A new route to iron carbonyls has enabled synthesis of 57Fe-​labeled [NiFe] hydrogenase mimic (OC)​357Fe(pdt)​Ni(dppe) (pdt = 1,​3-​propanedithiolate)​. Its study by nuclear resonance vibrational spectroscopy revealed Ni-​57Fe vibrations, as confirmed by calcns. The modes are absent for [(OC)​357Fe(pdt)​Ni(dppe)​]​+, which lacks Ni-​57Fe bonding, underscoring the utility of the analyses in identifying metal-​metal interactions

Cramer, Stephen P.

Gee, Leland B.

Kaupp, Martin

Meier, Florian

Pelmenschikov, Vladimir

Rauchfuss, Thomas B.

Schilter, David

Wang, Hongxin

Yoda, Yoshitaka

Chemical Communications

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This journal is©The Royal Society of Chemistry 2014 Chem. Commun., 2014, 50, 13469--13472 | 13469Cite this:Chem. Commun., 2014,50, 13469Synthesis and vibrational spectroscopyof 57Fe-labeled models of [NiFe] hydrogenase: firstdirect observation of a nickel–iron interaction†David Schilter,*a Vladimir Pelmenschikov,b Hongxin Wang,cd Florian Meier,bLeland B. Gee,c Yoshitaka Yoda,e Martin Kaupp,b Thomas B. Rauchfussa andStephen P. Cramer*cdA new route to iron carbonyls has enabled synthesis of 57Fe-labeled[NiFe] hydrogenase mimic (OC)357Fe(pdt)Ni(dppe). Its study by nuclearresonance vibrational spectroscopy revealed Ni–57Fe vibrations, asconfirmed by calculations. The modes are absent for [(OC)357Fe(pdt)-Ni(dppe)]+, which lacks Ni–57Fe bonding, underscoring the utility ofthe analyses in identifying metal–metal interactions.Despite our extremely low atmospheric concentration of dihydrogen(B1 ppm), this substrate is a key metabolite of many anaerobicbacteria.1 In such living systems can be found the most prevalentenzymes for hydrogen processing, the nickel–iron hydrogenases([NiFe]–H2ases).1,2 These electrocatalysts specifically mediate theredox reaction H2 " 2H+ + 2e at several hundred turnoversper second.3 Their heterobimetallic active sites exist in several states,some of which are summarized below (Fig. 1, left and centre).The active sites feature Ni bound to four cysteinato residues,two of which bridge to an Fe(CO)(CN)2 fragment. In the Ni–Cstate, Ni(III)Fe(II) centres bind a bridging hydride (H), reductiveelimination of which affords Ni–L.4 Thus, H+ is abstracted by aterminal cys ligand (Fig. 1, centre top), leaving a Ni(I)Fe(II) corewith a 2e bond between the metals.4The use of vibrational spectroscopy to study [NiFe]–H2ase isconvenient in that its active site features chromophores easilyidentifiable by such techniques. Spectral analyses are often aidedby comparison to data from synthetic models5 whose structures arewell understood. Specificity for 57Fe-coupled modes is affordedby nuclear resonance vibrational spectroscopy (NRVS, vide infra).This has recently enabled observation of characteristic Fe–CN/Fe–CO bending and stretching modes in [NiFe]–H2ase (Ni–A andNi–R) and the Fe subsite model [Fe(benzenedithiolato)(CN)2CO]2.6However, no NRVS studies have reported on metal–metal bonding,which is expected for low-valent clusters like Ni–L and itsmodels.4,7A near-complete [NiFe]–H2ase mimic is the Ni(II)Fe(I) species[(OC)3Fe(pdt)Ni(dppe)]+ ([1]+, pdt2 = S(CH2)3S; dppe = 1,2-bis-(diphenylphosphino)ethane), a model for Ni–L, albeit with metaloxidation states reversed (Fig. 1, right).8 This S = 1/2 model isprepared from (OC)3Fe(pdt)Ni(dppe) (1),9 itself the subject of densityfunctional theory (DFT) and resonance Raman investigations.10Disclosed here is methodology for 57Fe-labeled prototypes[(OC)357Fe(pdt)Ni(dppe)]0/+ ([1]0/+), enabling the study of metal–metal bonding with NRVS.The Ni(I)Fe(I) complex 1 is usually accessed by interaction of(pdt)Ni(dppe) with an Fe carbonyl such as Fe2(CO)9 or Fe(CO)4I2.11–14The precursor to these, Fe(CO)5, is not conveniently prepared fromelemental Fe, a factor that necessitated a new route adaptable to57Fe incorporation. Thus, metallic Fe was converted to the organo-soluble FeI2 source Fe2I4(iPrOH)4,15 which, upon combination with(pdt)Ni(dppe), gave the known diiodide I2Fe(pdt)Ni(dppe).14 Whilethe diiodide does not bind CO in CH2Cl2, when treated withAgBF4 it converts to the putative electrophile ‘[IFe(pdt)Ni(dppe)]+’(or perhaps its dimer), which undergoes carbonylation to affordFig. 