From lignin to nylon: Cascaded chemical and biochemical conversion using metabolically engineered Pseudomonas putida

Metabolic Engineering

Volumn 47, Issue , 2018, Pages 279-293

  Kohlstedt, Michael ^a   Starck, Sören ^a   Barton, Nadja ^a   Stolzenberger, Jessica ^a   Selzer, Mirjam ^a   Mehlmann, Kerstin ^c   Schneider, Roland ^c   Pleissner, Daniel ^c,d   Rinkel, Jan ^b   Dickschat, Jeroen S ^b   Venus, Joachim ^c   B J H van Duuren, Jozef ^a   Wittmann, Christoph ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c LEIBNIZ INSTITUTE FOR AGRICULTURAL ENGINEERING AND BIOECONOMY ATB   (Germany)

^d LEUPHANA UNIVERSITY OF LÜNEBURG   (Germany)

Author keywords

Bionylon; Catechol; Catechol dioxygenase; Cis,cis muconic acid; Cresol; Funneling; Hydrothermal conversion; Lignin; Methyl adipic acid; Methyl muconic acid, adipic acid; Nylon 6,6; Phenol; Phenol hydroxylase; Pseudomonas putida; Synthetic promoter library

Indexed keywords

AROMATIZATION; BACTERIA; BATCH DATA PROCESSING; LIGNIN; POLYAMIDES; RAYON;

ADIPIC ACIDS; BIONYLON; CATECHOL; CATECHOL DIOXYGENASES; CRESOL; FUNNELING; HYDROTHERMAL CONVERSION; MUCONIC ACID; NYLON-6 ,6; PHENOL HYDROXYLASE; PSEUDOMONAS PUTIDA;

PHENOLS;

ADENOSINE TRIPHOSPHATE; ADIPIC ACID; CATECHOL; CATECHOL 1,2 DIOXYGENASE; LIGNIN; META CRESOL; MUCONIC ACID; NYLON; ORTHO CRESOL; PARA CRESOL; PHENOL; PHENOL HYDROXYLASE; UNCLASSIFIED DRUG; SORBIC ACID;

ARTICLE; BACTERIAL GENOME; CELL ENERGY; DEPOLYMERIZATION; ENZYME ACTIVITY; HYDROGENATION; NONHUMAN; OXIDATION; POLYMERIZATION; PRIORITY JOURNAL; PSEUDOMONAS PUTIDA; TRANSGENIC MICROORGANISM; ANALOGS AND DERIVATIVES; GENETICS; METABOLIC ENGINEERING; METABOLISM;

BACTERIA; MUCONIC ACID; POLYAMIDES; RAYON;

LIGNIN; METABOLIC ENGINEERING; MICROORGANISMS, GENETICALLY-MODIFIED; NYLONS; PSEUDOMONAS PUTIDA; SORBIC ACID;

EID: 85045437318     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2018.03.003     Document Type: Article

References (65)

