Applied Biological Chemistry

, Volume 61, Issue 1, pp 73–78 | Cite as

Thermodynamic analysis of MauG, a diheme oxygenase

  • Han-bin Kim
  • Sooim Shin
  • Moonsung Choi


MauG is a unique c-type diheme oxygenase. One heme of MauG is five-coordinate and solvent accessible with His53 as axial ligand, while the other heme of MauG is six-coordinate with His205 and Tyr294. MauG catalyzes posttranslational modification including oxygen insertion, cross-linkage of two tryptophan and oxidation of quinol to quinone of precursor methylamine dehydrogenase (preMADH) to form mature tryptophan tryptophylquinone (TTQ) which is one of protein-derived cofactors. Long-range remote catalysis of substrate is possible without direct contact between hemes of MauG and its substrate, preMADH. Although catalytic properties and mechanisms of MauG have been well studied, temperature dependence of MauG has never been reported yet. Therefore, the objective of this study was to perform thermodynamic analysis of MauG. ΔH° of 87.6 ± 6.7 kJ mol−1 and ΔS° of 232 ± 15.6 J mol−1 K−1 were directly measured for oxidized MauG in this study. Those results provide fundamental information on controlling electron transfer rates for biosynthesis of TTQ in MADH and are used as a good thermodynamic example study for other diheme systems.


C-type diheme enzyme MauG Oxygenase Thermodynamic parameters 



This work was supported by NRF Grants (2016R1C1B1008673 and 2016R1C1B2008836).


  1. 1.
    Davidson VL (2001) Pyrroloquinoline quinone (PQQ) from methanol dehydrogenase and tryptophan tryptophylquinone (TTQ) from methylamine dehydrogenase. Adv Protein Chem 58:95–140CrossRefGoogle Scholar
  2. 2.
    Husain M, Davidson VL (1985) An inducible periplasmic blue copper protein from paracoccus denitrificans. Purification, properties, and physiological role. J Biol Chem 260:14626–14629Google Scholar
  3. 3.
    Jensen LM, Sanishvili R, Davidson VL, Wilmot CM (2010) In crystallo posttranslational modification within a MauG/pre-methylamine dehydrogenase complex. Science 327:1392–1394CrossRefGoogle Scholar
  4. 4.
    Sono M, Roach MP, Coulter ED, Dawson JH (1996) Heme-containing oxygenases. Chem Rev 96:2841–2888CrossRefGoogle Scholar
  5. 5.
    Kovaleva EG, Neibergall MB, Chakrabarty S, Lipscomb JD (2007) Finding intermediates in the o2 activation pathways of non-heme iron oxygenases. Acc Chem Res 40:475–483CrossRefGoogle Scholar
  6. 6.
    Li XH, Fu R, Lee SY, Krebs C, Davidson VL, Liu AM (2008) A catalytic di-heme bis-Fe(iv) intermediate, alternative to an Fe(IV)=O porphyrin radical. Proc Natl Acad Sci USA 105:8597–8600CrossRefGoogle Scholar
  7. 7.
    Wang Y, Graichen ME, Liu A, Pearson AR, Wilmot CM, Davidson VL (2003) Maug, a novel diheme protein required for tryptophan tryptophylquinone biogenesis. Biochemistry US 42:7318–7325CrossRefGoogle Scholar
  8. 8.
    Wang Y, Li X, Jones LH, Pearson AR, Wilmot CM, Davidson VL (2005) Maug-dependent in vitro biosynthesis of tryptophan tryptophylquinone in methylamine dehydrogenase. J Am Chem Soc 127:8258–8259CrossRefGoogle Scholar
  9. 9.
    Pettigrew GW, Echalier A, Pauleta SR (2006) Structure and mechanism in the bacterial dihaem cytochrome c peroxidases. J Inorg Biochem 100:551–567CrossRefGoogle Scholar
  10. 10.
    Paoli M, Marles-Wright J, Smith A (2002) Structure-function relationships in heme-proteins. DNA Cell Biol 21:271–280CrossRefGoogle Scholar
  11. 11.
    Li X, Feng M, Wang Y, Tachikawa H, Davidson VL (2006) Evidence for redox cooperativity between c-type hemes of maug which is likely coupled to oxygen activation during tryptophan tryptophylquinone biosynthesis. Biochemistry 45:821–828CrossRefGoogle Scholar
  12. 12.
    Lee S, Shin S, Li X, Davidson VL (2009) Kinetic mechanism for the initial steps in maug-dependent tryptophan tryptophylquinone biosynthesis. Biochemistry US 48:2442–2447CrossRefGoogle Scholar
  13. 13.
    Shin S, Feng ML, Chen Y, Jensen LMR, Tachikawa H, Wilmot CM, Liu AM, Davidson VL (2011) The tightly bound calcium of maug is required for tryptophan tryptophylquinone cofactor biosynthesis. Biochemistry US 50:144–150CrossRefGoogle Scholar
  14. 14.
    Yonetani T, Anni H (1987) Yeast cytochrome c peroxidase. Coordination and spin states of heme prosthetic group. J Biol Chem 262:9547–9554Google Scholar
  15. 15.
    Hashimoto S, Teraoka J, Inubushi T, Yonetani T, Kitagawa T (1986) Resonance raman study on cytochrome c peroxidase and its intermediate. Presence of the Fe(IV)=O bond in compound ES and heme-linked ionization. J Biol Chem 261:11110–11118Google Scholar
  16. 16.
    Teraoka J, Kitagawa T (1981) Structural implication of the heme-linked ionization of horseradish peroxidase probed by the Fe-histidine stretching raman line. J Biol Chem 256:3969–3977Google Scholar
  17. 17.
    Wittung-Stafshede P (1999) Effect of redox state on unfolding energetics of heme proteins. BBA Protein Struct M 1432:401–405CrossRefGoogle Scholar
  18. 18.
    Cohen DS, Pielak GJ (1995) Entropic stabilization of cytochrome-c upon reduction. J Am Chem Soc 117:1675–1677CrossRefGoogle Scholar
  19. 19.
    Yukl ET, Liu F, Krzystek J, Shin S, Jensen LM, Davidson VL, Wilmot CM, Liu A (2013) Diradical intermediate within the context of tryptophan tryptophylquinone biosynthesis. Proc Natl Acad Sci USA 110:4569–4573CrossRefGoogle Scholar

Copyright information

© The Korean Society for Applied Biological Chemistry 2017

Authors and Affiliations

  1. 1.Interdisciplinary Program of Bioenergy and Biomaterials Graduate School (BK21 Plus Program), Department of Biotechnology and Bioengineering, College of EngineeringChonnam National UniversityGwangjuRepublic of Korea
  2. 2.Department of Optometry, College of Energy and BiotechnologySeoul National University of Science and TechnologySeoulRepublic of Korea

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