Perspectives for biocatalytic lignin utilization: cleaving 4-O-5 and Cα–Cβ bonds in dimeric lignin model compounds catalyzed by a promiscuous activity of tyrosinase

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Abstract

Background

In the biorefinery utilizing lignocellulosic biomasses, lignin decomposition to value-added phenolic derivatives is a key issue, and recently biocatalytic delignification is emerging owing to its superior selectivity, low energy consumption, and unparalleled sustainability. However, besides heme-containing peroxidases and laccases, information about lignolytic biocatalysts is still limited till date.

Results

Herein, we report a promiscuous activity of tyrosinase which is closely associated with delignification requiring high redox potentials (>1.4 V vs. normal hydrogen electrode [NHE]). The promiscuous activity of tyrosinase not only oxidizes veratryl alcohol, a commonly used nonphenolic substrate for assaying ligninolytic activity, to veratraldehyde but also cleaves the 4- O-5 and C _α–C _β bonds in 4-phenoxyphenol and guaiacyl glycerol-β-guaiacyl ether (GGE) that are dimeric lignin model compounds. Cyclic voltammograms additionally verified that the promiscuous activity oxidizes lignin-related high redox potential substrates.

Conclusion

These results might be applicable for extending the versatility of tyrosinase toward biocatalytic delignification as well as suggesting a new perspective for sustainable lignin utilization. Furthermore, the results provide insight for exploring the previously unknown promiscuous activities of biocatalysts much more diverse than ever thought before, thereby innovatively expanding the applicable area of biocatalysis.

Electronic supplementary material

The online version of this article (doi:10.1186/s13068-017-0900-3) contains supplementary material, which is available to authorized users.

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Most cited references 36

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Crystal structure of Agaricus bisporus mushroom tyrosinase: identity of the tetramer subunits and interaction with tropolone.

Henriëtte Rozeboom, H Wichers, Fabrizia Fusetti … (2011)

Tyrosinase catalyzes the conversion of phenolic compounds into their quinone derivatives, which are precursors for the formation of melanin, a ubiquitous pigment in living organisms. Because of its importance for browning reactions in the food industry, the tyrosinase from the mushroom Agaricus bisporus has been investigated in depth. In previous studies the tyrosinase enzyme complex was shown to be a H(2)L(2) tetramer, but no clues were obtained of the identities of the subunits, their mode of association, and the 3D structure of the complex. Here we unravel this tetramer at the molecular level. Its 2.3 Å resolution crystal structure is the first structure of the full fungal tyrosinase complex. The complex comprises two H subunits of ∼392 residues and two L subunits of ∼150 residues. The H subunit originates from the ppo3 gene and has a fold similar to other tyrosinases, but it is ∼100 residues larger. The L subunit appeared to be the product of orf239342 and has a lectin-like fold. The H subunit contains a binuclear copper-binding site in the deoxy-state, in which three histidine residues coordinate each copper ion. The side chains of these histidines have their orientation fixed by hydrogen bonds or, in the case of His85, by a thioether bridge with the side chain of Cys83. The specific tyrosinase inhibitor tropolone forms a pre-Michaelis complex with the enzyme. It binds near the binuclear copper site without directly coordinating the copper ions. The function of the ORF239342 subunits is not known. Carbohydrate binding sites identified in other lectins are not conserved in ORF239342, and the subunits are over 25 Å away from the active site, making a role in activity unlikely. The structures explain how calcium ions stabilize the tetrameric state of the enzyme.

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Identification of DypB from Rhodococcus jostii RHA1 as a lignin peroxidase.

Lindsay D. Eltis, J. Roberts, M. Ahmad … (2011)

Rhodococcus jostii RHA1, a polychlorinated biphenyl-degrading soil bacterium whose genome has been sequenced, shows lignin degrading activity in two recently developed spectrophotometric assays. Bioinformatic analysis reveals two unannotated peroxidase genes present in the genome of R. jostii RHA1 with sequence similarity to open reading frames in other lignin-degrading microbes. They are members of the Dyp peroxidase family and were annotated as DypA and DypB, on the basis of bioinformatic analysis. Assay of gene deletion mutants using a colorimetric lignin degradation assay reveals that a ΔdypB mutant shows greatly reduced lignin degradation activity, consistent with a role in lignin breakdown. Recombinant DypB protein shows activity in the colorimetric assay and shows Michaelis-Menten kinetic behavior using Kraft lignin as a substrate. DypB is activated by Mn(2+) by 5-23-fold using a range of assay substrates, and breakdown of wheat straw lignocellulose by recombinant DypB is observed over 24-48 h in the presence of 1 mM MnCl(2). Incubation of recombinant DypB with a β-aryl ether lignin model compound shows time-dependent turnover, giving vanillin as a product, indicating that C(α)-C(β) bond cleavage has taken place. This reaction is inhibited by addition of diaphorase, consistent with a radical mechanism for C-C bond cleavage. Stopped-flow kinetic analysis of the DypB-catalyzed reaction shows reaction between the intermediate compound I (397 nm) and either Mn(II) (k(obs) = 2.35 s(-1)) or the β-aryl ether (k(obs) = 3.10 s(-1)), in the latter case also showing a transient at 417 nm, consistent with a compound II intermediate. These results indicate that DypB has a significant role in lignin degradation in R. jostii RHA1, is able to oxidize both polymeric lignin and a lignin model compound, and appears to have both Mn(II) and lignin oxidation sites. This is the first detailed characterization of a recombinant bacterial lignin peroxidase.

