From gene to biorefinery: Microbial β-etherases as promising biocatalysts for lignin valorization

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Picart, Pere ^a   De María, Pablo Domínguez ^b   Schallmey, Anett ^c  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b Sustainable Momentum   (Spain)

^c TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Biocatalysis; Biomass utilization; Biorefineries; Lignin; arylether cleavage; etherases

Indexed keywords

ALPHA O (BETA METHYLUMBELLIFERYL) ACETOVANILLONE; BACTERIAL ENZYME; BETA (2,6 METHOXYPHENOXY) ALPHA VERATRYLGLYCERONE; BETA (3,5 METHOXYPHENOXY) ALPHA VERATRYLGLYCERONE; BETA ETHERASE; BETA GUAIACYL ALPHA VERATRYLETHANONE; BETA GUAIACYL ALPHA VERATRYLGLYCERONE; CONIFERYL ALCOHOL; ETHER DERIVATIVE; GLUTATHIONE DEPENDENT BETA ETHERASE; GSH DEPENDENT GLUTATHIONE LYASE LIGNIN G; GUAIFENESIN; LIGNIN; LIGNIN E; LIGNIN F; LIGNIN P; LIGNOCELLULOSE; UNCLASSIFIED DRUG;

BIOCATALYSIS; BIOMASS PRODUCTION; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; NONHUMAN; SEQUENCE HOMOLOGY; SHORT SURVEY;

EID: 84946719915     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00916     Document Type: Short Survey

References (66)