1. Alper, H., Fischer, C., Nevoigt, E., Stephanopoulos, G., Tuning genetic control through promoter engineering. Proc. Natl. Acad. Sci. USA 102 (2005), 12678–12683.
2. An, H.R., Park, H.H., Kim, E.S., Cloning and expression of thermophilic catechol 1,2-dioxygenase gene (catA) from Streptomyces setonii. FEMS Microbiol. Lett. 195 (2001), 17–22.
3. Atkinson, D.E., The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7 (1968), 4030–4034.
4. Bartilson, M., Nordlund, I., Shingler, V., Location and organization of the dimethylphenol catabolic genes of Pseudomonas CF600. Mol. Gen. Genet. 220 (1990), 294–300.
5. Barton, N., Horbal, L., Starck, S., Kohlstedt, M., Luzhetskyy, A., Wittmann, C., Enabling the valorization of guaiacol-based lignin: integrated chemical and biochemical production of cis,cis-muconic acid using metabolically engineered Amycolatopsis sp. ATCC 39116. Metab. Eng. 45 (2018), 200–2010.
6. Becker, J., Klopprogge, C., Zelder, O., Heinzle, E., Wittmann, C., Amplified expression of fructose 1,6-bisphosphatase in Corynebacterium glutamicum increases in vivo flux through the pentose phosphate pathway and lysine production on different carbon sources. Appl. Environ. Microbiol. 71 (2005), 8587–8596.
7. Becker, J., Zelder, O., Haefner, S., Schröder, H., Wittmann, C., From zero to hero–design-based systems metabolic engineering of Corynebacterium glutamicum for L-lysine production. Metab. Eng. 13 (2011), 159–168.
8. Beckham, G.T., Johnson, C.W., Karp, E.M., Salvachua, D., Vardon, D.R., Opportunities and challenges in biological lignin valorization. Curr. Opin. Biotechnol. 42 (2016), 40–53.
9. Belda, E., van Heck, R.G., Jose Lopez-Sanchez, M., Cruveiller, S., Barbe, V., Fraser, C., Klenk, H.P., Petersen, J., Morgat, A., Nikel, P.I., Vallenet, D., Rouy, Z., Sekowska, A., Martins Dos Santos, V.A., de Lorenzo, V., Danchin, A., Medigue, C., The revisited genome of Pseudomonas putida KT2440 enlightens its value as a robust metabolic chassis. Environ. Microbiol. 18 (2016), 3403–3424.
10. Benedetti, I., de Lorenzo, V., Nikel, P.I., Genetic programming of catalytic Pseudomonas putida biofilms for boosting biodegradation of haloalkanes. Metab. Eng. 33 (2016), 109–118.
11. Carraher, J.M., Pfennig, T., Rao, R.G., Shanks, B.H., Tessonnier, J.-P., Cis,cis-Muconic acid isomerization and catalytic conversion to biobased cyclic-C6-1,4-diacid monomers. Green Chem. 19 (2017), 3042–3050.
12. Chapman, A.G., Fall, L., Atkinson, D.E., Adenylate energy charge in Escherichia coli during growth and starvation. J. Bacteriol. 108 (1971), 1072–1086.
13. Chavarria, M., Nikel, P.I., Perez-Pantoja, D., de Lorenzo, V., The Entner-Doudoroff pathway empowers Pseudomonas putida KT2440 with a high tolerance to oxidative stress. Environ. Microbiol. 15 (2013), 1772–1785.
14. Chua, J.W., Hsieh, J.H., Oxidative bioconversion of toluene to 1,3-butadiene-1,4-dicarboxylic acid (cis,cis-muconic acid). World J. Microbiol. Biotechnol. 6 (1990), 127–143.
15. Ebert, B.E., Kurth, F., Grund, M., Blank, L.M., Schmid, A., Response of Pseudomonas putida KT2440 to increased NADH and ATP demand. Appl. Environ. Microbiol. 77 (2011), 6597–6605.
16. George, K.W., Hay, A., Less is more: reduced catechol production permits Pseudomonas putida F1 to grow on styrene. Microbiology 158 (2012), 2781–2788.
17. Guzik, U., Hupert-Kocurek, K., Sitnik, M., Wojcieszyńska, D., High activity catechol 1,2-dioxygenase from Stenotrophomonas maltophilia strain KB2 as a useful tool in cis,cis-muconic acid production. Antonie Van Leeuwenhoek 103 (2013), 1297–1307.
18. Jeenpadiphat, S., Mongkolpichayarak, I., Tungasmita, D.N., Catechol production from lignin by Al-doped mesoporous silica catalytic cracking. J. Anal. Appl. Pyrolysis 121 (2016), 318–328.
