Comprehensive Sequence-Flux Mapping of a Levoglucosan Utilization Pathway in E. coli

ACS Synthetic Biology

Volumn 4, Issue 11, 2015, Pages 1235-1243

  Klesmith, Justin R ^a   Bacik, John Paul ^b   Michalczyk, Ryszard ^b   Whitehead, Timothy A ^c,d  

^a Michigan State University   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c Michigan State University   (United States)

^d Michigan State University   (United States)

Author keywords

biomass conversion; deep mutational scanning; fast pyrolysis; metabolic engineering; protein design

Indexed keywords

LEVOGLUCOSAN; 1,6-ANHYDRO-BETA-GLUCOPYRANOSE; GLUCOSE; PHOSPHOTRANSFERASE;

ARTICLE; CARBON SOURCE; CELL GROWTH; CELL LYSATE; ENZYME ACTIVITY; ENZYME STABILITY; ESCHERICHIA COLI; GAIN OF FUNCTION MUTATION; HYDROGEN BOND; MICROBIAL GROWTH; NONHUMAN; PRIORITY JOURNAL; THERMOSTABILITY; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; BIOCATALYSIS; BIOMASS; ENZYMOLOGY; GENETICS; METABOLISM; SYNTHETIC BIOLOGY;

BIOCATALYSIS; BIOMASS; ENZYME STABILITY; ESCHERICHIA COLI; GLUCOSE; PHOSPHOTRANSFERASES; SYNTHETIC BIOLOGY;

EID: 84947968739     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.5b00131     Document Type: Article

References (48)