1 Key [NiFe]–H2ase states (left and centre) and two model complexes(right).a Department of Chemistry, University of Illinois at Urbana-Champaign, Urbana,IL 61801, USA. E-mail: schilter@illinois.edub Institut fu¨r Chemie, Technische Universita¨t Berlin, 10623 Berlin, Germanyc Department of Chemistry, University of California, Davis, CA 95616, USA.E-mail: spjcramer@ucdavis.edud Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley,CA 94720, USAe JASRI, SPring-8, Sayo-gun, Hyogo 679-5198, Japan† Electronic supplementary information (ESI) available: Experimental proce-dures, spectral data, computational chemistry details, animated vibrationalmodes as GIFs. See DOI: 10.1039/c4cc04572fReceived 16th June 2014,Accepted 9th September 2014DOI: 10.1039/c4cc04572fwww.rsc.org/chemcommChemCommCOMMUNICATIONOpen Access Article. Published on 10 September 2014. Downloaded on 24/02/2016 15:47:14.  This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.View Article OnlineView Journal  | View Issue13470 | Chem. Commun., 2014, 50, 13469--13472 This journal is©The Royal Society of Chemistry 2014[(OC)3FeI(pdt)Ni(dppe)]+ ([1I]+).14 Reduction with CoCp2 gave 1in yields comparable to the (pdt)Ni(dppe)/Fe2(CO)9 route.11In adapting the synthesis to the Ni57Fe target, elemental 57Fewas oxidized to 57Fe2I4(iPrOH)4,12 which was converted into violet[(OC)357FeI(pdt)Ni(dppe)]+ (ESI-MS: m/z 829.5 [10I]+ vs. 828.9 [1I]+),with reduction aﬀording green (OC)357Fe(pdt)Ni(dppe) (10) in 35%yield (Scheme 1).While nCO energies and analytical and31P{1H} NMR data for 10are virtually identical to those of natural abundance 1, LI-FDI-MS(liquid introduction field desorption ionization mass spectrometry)analyses are telling. Soft ionization of non-polar 10 and 1 allowedfor the detection of parent cations at m/z 702.9 and 701.9, respec-tively (Fig. S4, ESI†). Oxidation of 10 with FcBF4 aﬀorded mixed-valent salt [10]BF4, whose EPR signal is broadened relative to that of[1]BF4 due to hyperfine interactions.Investigations into Ni–Fe bonding in the new 57Fe-labeledvariants of the reduced and oxidized complexes (respectively 10 and[10]+) were undertaken using NRVS. This technique, enabled bythe development of third generation synchrotron sources, insertiondevices and advanced X-ray optics,16–18 involves scanning anextremely monochromatic (e.g. 0.8 meV) X-ray beam through anuclear resonance of a Mo¨ssbauer-active isotope (e.g. 14.4 keV for57Fe). Subsequent relaxation causes the generation/annihilation ofphonons, the detection of which reveals all modes in which the 57Fenucleus moves along the direction of the incident X-ray. NRVS hasseveral advantages over traditional IR and resonance Raman spectro-scopies,19 not least in terms of element and isotope specificityand absence of the optical selection rules, which have allowed forthe resolution of nFe–X (X = S, P, Cl, CO, CN, NO) vibrationsin complicated systems.6,13,19,20 This relatively new but powerfultechnique in inorganic and biological iron chemistry is applied hereto [10]0/+. The analysed spectra in terms of 57Fe partial vibrationaldensity of states (PVDOS) are given in Fig. 2.Intense bands assigned to nFe–CO and dFe–COmodes were observedat 440–630 cm1, with full-range NRVS spectra and Fe–C(O) kineticenergy distribution (KED) diagrams presented in Fig. S9 (ESI†).Similar signals were found for [NiFe]–H2ase.6 It was expected thatnFe–S, dFe–S and nFe–Ni bands, if observable, would lie at low energies(r400 cm1). Upon comparing data for 10 and [10]+ (Fig. 2a), a sharpand prominent NRVS peak at 158 cm1 for 10 was noticed. Thisband, absent from the spectra of [10]+, was tentatively ascribed tovibration of the Ni–Fe bond, such interactions not being significantin [10]+. Differences in NRVS data of 10 and [10]+ were less marked inother spectral regions, although peaks for [10]+ were broader.The assignment of vibrational bands was elaborated usingDFT calculations on [10]0/+ as detailed in the ESI;† simulated NRVS(57Fe PVDOS) and Fe–Ni KED diagrams for [10]+ and 10 are alsopresented in Fig. 2b and c, respectively. Band positions