19. Jiménez, J.I., Pérez-Pantoja, D., Chavarría, M., Díaz, E., de Lorenzo, V., A second chromosomal copy of the catA gene endows Pseudomonas putida mt-2 with an enzymatic safety valve for excess of catechol. Environ. Microbiol. 16 (2014), 1767–1778.
20. Johnson, C.W., Abraham, P.E., Linger, J.G., Khanna, P., Hettich, R.L., Beckham, G.T., Eliminating a global regulator of carbon catabolite repression enhances the conversion of aromatic lignin monomers to muconate in Pseudomonas putida KT2440. Metab. Eng. Commum. 5 (2017), 19–25.
21. Johnson, C.W., Salvachúa, D., Khanna, P., Smith, H., Peterson, D.J., Beckham, G.T., Enhancing muconic acid production from glucose and lignin-derived aromatic compounds via increased protocatechuate decarboxylase activity. Metab. Eng. Commun. 3 (2016), 111–119.
22. Kind, S., Neubauer, S., Becker, J., Yamamoto, M., Völkert, M., Abendroth, G.V., Zelder, O., Wittmann, C., From zero to hero - production of bio-based nylon from renewable resources using engineered Corynebacterium glutamicum. Metab. Eng. 25 (2014), 113–123.
23. Kuepper, J., Dickler, J., Biggel, M., Behnken, S., Jager, G., Wierckx, N., Blank, L.M., Metabolic engineering of Pseudomonas putida KT2440 to produce anthranilate from glucose. Front. Microbiol., 6, 2015, 1310.
24. Kukor, J.J., Olsen, R.H., Complete nucleotide sequence of tbuD, the gene encoding phenol/cresol hydroxylase from Pseudomonas pickettii PKO1, and functional analysis of the encoded enzyme. J. Bacteriol. 174 (1992), 6518–6526.
25. 13C metabolic flux analysis and metabolic engineering of the rumen bacterium Basfia succiniciproducens. Metab. Eng. 44 (2017), 198–212.
26. Lieder, S., Nikel, P.I., de Lorenzo, V., Takors, R., Genome reduction boosts heterologous gene expression in Pseudomonas putida. Microb. Cell Fact., 14, 2015, 23.
27. Linger, J.G., Vardon, D.R., Guarnieri, M.T., Karp, E.M., Hunsinger, G.B., Franden, M.A., Johnson, C.W., Chupka, G., Strathmann, T.J., Pienkos, P.T., Beckham, G.T., Lignin valorization through integrated biological funneling and chemical catalysis. Proc. Natl. Acad. Sci. USA 111 (2014), 12013–12018.
28. Martínez-García, E., de Lorenzo, V., Engineering multiple genomic deletions in Gram-negative bacteria: analysis of the multi-resistant antibiotic profile of Pseudomonas putida KT2440. Environ. Microbiol. 13 (2011), 2702–2716.
29. Martínez-García, E., Jatsenko, T., Kivisaar, M., de Lorenzo, V., Freeing Pseudomonas putida KT2440 of its proviral load strengthens endurance to environmental stresses. Environ. Microbiol. 17 (2015), 76–90.
30. Martínez-García, E., Nikel, P.I., Aparicio, T., de Lorenzo, V., Pseudomonas 2.0: genetic upgrading of P. putida KT2440 as an enhanced host for heterologous gene expression. Microb. Cell Fact., 13, 2014, 159.
31. Matthiesen, J.E., Carraher, J.M., Vasiliu, M., Dixon, D.A., Tessonnier, J.-P., Electrochemical conversion of muconic acid to biobased diacid monomers. ACS Sustain. Chem. Eng. 4 (2016), 3575–3585.
32. Maxwell, P.C., 1988. Process for the Production of Muconic Acid, US4731328 A.
33. Nelson, K.E., Weinel, C., Paulsen, I.T., Dodson, R.J., Hilbert, H., Martins dos Santos, V.A., Fouts, D.E., Gill, S.R., Pop, M., Holmes, M., Brinkac, L., Beanan, M., DeBoy, R.T., Daugherty, S., Kolonay, J., Madupu, R., Nelson, W., White, O., Peterson, J., Khouri, H., Hance, I., Chris Lee, P., Holtzapple, E., Scanlan, D., Tran, K., Moazzez, A., Utterback, T., Rizzo, M., Lee, K., Kosack, D., Moestl, D., Wedler, H., Lauber, J., Stjepandic, D., Hoheisel, J., Straetz, M., Heim, S., Kiewitz, C., Eisen, J.A., Timmis, K.N., Dusterhoft, A., Tummler, B., Fraser, C.M., Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4 (2002), 799–808.
