research papers\(\def\hfill{\hskip 5em}\def\hfil{\hskip 3em}\def\eqno#1{\hfil {#1}}\)

Journal logoSTRUCTURAL
CHEMISTRY
ISSN: 2053-2296

Crystal structure of a calcium(II)–pyrrolo­quinoline quinone (PQQ) complex outside a protein environment1

aDepartment of Chemistry, Ludwig-Maximilians-Universität München, Butenandtstrasse 5-13, Munich, Bavaria 81377, Germany
*Correspondence e-mail: lena.daumann@cup.lmu.de

Edited by Y. Ohgo, Teikyo University, Japan (Received 10 September 2020; accepted 27 October 2020; online 5 November 2020)

Pyrrolo­quinoline quinone (PQQ) is an important cofactor of calcium- and lanthanide-dependent alcohol de­hydrogenases, and has been known for over 30 years. Crystal structures of Ca–MDH enzymes (MDH is methanol de­hydrogenase) have been known for some time; however, crystal structures of PQQ with biorelevant metal ions have been lacking in the literature for decades. We report here the first crystal structure analysis of a Ca–PQQ com­plex outside the protein environment, namely, poly[[undeca­aqua­bis­(μ-4,5-dioxo-4,5-di­hydro-1H-pyrrolo­[2,3-f]quinoline-2,7,9-tri­carboxyl­ato)tricalcium(II)] dihydrate], {[Ca3(C14H3N2O8)2(H2O)11]·2H2O}n. The com­plex crystallized as Ca3PQQ2·13H2O with Ca2+ in three different positions and PQQ3−, including an extensive hydrogen-bond network. Similarities and differences to the recently reported structure with biorelevant europium (Eu2PQQ2) are discussed.

1. Introduction

Pyrrolo­quinoline quinone (PQQ) is the redox cofactor of glucose de­hydrogenase enzymes and alcohol de­hydrogenases. In particular, the methanol de­hydrogenase (MDH) enzymes, which catalyze the oxidation of methanol for the energy household of many methano- and methyl­otrophic microorganisms, have attracted attention recently. For proper functionality, a metal ion is needed, which acts as a Lewis acid and which is coordinated by PQQ and several amino acids in the enzymatic active site (Fig. 1[link]). The Ca-dependent MDH, encoded by the mxaF gene, was first discovered by Anthony & Zatman (1964a[Anthony, C. & Zatman, L. J. (1964a). Biochem. J. 92, 609-614.],b[Anthony, C. & Zatman, L. J. (1964b). Biochem. J. 92, 614-621.]).

[Figure 1]
Figure 1
The structure of the active site from Ca-dependent MDH (PDB code 1w6s).