1. Abdel-Hamid, A. M., Solbiati, J. O., and Cann, I. K. (2013). Insights into lignin degradation and its potential industrial applications. Adv. Appl. Microbiol. 82, 1-28. doi: 10.1016/B978-0-12-407679-2.00001-6
2. Adler, E. (1977). Lignin chemistry-Past, present and future. Wood Sci. Technol. 11, 169-218. doi: 10.1007/BF00365615
3. Ahmad, M., Roberts, J. N., Hardiman, E. M., Singh, R., Eltis, L. D., and Bugg, T. D. H. (2011). Identification of DypB from Rhodococcus jostii RHA1 as a lignin peroxidase. Biochemistry 50, 5096-5107. doi: 10.1021/bi101892z
4. Austin, A. T., and Ballare, C. L. (2010). Dual role of lignin in plant litter decomposition in terrestrial ecosystems. Proc. Natl. Acad. Sci. U.S.A. 107, 4618-4622. doi: 10.1073/pnas.0909396107
5. Brown, M. E., Barros, T., and Chang, M. C. (2012). Identification and characterization of a multifunctional dye peroxidase from a lignin-reactive bacterium. ACS Chem. Biol. 7, 2074-2081. doi: 10.1021/cb300383y
6. Brown, M. E., and Chang, M. C. (2014). Exploring bacterial lignin degradation. Curr. Opin. Chem. Biol. 19, 1-7. doi: 10.1016/j.cbpa.2013.11.015
7. Bugg, T. D. H., Ahmad, M., Hardiman, E. M., and Singh, R. (2011). The emerging role for bacteria in lignin degradation and bio-product formation. Curr. Opin. Biotechnol. 22, 394-400. doi: 10.1016/j.copbio.2010.10.009
8. Bugg, T. D. H., and Rahmanpour, R. (2015). Enzymatic conversion of lignin into renewable chemicals. Curr. Opin. Chem. Biol. 29, 10-17. doi: 10.1016/j.cbpa.2015.06.009
9. Camarero, S., Galletti, G. C., and Martínez, A. T. (1994). Preferential degradation of phenolic lignin units by two white rot fungi. Appl. Environ. Microbiol. 60, 4509-4516.
10. Cañas, A. I., and Camarero, S. (2010). Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol. Adv. 28, 694-705. doi: 10.1016/j.biotechadv.2010.05.002
11. Caramelo, L., Martínez, M. J., and Martínez, A. T. (1999). A search for ligninolytic peroxidases in the fungus Pleurotus eryngii involving a-keto-gamma-thiomethylbutyric acid and lignin model dimers. Appl. Environ. Microbiol. 65, 916-922.
12. Chatterjee, R., Zahn, K., Mitchell, K., and Liu, Y. (2012a). Ligf-type Enzymes for Bioconversion of Lignin-Derived Compounds. Patent number US20120196334.
13. Chatterjee, R., Zahn, K., Mitchell, K., and Liu, Y. (2012b). Bioproduction of Aromatic Chemicals from Lignin-Derived Compounds. Patent number WO2012036884A2.
14. Chen, Y. R., Sarkanen, S., and Wang, Y. Y. (2012). Lignin-degrading enzyme activities. Methods Mol. Biol. 908, 251-268. doi: 10.1007/978-1-61779-956-3_21
15. Cox, B. J., and Ekerdt, J. G. (2012). Depolymerization of oak wood lignin under mild conditions using the acidic ionic liquid 1-H-3-methylimidazolium chloride as both solvent and catalyst. Bioresour. Technol. 118, 584-588. doi: 10.1016/j.biortech.2012.05.012
16. Faix, O. (1991). Classification of lignins from different botanical origins by FTIR spectroscopy. Holzforschung 45, 21-27. doi: 10.1515/hfsg.1991.45.s1.21
17. Gall, D. L., Kim, H., Lu, F., Donohue, T. J., Noguera, D. R., and Ralph, J. (2014a). Stereochemical features of glutathione-dependent enzymes in the Sphingobium sp. strain SYK-6 β-aryl etherase pathway. J. Biol. Chem. 289, 8656-8667. doi: 10.1074/jbc.M113.536250
18. Gall, D. L., Ralph, J., Donohue, T. J., and Noguera, D. R. (2014b). A group of sequence-related sphingomonad enzymes catalyzes cleavage of β-aryl ether linkages in lignin β-guaiacyl and β-syringyl ether dimers. Environ. Sci. Technol. 48, 12454-12463. doi: 10.1021/es503886d
19. Gold, M. H., and Alic, M. (1993). Molecular biology of the lignin-degrading basidiomycete Phanerochaete chrysosporium. Microbiol. Rev. 57, 605-622.
20. Gold, M. H., Youngs, H. L., and Gelpke, M. D. (2000). Manganese peroxidase. Met. Ions Biol. Syst. 37, 559-586.
21. Gosselink, R. J. A., Teunissen, W., van Dam, J. E. G., de Jonk, E., Gellerstedt, G., Scott, E. L., et al. (2012). Lignin depolymerisation in supercritical carbon dioxide/acetone/water fluid for the production of aromatic chemicals. Bioresour. Technol. 106, 173-177. doi: 10.1016/j.biortech.2011.11.121
22. Hammel, K. E., Jensen, K. A., Mozuch, M. D., Landucci, L. L., Tien, M., and Pease, E. A. (1993). Ligninolysis by a purified lignin peroxidase. J. Biol. Chem. 268, 12274-12281.
23. Hendriks, A. T., and Zeeman, G. (2009). Pretreatments to enhance the digestibility of lignocellulosic biomass. Bioresour. Technol. 100, 10-18. doi: 10.1016/j.biortech.2008.05.027
24. Himmel, M. E., Ding, S., Johnson, D. K., Adney, W. S., Nimlos, M. R., Brady, J. W., et al. (2007). Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315, 804-807. doi: 10.1126/science.1137016