34. Neu, A-K., Pleissner, D., Mehlmann, K., Schneider, R., Puerta-Quintero, G.I., Venus, J., Fermentative utilization of coffee mucilage using Bacillus coagulans and investigation of down-stream processing of fermentation broth for optically pure L(+)-lactic acid production. Bioresour. Technol. 211 (2016), 398–405.
35. Nikel, P.I., Chavarría, M., Fuhrer, T., Sauer, U., de Lorenzo, V., Pseudomonas putida KT2440 strain metabolizes glucose through a cycle formed by enzymes of the Entner-Doudoroff, Embden-Meyerhof-Parnas, and pentose phosphate pathways. J. Biol. Chem. 290 (2015), 25920–25932.
36. Nordlund, I., Powlowski, J., Shingler, V., Complete nucleotide sequence and polypeptide analysis of multicomponent phenol hydroxylase from Pseudomonas sp. strain CF600. J. Bacteriol. 172 (1990), 6826–6833.
37. Pandey, M.P., Kim, C.S., Lignin depolymerization and conversion: a review of thermochemical methods. Chem. Eng. Technol. 34 (2011), 29–41.
38. Park, H.J., Kim, E.S., An inducible Streptomyces gene cluster involved in aromatic compound metabolism. FEMS Microbiol. Lett. 226 (2003), 151–157.
39. Park, W., Jeon, C.O., Cadillo, H., DeRito, C., Madsen, E.L., Survival of naphthalene-degrading Pseudomonas putida NCIB 9816-4 in naphthalene-amended soils: toxicity of naphthalene and its metabolites. Appl. Microbiol. Biotechnol. 64 (2004), 429–435.
40. Poblete-Castro, I., Becker, J., Dohnt, K., dos Santos, V.M., Wittmann, C., Industrial biotechnology of Pseudomonas putida and related species. Appl. Microbiol. Biotechnol. 93 (2012), 2279–2290.
41. Poblete-Castro, I., Binger, D., Rodrigues, A., Becker, J., Martins Dos Santos, V.A., Wittmann, C., In-silico-driven metabolic engineering of Pseudomonas putida for enhanced production of poly-hydroxyalkanoates. Metab. Eng. 15 (2013), 113–123.
42. Ragauskas, A.J., Beckham, G.T., Biddy, M.J., Chandra, R., Chen, F., Davis, M.F., Davison, B.H., Dixon, R.A., Gilna, P., Keller, M., Langan, P., Naskar, A.K., Saddler, J.N., Tschaplinski, T.J., Tuskan, G.A., Wyman, C.E., Lignin valorization: improving lignin processing in the biorefinery. Science, 344, 2014, 1246843.
43. Rinaldi, R., Jastrzebski, R., Clough, M.T., Ralph, J., Kennema, M., Bruijnincx, P.C.A., Weckhuysen, B.M., Paving the way for lignin valorisation: recent advances in bioengineering, biorefining and catalysis. Angew. Chem. Int. Ed. 55 (2016), 8164–8215.
44. Rodriguez, A., Salvachúa, D., Katahira, R., Black, B.A., Cleveland, N.S., Reed, M., Smith, H., Baidoo, E.E.K., Keasling, J.D., Simmons, B.A., Beckham, G.T., Gladden, J.M., Base-catalyzed depolymerization of solid lignin-rich streams enables microbial conversion. ACS Sustain. Chem. Eng. 5 (2017), 8171–8180.
45. Rohles, C.M., Giesselmann, G., Kohlstedt, M., Wittmann, C., Becker, J., Systems metabolic engineering of Corynebacterium glutamicum for the production of the carbon-5 platform chemicals 5-aminovalerate and glutarate. Microb. Cell Fact., 15, 2016, 154.
46. Rorrer, N.A., Dorgan, J.R., Vardon, D.R., Martinez, C.R., Yang, Y., Beckham, G.T., Renewable unsaturated polyesters from muconic acid. ACS Sustain. Chem. Eng. 4 (2016), 6867–6876.
47. Sambrook, J., Fritsch, E.F., Maniatis, T., Molecular cloning: A laboratory manual. 2nd ed., 1989, Cold Spring Harbor Laboratory Press, New York.
48. Schuler, J., Hornung, U., Kruse, A., Dahmen, N., Sauer, J., Hydrothermal liquefaction of lignin. J. Biomater. Nanobiotechnol. 8 (2017), 96–108.
49. Schweigert, N., Zehnder, A.J.B., Eggen, R.I.L., Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ. Microbiol. 3 (2001), 81–91.