After the structure of MDH was elucidated in 1978–79 (Duine et al., 1978[Duine, J. A., Frank, J. & Westerling, J. (1978). Biochim. Biophys. Acta Enzymol. 524, 277-287.]; Westerling et al., 1979[Westerling, J., Frank, J. & Duine, J. A. (1979). Biochem. Biophys. Res. Commun. 87, 719-724.]; Salisbury et al., 1979[Salisbury, S. A., Forrest, H. S., Cruse, W. B. T. & Kennard, O. (1979). Nature, 280, 843-844.]), the cofactor attracted much attention in the following years, with articles published concerning its total synthesis (Corey & Tramontano, 1981[Corey, E. J. & Tramontano, A. (1981). J. Am. Chem. Soc. 103, 5599-5600.]), redox chemistry (Eckert et al., 1982[Eckert, T. S., Bruice, T. C., Gainor, J. A. & Weinreb, S. M. (1982). Proc. Natl Acad. Sci. USA, 79, 2533-2536.]), metal coordination (Noar et al., 1985[Noar, J. B., Rodriguez, E. J. & Bruice, T. C. (1985). J. Am. Chem. Soc. 107, 7198-7199.]) and small-mol­ecule inter­action (van Koningsveld et al., 1985[Koningsveld, H. van, Jansen, J. C., Jongejan, J. A., Frank, J. Jzn. & Duine, J. A. (1985). Acta Cryst. C41, 89-92.]). Itoh and co-workers published several articles presenting the inter­action of PQQ with Ca and other alkaline earth metals (Itoh et al., 1997[Itoh, S., Kawakami, H. & Fukuzumi, S. (1997). J. Am. Chem. Soc. 119, 439-440.], 1998[Itoh, S., Kawakami, H. & Fukuzumi, S. (1998). Biochemistry, 37, 6562-6571.]), and the synthesis of model com­pounds, mimicking the active site of MDH (Itoh et al., 2000[Itoh, S., Kawakami, H. & Fukuzumi, S. (2000). J. Mol. Catal. B Enzym. 8, 85-94.]). Those publications contributed to a better understanding of the functionality and reactivity of PQQ. However, no crystal structures were presented in those studies, which would reveal in-depth structural information of PQQ–metal inter­actions. While no Ca–PQQ structure has been published to date, in addition, few other crystal structures exist for PQQ with other metals. Outside of the Ca–MDH network (Blake et al., 1994[Blake, C. C. F., Ghosh, M., Harlos, K., Avezoux, A. & Anthony, C. (1994). Nat. Struct. Mol. Biol. 1, 102-105.]; Williams et al., 2005[Williams, P. A., Coates, L., Mohammed, F., Gill, R., Erskine, P. T., Coker, A., Wood, S. P., Anthony, C. & Cooper, J. B. (2005). Acta Cryst. D61, 75-79.]), several structures were published with sodium (Ishida et al., 1989[Ishida, T., Doi, M., Tomita, K., Hayashi, H., Inoue, M. & Urakami, T. (1989). J. Am. Chem. Soc. 111, 6822-6828.]; Ikemoto et al., 2012[Ikemoto, K., Sakamoto, H. & Nakano, M. (2012). Chem. Cent. J. 6, 57.]; Ikemoto et al., 2017[Ikemoto, K., Sakamoto, Y., Tanaka, R., Ogata, K., Matsushita, N. & Nakamura, S. (2017). Cryst. Growth Des. 17, 4118-4123.]), with PQQ structural analogs and iron (Tommasi et al., 1995[Tommasi, L., Shechter-Barloy, L., Varech, D., Battioni, J. P., Donnadieu, B., Verelst, M., Bousseksou, A., Mansuy, D. & Tuchagues, J. P. (1995). Inorg. Chem. 34, 1514-1523.]), with copper and terpyridine (terpy) as co-ligand (Nakamura et al., 1994[Nakamura, N., Kohzuma, T., Kuma, H. & Suzuki, S. (1994). Inorg. Chem. 33, 1594-1599.]), with copper and tri­phenyl­phosphine (Wanner et al., 1999[Wanner, M., Sixt, T., Klinkhammer, K.