1. Lee, J. W., Na, D., Park, J. M., Lee, J., Choi, S., and Lee, S. Y. (2012) Systems metabolic engineering of microorganisms for natural and non-natural chemicals Nat. Chem. Biol. 8, 536-546 10.1038/nchembio.970
2. Paddon, C. J., Westfall, P. J., Pitera, D. J., Benjamin, K., Fisher, K., McPhee, D., Leavell, M. D., Tai, A., Main, A., Eng, D., Polichuk, D. R., Teoh, K. H., Reed, D. W., Treynor, T., Lenihan, J., Fleck, M., Bajad, S., Dang, G., Dengrove, D., Diola, D., Dorin, G., Ellens, K. W., Fickes, S., Galazzo, J., Gaucher, S. P., Geistlinger, T., Henry, R., Hepp, M., Horning, T., Iqbal, T., Jiang, H., Kizer, L., Lieu, B., Melis, D., Moss, N., Regentin, R., Secrest, S., Tsuruta, H., Vazquez, R., Westblade, L. F., Xu, L., Yu, M., Zhang, Y., Zhao, L., Lievense, J., Covello, P. S., Keasling, J. D., Reiling, K. K., Renninger, N. S., and Newman, J. D. (2013) High-level semi-synthetic production of the potent antimalarial artemisinin Nature 496, 528-532 10.1038/nature12051
3. Chang, M. C. Y., Eachus, R. A., Trieu, W., Ro, D. K., and Keasling, J. D. (2007) Engineering Escherichia coli for production of functionalized terpenoids using plant P450s Nat. Chem. Biol. 3, 274-277 10.1038/nchembio875
4. Yim, H., Haselbeck, R., Niu, W., Pujol-Baxley, C., Burgard, A., Boldt, J., Khandurina, J., Trawick, J. D., Osterhout, R. E., Stephen, R., Estadilla, J., Teisan, S., Schreyer, H. B., Andrae, S., Yang, T. H., Lee, S. Y., Burk, M. J., and Van Dien, S. (2011) Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol Nat. Chem. Biol. 7, 445-452 10.1038/nchembio.580
5. Zhang, K., Li, H., Cho, K. M., and Liao, J. C. (2010) Expanding metabolism for total biosynthesis of the nonnatural amino acid L-homoalanine Proc. Natl. Acad. Sci. U. S. A. 107, 6234-6239 10.1073/pnas.0912903107
6. Zhang, K., Sawaya, M. R., Eisenberg, D. S., and Liao, J. C. (2008) Expanding metabolism for biosynthesis of nonnatural alcohols Proc. Natl. Acad. Sci. U. S. A. 105, 20653-20658 10.1073/pnas.0807157106
7. Zelcbuch, L., Antonovsky, N., Bar-Even, A., Levin-Karp, A., Barenholz, U., Dayagi, M., Liebermeister, W., Flamholz, A., Noor, E., Amram, S., Brandis, A., Bareia, T., Yofe, I., Jubran, H., and Milo, R. (2013) Spanning high-dimensional expression space using ribosome-binding site combinatorics Nucleic Acids Res. 41, e98 10.1093/nar/gkt151
8. Lee, M. E., Aswani, A., Han, A. S., Tomlin, C. J., and Dueber, J. E. (2013) Expression-level optimization of a multi-enzyme pathway in the absence of a high-throughput assay Nucleic Acids Res. 41, 10668-10678 10.1093/nar/gkt809
9. Latimer, L. N., Lee, M. E., Medina-Cleghorn, D., Kohnz, R. A., Nomura, D. K., and Dueber, J. E. (2014) Employing a combinatorial expression approach to characterize xylose utilization in Saccharomyces cerevisiae Metab. Eng. 25, 20-29 10.1016/j.ymben.2014.06.002
10. Du, J., Yuan, Y. B., Si, T., Lian, J. Z., and Zhao, H. M. (2012) Customized optimization of metabolic pathways by combinatorial transcriptional engineering Nucleic Acids Res. 40, e142 10.1093/nar/gks549
11. Woo, H. M., Murray, G. W., Batth, T. S., Prasad, N., Adams, P. D., Keasling, J. D., Petzold, C. J., and Lee, T. S. (2013) Application of targeted proteomics and biological parts assembly in E. coli to optimize the biosynthesis of an anti-malarial drug precursor, amorpha-4,11-diene Chem. Eng. Sci. 103, 21-28 10.1016/j.ces.2013.04.033
12. Bond-Watts, B. B., Bellerose, R. J., and Chang, M. C. Y. (2011) Enzyme mechanism as a kinetic control element for designing synthetic biofuel pathways Nat. Chem. Biol. 7, 222-227 10.1038/nchembio.537
13. Leonard, E., Ajikumar, P. K., Thayer, K., Xiao, W.-H., Mo, J. D., Tidor, B., Stephanopoulos, G., and Prather, K. L. J. (2010) Combining metabolic and protein engineering of a terpenoid biosynthetic pathway for overproduction and selectivity control Proc. Natl. Acad. Sci. U. S. A. 107, 13654-13659 10.1073/pnas.1006138107
