JBIC Journal of Biological Inorganic Chemistry

, Volume 22, Issue 8, pp 1281–1293 | Cite as

Mn K-edge X-ray absorption studies of mononuclear Mn(III)–hydroxo complexes

  • Derek B. Rice
  • Gayan B. Wijeratne
  • Timothy A. JacksonEmail author
Original Paper


Mn K-edge X-ray absorption spectroscopy experiments were performed on the solid- and solution-phase samples of [MnII(dpaqR)](OTf) (R=H, Me) and [MnIII(OH)(dpaqR)](OTf). The extended X-ray absorption fine structure (EXAFS) data show distinct differences between the MnII and MnIII–OH complexes, with fits providing metric parameters in excellent agreement with values from X-ray crystallography and density functional theory (DFT) computations. Evaluation of the EXAFS data for solid-phase [MnIII(OH)(dpaq)](OTf) resolved a short Mn–OH bond distance of 1.79 Å; however, the short trans-amide nitrogen bond of the supporting ligand precluded the resolution of the Mn–OH bond distance in the corresponding solution-phase sample and for both [MnIII(OH)(dpaqMe)](OTf) samples. The edge energy also increases by approximately 2 eV from the MnII to the MnIII–OH complexes. Experimental pre-edge analysis shows the MnII complexes to have pre-edge areas comparable to the MnIII–OH complexes, despite the presence of the relatively short Mn–OH distance. Time-dependent density functional theory (TD-DFT) computations illustrate that Mn 3d–4p mixing, a primary contributor to pre-edge intensities, decreases by ~ 0.3% from the MnII to MnIII–OH complexes, which accounts for the very similar pre-edge areas. Collectively, this work shows that combined EXAFS and XANES analysis has great potential for identification of reactive MnIII–OH intermediates, such as those proposed in enzyme active sites.

Graphical Abstract


X-ray absorption spectroscopy Manganese Coordination chemistry Density functional theory Hydroxo ligands 



This work was supported by NSF Grant 1565661. Use of the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, is supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (including P41GM103393). The contents of this publication are solely the responsibility of the authors and do not necessarily represent the official views of NIGMS or NIH. Use of Beamline 2-2 at SSRL was partially supported by the National Synchrotron Light Source II, Brookhaven National Laboratory, under US Department of Energy Contract No. DE-SC0012704. XAS experiments were supported by the Case Western Reserve University Center for Synchrotron Biosciences NIH Grant, P30-EB-009998, from the National Institute of Biomedical Imaging and Bioengineering (NIBIB). We thank Dr. Erik Farquhar at NSLS for outstanding support of our XAS experiments and for helpful conversations.

Supplementary material

775_2017_1501_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1273 kb)