-W. & Kaim, W. (1999). Inorg. Chem. 38, 2753-2755.]), with ruthenium and terpy (Mitome et al., 2015[Mitome, H., Ishizuka, T., Shiota, Y., Yoshizawa, K. & Kojima, T. (2015). Dalton Trans. 44, 3151-3158.]), and with ruthenium, silver and terpy (Mitome et al., 2013[Mitome, H., Ishizuka, T., Shiota, Y., Yoshizawa, K. & Kojima, T. (2013). Inorg. Chem. 52, 2274-2276.]). In 2014, Pol et al. reported a new kind of MDH, found in the extremo­phile Methyl­acidiphilum fumariolicum SolV (SolV), which is native to volcanic mudpots close to the Solfatara crater in Italy (Pol et al., 2014[Pol, A., Barends, T. R. M., Dietl, A., Khadem, A. F., Eygensteyn, J., Jetten, M. S. M. & Op den Camp, H. J. M. (2014). Environ. Microbiol. 16, 255-264.]). This MDH turned out to be strictly dependent on lanthanides (Pol et al., 2014[Pol, A., Barends, T. R. M., Dietl, A., Khadem, A. F., Eygensteyn, J., Jetten, M. S. M. & Op den Camp, H. J. M. (2014). Environ. Microbiol. 16, 255-264.]; Lumpe et al., 2018[Lumpe, H., Pol, A., Op den Camp, H. J. M. & Daumann, L. J. (2018). Dalton Trans. 47, 10463-10472.]; Bogart et al., 2015[Bogart, J. A., Lewis, A. J. & Schelter, E. J. (2015). Chem. Eur. J. 21, 1743-1748.]). While SolV was originally thought to be a biological curiosity, more and more organisms in all kinds of ecosystems were found to be lanthanide dependent in the following years, not restricted to such extreme environments like SolV (Keltjens et al., 2014[Keltjens, J. T., Pol, A., Reimann, J. & Op den Camp, H. J. M. (2014). Appl. Microbiol. Biotechnol. 98, 6163-6183.]; Ramachandran & Walsh, 2015[Ramachandran, A. & Walsh, D. A. (2015). FEMS Microbiol. Ecol. 91, fiv105/1-fiv105/10.]; Taubert et al., 2015[Taubert, M., Grob, C., Howat, A. M., Burns, O. J., Dixon, J. L., Chen, Y. & Murrell, J. C. (2015). Environ. Microbiol. 17, 3937-3948.]). This also pushed lanthanide bioinorganic chemistry as a new and emerging scientific field with several reviews published (Skovran & Martinez-Gomez, 2015[Skovran, E. & Martinez-Gomez, N. C. (2015). Science, 348, 862-863.]; Cheisson & Schelter, 2019[Cheisson, T. & Schelter, E. J. (2019). Science, 363, 489-493.]; Chistoserdova, 2019[Chistoserdova, L. (2019). Mol. Microbiol. 111, 1127-1131.]; Cotruvo, 2019[Cotruvo, J. A. (2019). ACS Cent. Sci. 9, 1496-1506.]; Daumann, 2019[Daumann, L. J. (2019). Angew. Chem. Int. Ed. 58, 12795-12802.]; Picone & Op den Camp, 2019[Picone, N. & Op den Camp, H. J. M. (2019). Curr. Opin. Chem. Biol. 49, 39-44.]; Semrau et al., 2018[Semrau, J. D., DiSpirito, A. A., Gu, W. & Yoon, S. (2018). Appl. Environ. Microbiol. 84, e02289-17.]). Recently, also, the first crystal structure of a europium–PQQ com­plex outside the MDH network was published through a collaborative effort and was reported as an Eu2PQQ2 structure (Lumpe et al., 2020[Lumpe, H., Menke, A., Haisch, C., Mayer, P., Kabelitz, A., Yusenko, K. V., Guilherme Buzanich, A., Block, T., Pöttgen, R., Emmerling, F. & Daumann, L. J. (2020). Chem. Eur. J. 26, 10133-10139.]) (Fig. 2[link]). In light of those advances and the still scarce structural information available about PQQ–metal inter­actions, we present here the first crystal structure of a Ca–PQQ com­plex without the need of structural PQQ analogs or additional co-ligands. The mol­ecular formula of the com­plex is Ca3PQQ2·13H2O.