14. Araya, C. L. and Fowler, D. M. (2011) Deep mutational scanning: assessing protein function on a massive scale Trends Biotechnol. 29, 435-442 10.1016/j.tibtech.2011.04.003
15. Fowler, D. M., Araya, C. L., Fleishman, S. J., Kellogg, E. H., Stephany, J. J., Baker, D., and Fields, S. (2010) High-resolution mapping of protein sequence-function relationships Nat. Methods 7, 741-746 10.1038/nmeth.1492
16. Kowalsky, C. A., Klesmith, J. R., Stapleton, J. A., Kelly, V., Reichkitzer, N., and Whitehead, T. A. (2015) High-resolution sequence-function mapping of full-length proteins PLoS One 10, e0118193 10.1371/journal.pone.0118193
17. Whitehead, T. A., Chevalier, A., Song, Y., Dreyfus, C., Fleishman, S. J., De Mattos, C., Myers, C. A., Kamisetty, H., Blair, P., Wilson, I. A., and Baker, D. (2012) Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing Nat. Biotechnol. 30, 543-548 10.1038/nbt.2214
18. Roscoe, B. P., Thayer, K. M., Zeldovich, K. B., Fushman, D., and Bolon, D. N. (2013) Analyses of the effects of all ubiquitin point mutants on yeast growth rate J. Mol. Biol. 425, 1363-1377 10.1016/j.jmb.2013.01.032
19. Fowler, D. M. and Fields, S. (2014) Deep mutational scanning: a new style of protein science Nat. Methods 11, 801-807 10.1038/nmeth.3027
20. Walkiewicz, K., Benitez Cardenas, A. S., Sun, C., Bacorn, C., Saxer, G., and Shamoo, Y. (2012) Small changes in enzyme function can lead to surprisingly large fitness effects during adaptive evolution of antibiotic resistance Proc. Natl. Acad. Sci. U. S. A. 109, 21408-21413 10.1073/pnas.1209335110
21. Firnberg, E., Labonte, J. W., Gray, J. J., and Ostermeier, M. (2014) A Comprehensive, High-Resolution Map of a Genes Fitness Landscape Mol. Biol. Evol. 31, 1581-1592 10.1093/molbev/msu081
22. Stiffler, M. A., Hekstra Doeke, R., and Ranganathan, R. (2015) Evolvability as a Function of Purifying Selection in TEM-1 β-Lactamase Cell 160, 882-892 10.1016/j.cell.2015.01.035
23. Kosuri, S., Goodman, D. B., Cambray, G., Mutalik, V. K., Gao, Y., Arkin, A. P., Endy, D., and Church, G. M. (2013) Composability of regulatory sequences controlling transcription and translation in Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 110, 14024-14029 10.1073/pnas.1301301110
24. Noderer, W. L., Flockhart, R. J., Bhaduri, A., Diaz de Arce, A. J., Zhang, J., Khavari, P. A., and Wang, C. L. (2014) Quantitative analysis of mammalian translation initiation sites by FACS-seq Mol. Syst. Biol. 10, 748 10.15252/msb.20145136
25. Antal, M. J. and Varhegyi, G. (1995) Cellulose Pyrolysis Kinetics-the Current State Knowledge Ind. Eng. Chem. Res. 34, 703-717 10.1021/ie00042a001
26. Bennett, N. M., Helle, S. S., and Duff, S. J. B. (2009) Extraction and hydrolysis of levoglucosan from pyrolysis oil Bioresour. Technol. 100, 6059-6063 10.1016/j.biortech.2009.06.067
27. Prosen, E. M., Radlein, D., Piskorz, J., Scott, D. S., and Legge, R. L. (1993) Microbial Utilization of Levoglucosan in Wood Pyrolysate as a Carbon and Energy-Source Biotechnol. Bioeng. 42, 538-541 10.1002/bit.260420419
28. Jarboe, L. R., Wen, Z. Y., Choi, D. W., and Brown, R. C. (2011) Hybrid thermochemical processing: fermentation of pyrolysis-derived bio-oil Appl. Microbiol. Biotechnol. 91, 1519-1523 10.1007/s00253-011-3495-9
29. Dai, J., Yu, Z., He, Y., Zhang, L., Bai, Z., Dong, Z., Du, Y., and Zhang, H. (2009) Cloning of a novel levoglucosan kinase gene from Lipomyces starkeyi and its expression in Escherichia coli World J. Microbiol. Biotechnol. 25, 1589-1595 10.1007/s11274-009-0048-9
30. Bacik, J. P., Klesmith, J. R., Whitehead, T. A., Jarboe, L. R., Unkefer, C. J., Mark, B. L., and Michalczyk, R. (2015) Producing glucose-6-phosphate from cellulosic biomass: structural insights into levoglucosan bioconversion J. Biol. Chem. 10.1074/jbc.M115.674614