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Crystallographic evidence that the dinuclear copper center of tyrosinase is flexible during catalysis.

Hironari Yoshitsu, Takanori Kumagai, Yasuyuki Matoba … (2006)

At high resolution, we determined the crystal structures of copper-bound and metal-free tyrosinase in a complex with ORF378 designated as a "caddie" protein because it assists with transportation of two CuII ions into the tyrosinase catalytic center. These structures suggest that the caddie protein covers the hydrophobic molecular surface of tyrosinase and interferes with the binding of a substrate tyrosine to the catalytic site of tyrosinase. The caddie protein, which consists of one six-strandedbeta-sheet and one alpha-helix, has no similarity with all proteins deposited into the Protein Data Bank. Although tyrosinase and catechol oxidase are classified into the type 3 copper protein family, the latter enzyme lacks monooxygenase activity. The difference in catalytic activity is based on the structural observations that a large vacant space is present just above the active center of tyrosinase and that one of the six His ligands for the two copper ions is highly flexible. These structural characteristics of tyrosinase suggest that, in the reaction that catalyzes the ortho-hydroxylation of monophenol, one of the two Cu(II) ions is coordinated by the peroxide-originated oxygen bound to the substrate. Our crystallographic study shows evidence that the tyrosinase active center formed by dinuclear coppers is flexible during catalysis.

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Author and article information

Contributors

Kyoungseon Min: min4605@kier.re.kr

Taewoo Yum: t7630@hanmail.net

Jiye Kim: 114001@kist.re.kr

Han Min Woo: hmwoo@kist.re.kr

Yunje Kim: yjkim@kist.re.kr

Byoung-In Sang: biosang@hanyang.ac.kr

Young Je Yoo: yjyoo@snu.ac.kr

Yong Hwan Kim: metalkim@unist.ac.kr

Youngsoon Um: +82-2-958-5819 , yum@kist.re.kr

Journal

Journal ID (nlm-ta): Biotechnol Biofuels

Journal ID (iso-abbrev): Biotechnol Biofuels

Title: Biotechnology for Biofuels

Publisher: BioMed Central (London )

ISSN (Electronic): 1754-6834

Publication date (Electronic): 11 September 2017

Publication date PMC-release: 11 September 2017

Publication date Collection: 2017

Volume: 10

Electronic Location Identifier: 212

Affiliations

[1 ]ISNI 0000000121053345, GRID grid.35541.36, Clean Energy Research Center, , Korea Institute of Science and Technology (KIST), ; Seoul, 02792 Republic of Korea

[2 ]ISNI 0000 0004 0381 814X, GRID grid.42687.3f, School of Energy and Chemical Engineering, , Ulsan National Institute of Science and Technology (UNIST), ; Ulsan, 44919 Republic of Korea

[3 ]ISNI 0000 0001 1364 9317, GRID grid.49606.3d, Department of Chemical Engineering, , Hanyang University, ; Seoul, 04763 Republic of Korea

[4 ]ISNI 0000 0004 0470 5905, GRID grid.31501.36, School of Chemical and Biological Engineering, , Seoul National University, ; Seoul, 08826 Republic of Korea

[5 ]ISNI 0000 0001 0691 7707, GRID grid.418979.a, Present Address: Gwangju Bioenergy Research Center, , Korea Institute of Energy Research (KIER), ; Daejeon, 34129 Republic of Korea

[6 ]ISNI 0000 0001 2181 989X, GRID grid.264381.a, Present Address: Department of Food Sciencen and Biotechnology, , Sungkyunkwan University, ; Suwon, 16419 Republic of Korea

Article

Publisher ID: 900

DOI: 10.1186/s13068-017-0900-3

PMC ID: 5594458

PubMed ID: 28912833

SO-VID: 42c3d221-3302-41ca-bd3f-69c02fc8063e

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 29 May 2017

Date accepted : 5 September 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;

Award ID: NRF-2009-C1AAA001-0093286

Award Recipient : Youngsoon Um

Funded by: FundRef http://dx.doi.org/10.13039/501100003662, Korea Evaluation Institute of Industrial Technology;

Award ID: 10049675

Award Recipient : Yong Hwan Kim

Funded by: FundRef http://dx.doi.org/10.13039/501100008783, National Research Council of Science and Technology;

Award ID: CAP-11-04-KIST

Award Recipient : Youngsoon Um

Custom metadata

ScienceOpen disciplines: Biotechnology

Keywords: sustainable lignin utilization,tyrosinase,promiscuous activity,4-phenoxyphenol,guaiacyl glycerol-β-guaiacyl ether (gge)

Data availability:

ScienceOpen disciplines: Biotechnology

Keywords: sustainable lignin utilization, tyrosinase, promiscuous activity, 4-phenoxyphenol, guaiacyl glycerol-β-guaiacyl ether (gge)