[Figure 2]
Figure 2
The crystal structure of the inversion-symmetric Eu2PQQ2 com­plex. The CIF is taken from Lumpe et al. (2020[Lumpe, H., Menke, A., Haisch, C., Mayer, P., Kabelitz, A., Yusenko, K. V., Guilherme Buzanich, A., Block, T., Pöttgen, R., Emmerling, F. & Daumann, L. J. (2020). Chem. Eur. J. 26, 10133-10139.]). Displacement ellipsoids are drawn at the 50% probability level. [Symmetry code: (i) −x + 1, −y + 1, −z + 1.]

2. Experimental

2.1. Materials

CaCl2·2H2O (99%) was purchased from VWR. Na2PQQ·H2O was extracted from Doctor's Best Science-Based Nutrition BioPQQ capsules, as described previously (Lumpe & Daumann, 2019[Lumpe, H. & Daumann, L. J. (2019). Inorg. Chem. 58, 8432-8441.]). Milli-Q-grade water (pH 5.5), obtained from a Millipore Synergy UV system from Merck (Darmstadt, Germany), was used for all experiments.

2.2. Crystal growth and analysis

Na2PQQ·H2O (32.8 mg, 0.08 mmol) was dissolved in H2O (12 ml). CaCl2·2H2O (2.0 equiv., 23.6 mg, 0.16 mmol) was added as a solid. The metal addition led to precipitation of a pale-grey–brown solid, which was centrifuged, removed and analyzed as a 1:1 PQQ–Ca com­plex, as described in our previous article (Lumpe & Daumann, 2019[Lumpe, H. & Daumann, L. J. (2019). Inorg. Chem. 58, 8432-8441.]). From the supernatant, consisting of a highly diluted aqueous mixture of Na2PQQ and CaCl2, small dark crystals, suitable for X-ray crystallography, grew over a period of several months. To obtain more crystalline material of better quality, a procedure from our recent publication (Lumpe et al., 2020[Lumpe, H., Menke, A., Haisch, C., Mayer, P., Kabelitz, A., Yusenko, K. V., Guilherme Buzanich, A., Block, T., Pöttgen, R., Emmerling, F. & Daumann, L. J. (2020). Chem. Eur. J. 26, 10133-10139.]) was implemented. Na2PQQ·H2O (24.2 mg, 61.8 µmol) was com­pletely dissolved in H2O (4 ml) at 80 °C in an ultrasonic bath. CaCl2·2H2O (27.3 mg, 185.4 µmol, 3 equiv.) was dissolved in a small amount of water (0.2 ml) and was added to the Na2PQQ solution at 80 °C, which caused precipitation of a grey–brown solid. The mixture was placed directly in a drying oven at 80 °C, which was then switched off and the reaction mixture allowed to cool slowly. After 1 d, small dark crystals had grown between the bulk precipitate. The crystals grew in size over the next few days while consuming the surrounding bulk precipitate. Crystals suitable for X-ray diffraction analysis were then picked out of the reaction mixture. The crystal used for analysis was selected in paraffin oil to prevent dehydration and then placed and measured on a Mitegen Microloop. The crystals obtained from both methods showed the same structure depicted in Fig. 3[link].

[Figure 3]
Figure 3
(a) The asymmetric unit of Ca3PQQ2·13H2O. (b) A strand along [[\overline{1}]11] consisting of inversion-symmetric Ca2PQQ22− pairs. Here, for clarity, all water mol­ecules, except for that involved in intra-pair hydrogen bonds (green arrows), have been omitted. For symmetry codes, see Table 2[link].

IR (diamond ATR, neat): [\~\nu]/cm−1 3643–2746 (w, broad), 1923–1714 (w, broad), 1686 (w), 1658 (w), 1605 (s), 1577 (m), 1553 (m), 1536 (m), 1498 (m), 1426 (w), 1400 (m), 1348 (s), 1277 (m), 1246 (m), 1191 (m), 1151 (m), 1132 (w), 1086 (w), 1027 (w), 972 (w), 951 (w), 926 (w), 868 (w), 824 (w), 767 (w), 719 (w), 700 (w), 669 (w). Elemental analysis (CHN) calculated (%) for Ca3PQQ2·11H2O or C28H28Ca3N4O27: C 34.57, H 2.90, N 5.76; found: C 34.30, H 3.20, N 6.06. Crystals were picked out of the reaction mixture and then dried for 1 d on filter paper prior to elemental analysis.

2.3. Refinement

Crystal data, data collection and structure refinement details are summarized in Table 1[link]. Four reflections have been omitted from the refinement. Three of them are hidden by the beam stop and show no intensity. A further omitted reflection of higher order (090) has a significantly higher Fo2 (63.72) com­pared to its Fc2 (1.09). This behaviour is observed quite often for reflections of higher order when multigraded X-ray mirrors are used as monochromators. All C-bound H atoms have been calculated in ideal geometry riding on their parent atoms, while the O- and N-bound H atoms were refined freely. Full details of the refinement strategy can be found in the embedded instruction file in the CIF.