31. Layton, D. S., Ajjarapu, A., Choi, D. W., and Jarboe, L. R. (2011) Engineering ethanologenic Escherichia coli for levoglucosan utilization Bioresour. Technol. 102, 8318-8322 10.1016/j.biortech.2011.06.011
32. Bienick, M. S., Young, K. W., Klesmith, J. R., Detwiler, E. E., Tomek, K. J., and Whitehead, T. A. (2014) The interrelationship between promoter strength, gene expression, and growth rate PLoS One 9, e109105 10.1371/journal.pone.0109105
33. Davis, J. H., Rubin, A. J., and Sauer, R. T. (2011) Design, construction and characterization of a set of insulated bacterial promoters Nucleic Acids Res. 39, 1131-1141 10.1093/nar/gkq810
34. Firnberg, E. and Ostermeier, M. (2012) PFunkel: efficient, expansive, user-defined mutagenesis PLoS One 7, e52031 10.1371/journal.pone.0052031
35. Kwon, W. S., Da Silva, N. A., and Kellis, J. T. (1996) Relationship between thermal stability, degradation rate and expression yield of barnase variants in the periplasm of Escherichia coli Protein Eng., Des. Sel. 9, 1197-1202 10.1093/protein/9.12.1197
36. Parsell, D. A. and Sauer, R. T. (1989) The structural stability of a protein is an important determinant of its proteolytic susceptibility in Escherichia coli J. Biol. Chem. 264, 7590-7595
37. Bloom, J. D., Labthavikul, S. T., Otey, C. R., and Arnold, F. H. (2006) Protein stability promotes evolvability Proc. Natl. Acad. Sci. U. S. A. 103, 5869-5874 10.1073/pnas.0510098103
38. Romero, P. A. and Arnold, F. H. (2009) Exploring protein fitness landscapes by directed evolution Nat. Rev. Mol. Cell Biol. 10, 866-876 10.1038/nrm2805
39. Tokuriki, N. and Tawfik, D. S. (2009) Stability effects of mutations and protein evolvability Curr. Opin. Struct. Biol. 19, 596-604 10.1016/j.sbi.2009.08.003
40. Solomon, K. V., Moon, T. S., Ma, B., Sanders, T. M., and Prather, K. L. J. (2013) Tuning Primary Metabolism for Heterologous Pathway Productivity ACS Synth. Biol. 2, 126-135 10.1021/sb300055e
41. Kadner, R. J., Murphy, G. P., and Stephens, C. M. (1992) Two mechanisms for growth inhibition by elevated transport of sugar phosphates in Escherichia coli J. Gen. Microbiol. 138, 2007-2014 10.1099/00221287-138-10-2007
42. Kuhlman, B. and Baker, D. (2000) Native protein sequences are close to optimal for their structures Proc. Natl. Acad. Sci. U. S. A. 97, 10383-10388 10.1073/pnas.97.19.10383
43. Fleishman, S. J., Leaver-Fay, A., Corn, J. E., Strauch, E.-M., Khare, S. D., Koga, N., Ashworth, J., Murphy, P., Richter, F., Lemmon, G., Meiler, J., and Baker, D. (2011) RosettaScripts: A Scripting Language Interface to the Rosetta Macromolecular Modeling Suite PLoS One 6, e20161 10.1371/journal.pone.0020161
44. Burgard, A. P., Pharkya, P., and Maranas, C. D. (2003) Optknock: A bilevel programming framework for identifying gene knockout strategies for microbial strain optimization Biotechnol. Bioeng. 84, 647-657 10.1002/bit.10803
45. Trinh, C. T., Unrean, P., and Srienc, F. (2008) Minimal Escherichia coli Cell for the Most Efficient Production of Ethanol from Hexoses and Pentoses Appl. Environ. Microbiol. 74, 3634-3643 10.1128/AEM.02708-07
46. Tang, S.-Y. and Cirino, P. C. (2011) Design and Application of a Mevalonate-Responsive Regulatory Protein Angew. Chem., Int. Ed. 50, 1084-1086 10.1002/anie.201006083
47. Stapleton, J. A., Kim, J., Hamilton, J. P., Wu, M., Irber, L. C., Maddamsetti, R., Briney, B., Newton, L., Burton, D. R., Brown, C. T., Chan, C., Buell, C. R., and Whitehead, T. A. (2015) Haplotype-phased synthetic long reads from short-read sequencing bioRxiv 10.1101/022897
48. Hong, L., Hong, S., Wong, H., Aw, P., Cheng, Y., Wilm, A., de Sessions, P., Lim, S., Nagarajan, N., Hibberd, M., Quake, S., and Burkholder, W. (2014) BAsE-Seq: a method for obtaining long viral haplotypes from short sequence reads Genome Biology 15, 517 10.1186/s13059-014-0517-9