50. Shingler, V., Franklin, F.C., Tsuda, M., Holroyd, D., Bagdasarian, M., Molecular analysis of a plasmid-encoded phenol hydroxylase from Pseudomonas CF600. J. Gen. Microbiol. 135 (1989), 1083–1092.
51. Silva-Rocha, R., de Lorenzo, V., A GFP-lacZ bicistronic reporter system for promoter analysis in environmental gram-negative bacteria. PLoS One, 7, 2012, e34675.
52. Silva-Rocha, R., de Lorenzo, V., The TOL network of Pseudomonas putida mt-2 processes multiple environmental inputs into a narrow response space. Environ. Microbiol. 15 (2013), 271–286.
53. Silva-Rocha, R., Martínez-García, E., Calles, B., Chavarría, M., Arce-Rodriguez, A., de Las Heras, A., Paez-Espino, A.D., Durante-Rodriguez, G., Kim, J., Nikel, P.I., Platero, R., de Lorenzo, V., The Standard European Vector Architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res. 41 (2013), D666–D675.
54. Sonoki, T., Morooka, M., Sakamoto, K., Otsuka, Y., Nakamura, M., Jellison, J., Goodell, B., Enhancement of protocatechuate decarboxylase activity for the effective production of muconate from lignin-related aromatic compounds. J. Biotechnol. 192:Pt A (2014), 71–77.
55. Sonoki, T., Takahashi, K., Sugita, H., Hatamura, M., Azuma, Y., Sato, T., Suzuki, S., Kamimura, N., Masai, E., Glucose-free cis,cis-muconic acid production via new metabolic designs corresponding to the heterogeneity of lignin. ACS Sustain. Chem. Eng. 6 (2018), 1256–1264.
56. Tiso, T., Sabelhaus, P., Behrens, B., Wittgens, A., Rosenau, F., Hayen, H., Blank, L.M., Creating metabolic demand as an engineering strategy in Pseudomonas putida - Rhamnolipid synthesis as an example. Metab. Eng. Commun. 3 (2016), 234–244.
57. van Duuren, J.B.J.H., Wijte, D., Karge, B., dos Santos, V.A., Yang, Y., Mars, A.E., Eggink, G., pH-stat fed-batch process to enhance the production of cis,cis-muconate from benzoate by Pseudomonas putida KT2440-JD1. Biotechnol. Prog. 28 (2012), 85–92.
58. van Duuren, J.B.J.H., Wijte, D., Leprince, A., Karge, B., Puchalka, J., Wery, J., Dos Santos, V.A., Eggink, G., Mars, A.E., Generation of a catR deficient mutant of P. putida KT2440 that produces cis,cis-muconate from benzoate at high rate and yield. J. Biotechnol. 156 (2011), 163–172.
59. Vardon, D.R., Franden, M.A., Johnson, C.W., Karp, E.M., Guarnieri, M.T., Linger, J.G., Salm, M.J., Strathmann, T.J., Beckham, G.T., Adipic acid production from lignin. Energ. Environ. Sci. 8 (2015), 617–628.
60. Vardon, D.R., Rorrer, N.A., Salvachua, D., Settle, A.E., Johnson, C.W., Menart, M.J., Cleveland, N.S., Ciesielski, P.N., Steirer, K.X., Dorgan, J.R., Beckham, G.T., Cis,cis-Muconic acid: separation and catalysis to bio-adipic acid for nylon-6,6 polymerization. Green Chem. 18 (2016), 3397–3413.
61. Wirth, B., Mumme, J., Anaerobic digestion of waste water from hydrothermal carbonization of corn silage. Appl. Bioenergy. 1 (2013), 1–10.
62. Wahyudiono, M.S., Goto, M., Recovery of phenolic compounds through the decomposition of lignin in near and supercritical water. Chem. Eng. Process. 47 (2008), 1609–1619.
63. Wittmann, C., Zeng, A.P., Deckwer, W.D., Growth inhibition by ammonia and use of a pH-controlled feeding strategy for the effective cultivation of Mycobacterium chlorophenolicum. Appl. Microbiol. Biotechnol. 44 (1995), 519–525.
64. Xie, N.Z., Liang, H., Huang, R.B., Xu, P., Biotechnological production of muconic acid: current status and future prospects. Biotechnol. Adv. 32 (2014), 615–622.
65. Zobel, S., Benedetti, I., Eisenbach, L., de Lorenzo, V., Wierckx, N., Blank, L.M., Tn7-based device for calibrated heterologous gene expression in Pseudomonas putida. ACS Synth. Biol. 4 (2015), 1341–1351.