Table 1
Experimental details

Crystal data
Chemical formula [Ca3(C14H3N2O8)2(H2O)11]·2H2O
Mr 1008.81
Crystal system, space group Triclinic, P[\overline{1}]
Temperature (K) 109
a, b, c (Å) 6.9363 (3), 15.9791 (7), 16.9786 (7)
α, β, γ (°) 90.844 (1), 93.106 (1), 98.296 (2)
V3) 1858.93 (14)
Z 2
Radiation type Mo Kα
μ (mm−1) 0.56
Crystal size (mm) 0.10 × 0.02 × 0.01
 
Data collection
Diffractometer Bruker D8 Venture TXS
Absorption correction Multi-scan (SADABS; Bruker, 2016[Bruker (2016). APEX3 and SADABS. Bruker AXS Inc., Madison, Wisconsin, USA.])
Tmin, Tmax 0.88, 0.99
No. of measured, independent and observed [I > 2σ(I)] reflections 33048, 8166, 7023
Rint 0.043
(sin θ/λ)max−1) 0.641
 
Refinement
R[F2 > 2σ(F2)], wR(F2), S 0.031, 0.072, 1.04
No. of reflections 8166
No. of parameters 689
H-atom treatment H atoms treated by a mixture of independent and constrained refinement
Δρmax, Δρmin (e Å−3) 0.39, −0.28
Computer programs: APEX3 (Bruker, 2016[Bruker (2016). APEX3 and SADABS. Bruker AXS Inc., Madison, Wisconsin, USA.]), SAINT (Bruker, 2017[Bruker (2017). SAINT. Bruker AXS Inc., Madison, Wisconsin, USA.]), SHELXT2014 (Sheldrick, 2015[Sheldrick, G. M. (2015). Acta Cryst. C71, 3-8.]a), SHELXL2018 (Sheldrick, 2015[Sheldrick, G. M. (2015). Acta Cryst. C71, 3-8.]b) and ORTEP-3 (Farrugia, 2012[Farrugia, L. J. (2012). J. Appl. Cryst. 45, 849-854.]).

3. Results and discussion

3.1. Investigation of PQQ–Ca com­plexation

In our previous article, PQQ–metal com­plexes were reported with the trivalent lanthanides La3+, Eu3+ and Lu3+, and with Ca2+ (Lumpe & Daumann, 2019[Lumpe, H. & Daumann, L. J. (2019). Inorg. Chem. 58, 8432-8441.]). Regardless of the excess of added metal salt, 1:1 com­plexes were identified by elemental analysis. While no further structural information could be provided in that study, we were recently able to verify the proposed stoichiometry by the crystal structure of an Eu–PQQ com­plex with the net formula Eu2PQQ2·12H2O (Lumpe et al., 2020[Lumpe, H., Menke, A., Haisch, C., Mayer, P., Kabelitz, A., Yusenko, K. V., Guilherme Buzanich, A., Block, T., Pöttgen, R., Emmerling, F. & Daumann, L. J. (2020). Chem. Eur. J. 26, 10133-10139.]). The Eu3+ ion is coordinated by PQQ in the same fashion as in MDH, with participation of N2, O4 and O5, in addition to the participation of O1 (Fig. 2[link]). The latter residue is not utilized in the enzyme for metal coordination.

From a similar experimental approach using Ca2+ instead of Eu3+, single crystals suitable for X-ray analysis were grown over a period of several days. Fig. 3[link] illustrates the com­position of the asymmetric unit: the charges of two triply deprotonated PQQ units are balanced by three Ca2+ ions supplemented by 13 water mol­ecules. The structural motif depicted in Fig. 2[link] – the formation of binuclear units by means of two PQQ ligands acting as linkers between the metal centres – is realized in Ca3PQQ2·13H2O in a com­parable fashion for two of the three Ca ions (Ca1 and Ca3). Ca1 is coordinated by PQQ in a similar fashion to Eu; however, the coordination sphere is com­pleted by a carboxyl­ate group of a nearby pyridine moiety of PQQ (instead of a carboxyl­ate of a pyrrole ring). Ca3, on the other hand, uses the same pocket and residues as Eu; however, this inter­action is assisted by a hydrogen bond of a Ca3-bound water mol­ecule to the carboxyl­ate group of the pyrrole ring (Fig. 3[link]b, green arrows). In the structure, these two types of alternating Ca1 and Ca3 units are connected via Ca1 into strands along [[\overline{1}]11]. The charge of the Ca2PQQ2 unit is balanced by Ca2, which is coordinated solely by water mol­ecules and carboxyl­ate groups, however, never in the biologically relevant ONO pocket of PQQ. All N—H and O—H donor groups are involved in classical hydrogen bonds with either carboxyl­ate groups, keto groups or water mol­ecules, acting as acceptors establishing a three-dimensional network (see Table 2[link] for hydrogen-bond details).