and inten-sities in the calculated and observed spectra are largely in agreement(particularly in Fig. 2c; see also Fig. S9, ESI†). In the case of [10]+,some differences are assigned to impurities (10 and/or [10H]+). Theband for 10 at 158 cm1, calculated by DFT at 157 cm1, indeedinvolves stretching of the Fe–Ni bond symmetrical to a Ni–P1 stretch(see Fig. 3, and the ESI† for animations). Such a vibrational couplingin the Fe–Ni–P1 triad implicates a strong Fe–Ni interaction, and ithas no complement in the normal modes pool calculated for [1]+.While very prominent in NRVS (owing to the large 57Fe displace-ment), the 157 cm1 band is weaker (B5%) in the Ni–Fe KEDdiagram, which reflects relative motion of Fe and Ni. Other Ni–Festretches, such as those calculated at 266, 311, and 386 cm1 (see inFig. 2c), are considerably stronger (representing 13%, 9%, and 11%total Ni–Fe KED, respectively). Yet only the first two modes can beassociated with bands observed at 262 and 303 cm1, while the lastone has vanishing NRVS intensity (Fig. 2a). The modes at 266, 311,and 386 cm1 have lower 57Fe PVDOS intensity as they involvedisplacement mostly of Ni (rather than Fe), this movement beingevident from the DFT results (Fig. S10, ESI†). Analysis of Fe–Nivibrations is further complicated by vibrational coupling to C/P/Satoms, in particular the bridging S donors. Notably, mixed nFe–Nimodes in the 220–360 cm1 region involving up to 14% contributionfrom the Fe–Ni stretch were also reported for 1.10Structural (X-ray diﬀraction) and DFT studies on unlabeled[1]0/+ have suggested that the reduced Ni(I)Fe(I) species mayfeature Ni–Fe bonding,9 while the oxidized Ni(II)Fe(I) does not.8This was confirmed by re-analysing bonding in [1]0/+ using ELF,21Scheme 1Fig. 2 Observed NRVS spectra for [10]+ (thick red lines, (a) and (b)) and 10(thick blue lines, (a) and (c)) vs. DFT calculated 57Fe PVDOS spectra for [10]+(thin red line, (b)) and 10 (thin blue line, (c)). Calculated Fe–Ni KED (green) isgiven in (b) for [10]+, and in (c) for 10. Key bands observed for 10 are labelledin (a), with DFT counterparts in (c) indicated by vertical lines. Modes givingrise to bands with significant Fe–Ni character are marked (*) and shown inFig. 3 and Fig. S10 (ESI†). For 0–650 cm1 spectra, see Fig. S9 (ESI†).Communication ChemCommOpen Access Article. Published on 10 September 2014. Downloaded on 24/02/2016 15:47:14.  This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.View Article OnlineThis journal is©The Royal Society of Chemistry 2014 Chem. Commun., 2014, 50, 13469--13472 | 13471ELI-D,22 and QTAIM23 electron density-based methods (Fig. 4;Fig. S11 and S12, ESI†), all of which indicated a Ni–Fe bond in 1.Notably, the ELF/ELI-D bond attractor and the bond critical pointfound by QTAIM are shifted from the Ni–Fe vector away from thebridging S atoms, such that Fe(I) is (pseudo)octahedral. Bondinginvolves overlap of two singly-occupied d(z2) orbitals and is absentwhen Ni is oxidized, with [1]+ featuring a Fe-localized d(z2) SOMO. Incontrast, Ni–L has a SOMO with Ni d(z2) and d(x2  y2) character,4and a 2e Ni-Fe dative bond (optimized Fe–Ni distance: 2.47 Å).4While [1]+ and Ni–L have the same electron count for the [NiFe]3+site, only one has Ni–Fe bonding. A key distinction is Ni geometry,which is planar in [1]+ but SF4-like in Ni–L.Since the Fe(I) centre in [1]+ is electron poor (average nCO =2010 cm1)8 it cannot supply 2e for a Fe-Ni coordinate bond.Another possibility, a covalent Ni–Fe bond, is unlikely due to thelow donicity of Ni(II). The metal centres in [1]+ are distant (ourDFT result: 2.80 Å), while those in electron-rich 1 (average nCO =1977 cm1) are sufficiently proximal (experimental: 2.47 Å,9 DFT:2.46 Å) for covalent Fe–Ni bonding (see Table S2 and Fig. S3, ESI†for structural and IR details).Obtaining direct evidence of metal–metal bonding in molecularsystems is nontrivial, and distances do not guarantee presence/absence of bonding. For example, EXAFS studies reveal similarFe–Ni distances for Ni–L and Ni–C,24 despite Ni not being bondedto Fe in the latter. This highlights that (i) [NiFe]–H2ase active siteligation is inflexible (relative to [1]0/+) and that (ii) EXAFS/XRDstudies typically only afford nuclear positions via core electrondensity, with bonding electron density betweenmetals being poorlyresolved.25 In rare cases when very high quality single crystal dataare obtained, multipole analysis, followed by topological analysisof static electron density (versus inspection of difference maps)can give insights into metal–metal bonding, as exemplified by(re)investigation of the archetypal Mn2(CO)10.26Metal–metal bonding is common in organoiron chemistry, butit also plays a role in the reduced states of some metalloenzymes,stabilizing low-valent metal centres poised for substrate activation.7In addition to [NiFe]–H2ase, Ni–Fe interactions are also proposedfor carbon monoxide dehydrogenase (CODH),7,27 with Ni–Niand Fe–Fe bonds being present in acetyl-CoA synthetase (ACS)7and [FeFe]–H2ase,28 respectively. NRVS is demonstrably effec-tive in unambiguous identification of low energy 57Fe-coupledmodes.13,20,29 Compared to IR and resonance Raman, it avoidsinterference from solvent and ‘fingerprint’ bands, enablingidentification of Fe-coupled vibrations, such as the 158 cm1nFe–Ni mode here. The use of NRVS to probe iron–metal modesin everything from small molecules to iron enzymes is antici-pated to provide a wealth of information on these catalysts.While primordial routes to iron carbonyls have been reported(e.g. the one-pot preparation of (CO)3Fe(pdt)Fe(CO)3 fromFeCl2),30 they are typically limited in scope and reproducibility.In contrast, the Fe2I4(iPrOH)4/CO/CoCp2 strategy will likely begeneralizable and aﬀord iron carbonyls of relevance to H2asesand organoiron chemistry in general. With the isolation of57Fe-labeled [NiFe]–H2asemimics [10]0/+, the element and isotopeselectivity of NRVS was exploited to obtain the first vibrationalspectroscopic evidence of Fe–Ni interactions. These results serveas an important benchmark, opening the door to work probingmetal–metal bonding in redox-active H2ase enzymes as well asrelated enzymatic and model systems.Thanks are given to Drs Mark J. Nilges and Haijun Yao forassistance with EPR and LI-FDI-MS, respectively. Financialsupport was provided by the National Institutes of Health(GM061153-10 to T.B.R. and GM-65440 to S.P.C.), U.S. Depart-ment of Energy Oﬃce of Biological and Environmental Research(DOE OBER) (S.P.C.), and the ‘Unifying Concepts in Catalysis’initiative of the German Research Council (V.P., F.M., and M.K.).NRVS experiments performed at SPring-8 BL09XU were fundedby JASRI (beamtime proposal 2013A0032).Fig. 3 Scaled arrow depiction of nuclear displacements for the normalmode calculated for 10 at 157 cm1 (a symmetric Fe–Ni–P1 stretch, seecorresponding 57Fe PVDOS band in Fig. 2c). Key [10]0/+ modes are animatedin the ESI.†Fig. 4 Electron localization function (ELF) analysis of the Ni–Fe bondingin [1]0/+ (top/bottom). Ni–Fe bond attractor position for [1]0 is indicated bythe localized area in green (center-top), absent for [1]+. See Fig. S11 andS12 (ESI†) for alternative bonding representations.ChemComm CommunicationOpen Access Article. Published on 10 September 2014. Downloaded on 24/02/2016 15:47:14.  This article is licensed under a Creative Commons Attribution 3.0 Unported Licence.View Article Online13472 | Chem. Commun., 2014, 50, 13469--13472 This journal is©The Royal Society of Chemistry 2014Notes and references1 P. M. Vignais and B. Billoud, Chem. Rev., 2007, 107, 4206.2 H. Ogata, W. Lubitz and Y. Higuchi, Dalton Trans., 2009, 7577.3 M. Frey, ChemBioChem, 2002, 3, 153.4 M. Kampa, M.-E. Pandelia, W. Lubitz, M. van Gastel and F. Neese,J. Am. Chem. Soc., 2013, 135, 3915.5 S. Kaur-Ghumaan and M. Stein, Dalton Trans., 2014, 43, 9392.6 S. Kamali, H. Wang, D. 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Synthesis and vibrational spectroscopy of Fe-57-labeled models of [NiFe] hydrogenase: first direct observation of a nickel-iron interaction

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Synthesis and vibrational spectroscopy of Fe-57-labeled models of [NiFe] hydrogenase: first direct observation of a nickel-iron interaction

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