  1. 1.
    Bull C, Niederhoffer EC, Yoshida T, Fee JA (1991) J Am Chem Soc 113:4069–4076CrossRefGoogle Scholar
  2. 2.
    Rulíšek L, Ryde U (2006) J Phys Chem B 110:11511–11518CrossRefPubMedGoogle Scholar
  3. 3.
    Wennman A, Oliw EH, Karkehabadi S, Chen Y (2016) J Biol Chem 291:8130–8139CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Wennman A, Karkehabadi S, Oliw EH (2014) Arch Biochem Biophys 555–556:9–15CrossRefPubMedGoogle Scholar
  5. 5.
    Su C, Oliw EH (1998) J Biol Chem 273:13072CrossRefPubMedGoogle Scholar
  6. 6.
    Su C, Sahlin M, Oliw EH (2000) J Biol Chem 275:18830–18835CrossRefPubMedGoogle Scholar
  7. 7.
    Gaffney BJ, Su C, Oliw EH (2001) Appl Magn Reson 21:413–424CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Pecoraro VL, Hsieh WY (2008) Inorg Chem 47:1765–1778CrossRefPubMedGoogle Scholar
  9. 9.
    McEvoy JP, Brudvig GW (2006) Chem Rev 106:4455–4483CrossRefPubMedGoogle Scholar
  10. 10.
    Glockner C, Kern J, Broser M, Zouni A, Yachandra V, Yano J (2013) J Biol Chem 288:22607–22620CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Yano J, Yachandra V (2014) Chem Rev 114:4175–4205CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Rice DB, Wijeratne GB, Burr AD, Parham JD, Day VW, Jackson TA (2016) Inorg Chem 55:8110–8120CrossRefPubMedGoogle Scholar
  13. 13.
    Wijeratne GB, Corzine B, Day VW, Jackson TA (2014) Inorg Chem 53:7622–7634CrossRefPubMedGoogle Scholar
  14. 14.
    Coggins MK, Brines LM, Kovacs JA (2013) Inorg Chem 52:12383–12393CrossRefPubMedGoogle Scholar
  15. 15.
    Goldsmith CR, Cole AP, Stack TDP (2005) J Am Chem Soc 127:9904–9912CrossRefPubMedGoogle Scholar
  16. 16.
    Yano J, Kern J, Irrgang KD, Latimer MJ, Bergmann U, Glatzel P, Pushkar Y, Biesiadka J, Loll B, Sauer K, Messinger J, Zouni A, Yachandra VK (2005) Proc Natl Acad Sci U S A 102:12047–12052CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Frank P, Benfatto M, Qayyam M, Hedman B, Hodgson KO (2015) J Chem Phys 142:084310CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kau LS, Spira-Solomon DJ, Penner-Hahn JE, Hodgson KO, Solomon EI (1987) J Am Chem Soc 109:6433–6442CrossRefGoogle Scholar
  19. 19.
    Westre TE, Kennepohl P, DeWitt JG, Hedman B, Hodgson KO, Solomon EI (1997) J Am Chem Soc 119:6297–6314CrossRefGoogle Scholar
  20. 20.
    DeBeer George S, Petrenko T, Neese F (2008) J Phys Chem A 112:12936–12943CrossRefPubMedGoogle Scholar
  21. 21.
    DeBeer George S, Brant P, Solomon EI (2005) J Am Chem Soc 127:667–674CrossRefGoogle Scholar
  22. 22.
    Leto DF, Jackson TA (2014) Inorg Chem 53:6179–6194CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    England J, Martinho M, Farquhar ER, Frisch JR, Bominaar EL, Munck E, Que L Jr (2009) Angew Chem Int Ed Engl 48:3622–3626CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Jackson TA, Rohde JU, Seo MS, Sastri CV, DeHont R, Stubna A, Ohta T, Kitagawa T, Munck E, Nam W, Que L Jr (2008) J Am Chem Soc 130:12394–12407CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Rohde JU, Torelli S, Shan XP, Lim MH, Klinker EJ, Kaizer J, Chen K, Nam WW, Que L (2004) J Am Chem Soc 126:16750–16761CrossRefPubMedGoogle Scholar
  26. 26.
    Krewald V, Lassalle-Kaiser B, Boron TT 3rd, Pollock CJ, Kern J, Beckwith MA, Yachandra VK, Pecoraro VL, Yano J, Neese F, DeBeer S (2013) Inorg Chem 52:12904–12914CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Rees JA, Martin-Diaconescu V, Kovacs JA, DeBeer S (2015) Inorg Chem 54:6410–6422CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Roemelt M, Beckwith MA, Duboc C, Collomb MN, Neese F, DeBeer S (2012) Inorg Chem 51:680–687CrossRefPubMedGoogle Scholar
  29. 29.
    Ravel B, Newville M (2005) J Synchrotron Radiat 12:537–541CrossRefPubMedGoogle Scholar
  30. 30.
    Rehr JJ, Mustre de Leon J, Zabinsky SI, Albers RC (1991) J Am Chem Soc 113:5135–5140CrossRefGoogle Scholar
  31. 31.
    Wojdyr M (2010) J Appl Crystallogr 43:1126–1128CrossRefGoogle Scholar
  32. 32.
    Neese F (2012) Wiley Interdisciplinary reviews: computational molecular science. J Comput Sci 2:73–78Google Scholar
  33. 33.
    Becke AD (1986) J Chem Phys 84:4524–4529CrossRefGoogle Scholar
  34. 34.
    Perdew JP (1986) Phys Rev B 33:8822–8824CrossRefGoogle Scholar
  35. 35.
    Schäfer A, Horn H, Ahlrichs R (1992) J Chem Phys 97:2571–2577CrossRefGoogle Scholar
  36. 36.
    Schäfer A, Huber C, Ahlrichs R (1994) J Chem Phys 100:5829–5835CrossRefGoogle Scholar
  37. 37.
    Neese F (2003) J Comput Chem 24:1740–1747CrossRefPubMedGoogle Scholar
  38. 38.
    Sinnecker S, Rajendran A, Klamt A, Diedenhofen M, Neese F (2006) J Phys Chem A 110:2235–2245CrossRefPubMedGoogle Scholar
  39. 39.
    Hirata S, Head-Gordon M (1999) Chem Phys Lett 302:375–382CrossRefGoogle Scholar
  40. 40.
    Hirata S, Head-Gordon M (1999) Chem Phys Lett 314:291–299CrossRefGoogle Scholar
  41. 41.
    Becke AD (1993) J Chem Phys 98:5648–5652CrossRefGoogle Scholar
  42. 42.
    Lee C, Yang W, Parr RG (1988) Phys Rev B 37:785–789CrossRefGoogle Scholar
  43. 43.
    Weigend F, Ahlrichs R (2005) Phys Chem Chem Phys 7:3297–3305CrossRefPubMedGoogle Scholar
  44. 44.
    Lenthe EV, Baerends EJ, Snijders JG (1993) J Chem Phys 99:4597–4610CrossRefGoogle Scholar
  45. 45.
    van Wüllen C (1998) J Chem Phys 109:392–399CrossRefGoogle Scholar
  46. 46.
    Ciringh Y, Gordon-Wylie SW, Norman RE, Clark GR, Weintraub ST, Horwitz CP (1997) Inorg Chem 36:4968–4982CrossRefGoogle Scholar
  47. 47.
    Ching WM, Zhou A, Klein J, Fan R, Knizia G, Cramer CJ, Guo Y, Que L Jr (2017) Inorg Chem 56:11129–11140CrossRefPubMedGoogle Scholar
  48. 48.
    Leto DF, Ingram R, Day VW, Jackson TA (2013) Chem Commun 49:5378–5380CrossRefGoogle Scholar
  49. 49.
    Colmer HE, Howcroft AW, Jackson TA (2016) Inorg Chem 55:2055–2069CrossRefPubMedGoogle Scholar

Copyright information

© SBIC 2017

Authors and Affiliations

  • Derek B. Rice
    • 1
  • Gayan B. Wijeratne
    • 1
  • Timothy A. Jackson
    • 1
    Email author
  1. 1.Department of Chemistry and Center for Environmentally Beneficial CatalysisUniversity of KansasLawrenceUSA

Personalised recommendations