2015), 2408–2422.
76. 76 Xiong, W., Lee, T.C., Rommelfanger, S., Gjersing, E., Cano, M., Maness, P.C., Ghirardi, M., Yu, J., Phosphoketolase pathway contributes to carbon metabolism in cyanobacteria. Nat Plants, 2016, 10.1038/nplants.2015.1187.
77. 77 Guo, W., He, R., Ma, L., Jia, W., Li, D., Chen, S., Construction of a constitutively expressed homo-fermentative pathway in Lactobacillus brevis. Appl Microbiol Biotechnol 98 (2014), 6641–6650.
78. 13C Nuclear Magnetic Resonance. Appl Environ Microbiol 79 (2013), 7628–7638.
79. 13C flux analysis. Metab Eng 13 (2011), 656–665.
80. 80 Russmayer, H., Buchetics, M., Gruber, C., Valli, M., Grillitsch, K., Modarres, G., Guerrasio, R., Klavins, K., Neubauer, S., Drexler, H., et al. Systems-level organization of yeast methylotrophic lifestyle. BMC Biol, 13, 2015, 80.
81. 13C-labeling in the Methylobacterium extorquens AM1 metabolome using the two-dimensional mass cluster method and principal component analysis. J Chromatogr A 1432 (2016), 111–121.
82. 82 Bogorad, I.W., Chen, C.T., Theisen, M.K., Wu, T.Y., Schlenz, A.R., Lam, A.T., Liao, J.C., Building carbon–carbon bonds using a biocatalytic methanol condensation cycle. Proc Natl Acad Sci U S A 111 (2014), 15928–15933.
83. 83 Siegel, J.B., Smith, A.L., Poust, S., Wargacki, A.J., Bar-Even, A., Louw, C., Shen, B.W., Eiben, C.B., Tran, H.M., Noor, E., et al. Computational protein design enables a novel one-carbon assimilation pathway. Proc Natl Acad Sci U S A 112 (2015), 3704–3709.