25. Jia, S., Cox, B. J., Guo, X., Zhang, Z. C., and Ekerdt, J. G. (2010). Cleaving the β-O-4 bonds of lignin model compounds in an acidic ionic liquid, 1-H-3-methylimidazolium chloride: an optional strategy for the degradation of lignin. ChemSusChem 24, 1078-1084. doi: 10.1002/cssc.201000112
26. Lancefield, C. S., Ojo, O. S., Tran, F., and Westwood, N. J. (2015). Isolation of functionalized phenolic monomers through selective oxidation and C-O bond cleavage of the β-O-4 linkages in lignin. Angew. Chem. Int. Ed. Engl. 54, 258-262. doi: 10.1002/anie.201409408
27. Lange, H., Decina, S., and Crestini, C. (2013). Oxidative upgrade of lignin-recent routes reviewed. Eur. Polym. J. 49, 1151-1173. doi: 10.1016/j.eurpolymj.2013.03.002
28. LaRoe, S. L., Wang, B., and Han, J. I. (2010). Isolation and characterization of a novel polycyclic aromatic hydrocarbon-degrading bacterium, Sphingopyxis sp. strain M2R2, capable of passive spreading motility through soil. Environ. Eng. Sci. 27, 505-512. doi: 10.1089/ees.2010.0054
29. Lavoie, J. M., Baré, W., and Bilodeau, M. (2011). Depolymerization of steam-treated lignin for the production of green chemicals. Bioresour. Technol. 102, 4917-4920. doi: 10.1016/j.biortech.2011.01.010
30. Lynd, L. R., Laser, M. S., Bransby, D., Dale, B. E., Davison, B., Hamilton, R., et al. (2008). How biotech can transform biofuels. Nat. Biotechnol. 26, 169-172. doi: 10.1038/nbt0208-169
31. Mai, C., Majcherczyk, A., and Huttermann, A. (2000). Chemo-enzymatic synthesis and characterization of graft copolymers from lignin and acrylic compounds. Enzyme Microb. Technol. 27, 167-175. doi: 10.1016/S0141-0229(00)00214-3
32. Martínez, A. T., Speranza, M., Ruiz-Dueñas, F. J., Ferreira, P., Camarero, S., Guillén, F., et al. (2005). Biodegradation of lignocellulosics: microbial, chemical and enzymatic aspects of the fungal attack of lignin. Int. Microbiol. 8, 195-204.
33. Masai, E., Ichimura, A., Sato, Y., Miyauchi, K., Katayama, Y., and Fukuda, M. (2003). Roles of the enantioselective glutathione S-transferases in cleavage of β-aryl ether. J. Bacteriol. 185, 1768-1775. doi: 10.1128/JB.185.6.1768-1775.2003
34. Masai, E., Katayama, Y., and Fukuda, M. (2007). Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds. Biosci. Biotechnol. Biochem. 71, 1-15. doi: 10.1271/bbb.60437
35. Masai, E., Katayama, Y., Kubota, S., Kawai, S., Yamasaki, M., and Morohoshi, N. (1993a). A bacterial enzyme degrading the model lignin compound β-etherase is a member of the glutathione-S-transferase superfamily. FEBS Lett. 323, 135-140. doi: 10.1016/0014-5793(93)81465-C
36. Masai, E., Kubota, S., Katayama, Y., Kawai, S., Yamasaki, M., and Morohoshi, N. (1993b). Characterization of the C a-dehydrogenase gene involved in the cleavage of β-aryl ether by Pseudomonas paucimobilis. Biosci. Biotechnol. Biochem. 57, 1655-1659. doi: 10.1271/bbb.57.1655
37. Masai, E., Katayama, Y., Nishikawa, S., and Fukuda, M. (1999). Characterization of Sphingomonas paucimobilis SYK-6 genes involved in degradation of lignin-related compounds. J. Ind. Microbiol. Biotechnol. 23, 364-373. doi: 10.1038/sj.jim.2900747
38. Masai, E., Katayama, Y., Nishikawa, S., Yamasaki, M., Morohoshi, N., and Haraguchi, T. (1989). Detection and localization of a new enzyme catalyzing the β-aryl ether cleavage in the soil bacterium (Pseudomonas paucimobilis SYK-6). FEBS Lett. 249, 348-352. doi: 10.1016/0014-5793(89)80656-8
39. Notomista, E., Pennacchio, F., Cafaro, V., Smaldone, G., Izzo, V., Troncone, L., et al. (2011). The marine isolate Novosphingobium sp. PP1Y shows specific adaptation to use the aromatic fraction of fuels as the sole carbon and energy source. Microb. Ecol. 61, 582-594. doi: 10.1007/s00248-010-9786-3
40. Otsuka, Y., Sonoki, T., Ikeda, S., Kajita, S., Nakamura, M., and Katayama, Y. (2003). Detection and characterization of a novel extracellular fungal enzyme that catalyzes the specific and hydrolytic cleavage of lignin guaiacylglycerol β-aryl ether linkages. Eur. J. Biochem. 270, 2353-2362. doi: 10.1046/j.1432-1033.2003.03545.x
41. Pandey, M. P., and Kim, C. S. (2011). Lignin depolymerization and conversion: a review of thermochemical methods. Chem. Eng. Technol. 34, 29-41. doi: 10.1002/ceat.201000270
42. Picart, P., Müller, C., Mottweiler, J., Wiermans, L., Bolm, C., Domínguez de María, P., et al. (2014). From gene towards selective biomass valorization: bacterial β-etherases with catalytic activity on lignin-like polymers. ChemSusChem. 7, 3164-3171. doi: 10.1002/cssc.201402465
43. Pollegioni, L., Tonin, F., and Rosini, E. (2015). Lignin-degrading enzymes. FEBS J. 282, 1190-1213. doi: 10.1111/febs.13224