Table 2
Hydrogen-bond geometry (Å, °)

D—H⋯A D—H H⋯A DA D—H⋯A
N1—H2⋯O8 0.86 (2) 2.01 (2) 2.7232 (19) 139.6 (19)
N3—H4⋯O16 0.86 (2) 1.83 (2) 2.6163 (19) 151 (2)
O17—H171⋯O10iii 0.85 (3) 1.91 (3) 2.7543 (18) 170 (3)
O17—H172⋯O1 0.86 (3) 2.08 (3) 2.9287 (19) 170 (2)
O18—H181⋯O28 0.88 (3) 1.82 (3) 2.681 (2) 166 (2)
O18—H182⋯O1iv 0.84 (3) 1.97 (3) 2.8107 (19) 176 (3)
O19—H191⋯O20ii 0.81 (3) 2.10 (3) 2.8789 (19) 161 (3)
O19—H192⋯O5i 0.85 (3) 1.89 (3) 2.7350 (18) 174 (3)
O20—H201⋯O11v 0.82 (3) 2.00 (3) 2.8221 (18) 173 (3)
O20—H202⋯O2vi 0.84 (3) 1.94 (3) 2.7620 (18) 169 (3)
O21—H211⋯O29iii 0.80 (3) 2.05 (3) 2.845 (2) 173 (3)
O21—H212⋯O16 0.85 (3) 1.90 (3) 2.7320 (18) 163 (3)
O22—H221⋯O19vi 0.76 (3) 2.26 (3) 2.958 (2) 152 (3)
O22—H222⋯O6vii 0.87 (3) 1.83 (3) 2.6985 (19) 175 (3)
O23—H231⋯O3viii 0.76 (3) 2.10 (3) 2.8398 (19) 164 (3)
O23—H232⋯O9iii 0.83 (3) 1.90 (3) 2.7217 (19) 169 (3)
O24—H241⋯O7ix 0.81 (3) 2.03 (3) 2.8040 (19) 163 (3)
O24—H242⋯O29 0.82 (3) 1.93 (3) 2.750 (2) 172 (3)
O25—H251⋯O13ix 0.85 (3) 2.02 (3) 2.8578 (18) 168 (3)
O25—H252⋯O3viii 0.81 (3) 2.41 (3) 3.0258 (19) 133 (2)
O25—H252⋯O4viii 0.81 (3) 2.28 (3) 3.0405 (18) 155 (3)
O26—H261⋯O27x 0.86 (3) 2.11 (3) 2.9018 (19) 154 (3)
O26—H262⋯O13ix 0.80 (3) 2.06 (3) 2.8506 (19) 170 (3)
O27—H271⋯O25iv 0.85 (3) 2.08 (3) 2.9022 (19) 164 (3)
O27—H272⋯O9v 0.83 (3) 1.99 (3) 2.8125 (18) 171 (2)
O28—H281⋯O10v 0.89 (4) 1.88 (4) 2.721 (2) 159 (3)
O28—H282⋯O26x 0.83 (4) 2.59 (3) 3.098 (2) 121 (3)
O29—H291⋯O6ix 0.84 (3) 1.85 (3) 2.6582 (19) 160 (3)
O29—H292⋯O11 0.79 (3) 2.27 (3) 3.021 (2) 159 (3)
O29—H292⋯O12 0.79 (3) 2.40 (3) 2.7789 (19) 110 (2)
Symmetry codes: (i) [-x+1, -y+1, -z+1]; (ii) [x-1, y, z]; (iii) [-x+1, -y, -z]; (iv) x+1, y, z; (v) [-x+2, -y, -z]; (vi) [-x+1, -y, -z+1]; (vii) [x, y-1, z]; (viii) [x, y, z-1]; (ix) [-x+1, -y+1, -z]; (x) [-x+2, -y+1, -z].