44. Ragauskas, A. J., Beckham, G. T., Biddy, M. J., Chandra, R., Chen, F., Davis, M. F., et al. (2014). Lignin valorization: improving lignin processing in the biorefinery. Science 344, 1246843-1246843. doi: 10.1126/science.1246843
45. Ragauskas, A. J., Williams, C. K., Davison, B. H., Britovsek, G., Cairney, J., Eckert, C. A., et al. (2006). The path forward for biofuels and biomaterials. Science 311, 484-489. doi: 10.1126/science.1114736
46. Rahimi, A., Ulbrich, A., Coon, J. J., and Stahl, S. S. (2013). Formic-acid-induced depolymerization of oxidized lignin to aromatics. Nature 13, 249-252. doi: 10.1038/nature13867
47. Rahmanpour, R., and Bugg, T. D. H. (2015). Characterisation of Dyp-type peroxidases from Pseudomonas fluorescens Pf-5: oxidation of Mn(II) and polymeric lignin by Dyp1B. Arch. Biochem. Biophys. 574, 93-98. doi: 10.1016/j.abb.2014.12.022
48. Ralph, J., Akiyama, T., Kim, H., Lu, F., Schatz, P. F., Marita, J. M., et al. (2006). Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J. Biol. Chem. 281, 8843-8853. doi: 10.1074/jbc.M511598200
49. Ralph, J., Lundquist, K., Brunow, G., Lu, F., Kim, H., Schatz, P. F., et al. (2004). Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl propanoids. Phytochem. Rev. 3, 29-60. doi: 10.1023/B:PHYT.0000047809.65444.a4
50. Reiter, J., Strittmatter, H., Wiemann, L. O., Schieder, D., and Sieber, V. (2013). Enzymatic cleavage of lignin β-O-4 aryl ether bonds via net internal hydrogen transfer. Green Chem. 15, 1373-1381. doi: 10.1039/c3gc40295a
51. Sánchez, C. (2009). Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol. Adv. 27, 185-194. doi: 10.1016/j.biotechadv.2008.11.001
52. Sato, Y., Moriuchi, H., Hishiyama, S., Otsuka, Y., Oshima, K., Kasai, D., et al. (2009). Identification of three alcohol dehydrogenase genes involved in the stereospecific catabolism of arylglycerol-β-aryl ether by Sphingobium sp. strain SYK-6. Appl. Environ. Microbiol. 75, 5195-5201. doi: 10.1128/AEM.00880-09
53. Song, Q., Wang, F., and Xu, J. (2012). Hydrogenolysis of lignosulfonate into phenols over heterogeneous nickel catalysts. Chem. Commun. 48, 7019-7021. doi: 10.1039/c2cc31414b
54. Sonoki, T., Iimura, Y., Masai, E., Kajita, S., and Katayama, Y. (2002). Specific degradation of β-aryl ether linkage in synthetic lignin (dehydrogenative polymerizate) by bacterial enzymes of Sphingomonas paucimobilis SYK-6 produced in recombinant Escherichia coli. J. Wood Sci. 48, 429-433. doi: 10.1007/BF00770705
55. Srinvasan, V. R., Cary, J. W., Chon, Y., and Navra, K. E. (1987). Gene for Lignin Degradation and Uses Thereof. Patent number US4713336A.
56. Tanamura, K., Abe, T., Kamimura, N., Kasai, D., Hishiyama, S., Otsuka, Y., et al. (2011). Characterization of the third glutathione-S-transferase gene involved in enantioselective cleavage of the β-aryl ether by Sphingobium sp. strain SYK-6. Biosci. Biotechnol. Biochem. 75, 2404-2407. doi: 10.1271/bbb.110525
57. ten Have, R., and Teunissen, P. J. M. (2001). Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chem. Rev. 101, 3397-3413. doi: 10.1021/cr000115l
58. Tien, M., and Kirk, T. K. (1983). Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium birds. Science 221, 661-663. doi: 10.1126/science.221.4611.661
59. Toledano, A., Serrano, L., and Labidi, J. (2012). Organosolv lignin depolymerization with different base catalysts. J. Chem. Technol. Biotechnol. 87, 1593-1599. doi: 10.1002/jctb.3799
60. Vicuña, R. (1988). Bacterial degradation of lignin. Enzyme Microbiol. Technol. 10, 646-655. doi: 10.1016/0141-0229(88)90055-5
61. Wang, H., Tucker, M., and Ji, Y. (2013). Recent development in chemical depolymerization of lignin: a review. J. Appl. Chem. 2013, 1-9. doi: 10.1155/2013/838645
62. Wong, D. W. (2009). Structure and action mechanism of ligninolytic enzymes. Appl. Biochem. Biotechnol. 157, 174-209. doi: 10.1007/s12010-008-8279-z
63. Xia, Y., Min, H., Rao, G., Lv, Z. M., Liu, J., Ye, Y. F., et al. (2005). Isolation and characterization of phenanthrene-degrading Sphingomonas paucimobilis strain ZX4. Biodegradation 16, 393-402. doi: 10.1007/s10532-004-2412-7
64. Xu, W., Miller, S. J., Agrawal, P. K., and Jones, C. W. (2012). Depolymerization and hydrodeoxygenation of switchgrass lignin with formic acid. ChemSusChem. 5, 667-675. doi: 10.1002/cssc.201100695
65. Zakzeski, J., Bruijnincx, P. C. A., Jongerius, A. L., and Weckhuysen, B. M. (2010). The catalytic valorization of lignin for the production of renewable chemicals. Chem. Rev. 110, 3552-3599. doi: 10.1021/cr900354u
66. Zimmermann, W. (1990). Degradation of lignin by bacteria. J. Biotechnol. 13, 119-130. doi: 10.1016/0168-1656(90)90098-V