Inter­estingly, while the elemental analysis of the initially precipitated (amorphous) solid showed a 1:1 Ca–PQQ stoichiometry (Lumpe & Daumann, 2019[Lumpe, H. & Daumann, L. J. (2019). Inorg. Chem. 58, 8432-8441.]), the present structure from slowly crystallized material reveals a network of three different Ca2+ ions and two differently-coordinated PQQ anionic ligands, resulting in a 3:2 stoichiometry. Also, in the Ca–PQQ structure, both PQQ mol­ecules coordinate in the same fashion as in the MDH enzyme (Fig. 1[link]), in addition to the participation of several carboxylate groups. One of the PQQ ligands coordinates to calcium with the participation of all three carboxylate groups: Ca1 via O8, N2, O5 and O4, and Ca2 via O1 and O2 in a bidentate manner. The second PQQ mol­ecule coordinates with only two of the three carboxylate groups and coordinates Ca1 with O14, Ca2 with O15 and Ca3 with N4, O12 and O13. In total, 13 water mol­ecules are present in the crystal structure, of which 11 directly coordinate to atoms Ca1–Ca3 and two water mol­ecules (O28 and O29) have no direct coordination partners. Inter­estingly, elemental analysis of the dried crystalline material fits best to only 11 water mol­ecules, most likely due to the disappearance of the two noncoordinating water mol­ecules during the drying process. Ca1 and Ca2 show penta­gonal–bipyramidal geometries, with coordination numbers (CNs) of 7 and Ca3 shows a distorted geometry with a CN of 8. All metal-to-ligand bond lengths and angles of Ca3PQQ2 are given in Table 3[link], in addition to the values for Eu2PQQ2. The known PQQ–water adduct (diol in C5 position), which is formed to some extent in aqueous solution (Dekker et al., 1982[Dekker, R. H., Duine, J. A., Frank, J., Verwiel, P. E. J. & Westerling, J. (1982). Eur. J. Biochem. 125, 69-73.]), is not present in the com­plex, and this is in line with all known crystal structures of PQQ, to the best of our knowledge.

Table 3
Selected bond lengths (Å) of the Ca3PQQ2·13H2O com­plex in com­parison with the previously reported Eu2PQQ2·12H2O structure

For symmetry data for Eu2PQQ2·12H2O, see Lumpe et al. (2020[Lumpe, H., Menke, A., Haisch, C., Mayer, P., Kabelitz, A., Yusenko, K. V., Guilherme Buzanich, A., Block, T., Pöttgen, R., Emmerling, F. & Daumann, L. J. (2020). Chem. Eur. J. 26, 10133-10139.]).

Ca3PQQ2·13H2O Eu2PQQ2·12H2O
Ca1i—O4 2.5928 (12) Eu1—O4 2.584 (2)
Ca1i—N2 2.5069 (14) Eu1—N2 2.648 (2)
Ca1i—O5 2.3784 (12) Eu1—O5 2.440 (2)
Ca1—O14 2.2514 (12) Eu1—O1 2.409 (2)
Ca1—O8 2.3137 (12) Eu1—Owater (5 bonds) 2.389 (2)–2.464 (2)
Ca1—O17 2.3694 (13)    
Ca1—O18 2.3145 (14) Ca3—O12 2.5703 (12)
Ca2ii—O1 2.4812 (12) Ca3—N4 2.5460 (14)
Ca2ii—O2 2.5279 (12) Ca3—O13 2.3963 (12)
Ca2—O15 2.3522 (12) Ca3—O23 2.4362 (14)
Ca2—O19 2.3894 (14) Ca3—O24 2.3607 (13)
Ca2—O20 2.4382 (13) Ca3—O25 2.5787 (14)
Ca2—O21 2.3824 (14) Ca3—O26 2.3962 (14)
Ca2—O22 2.3383 (14) Ca3—O27 2.4924 (14)
Symmetry codes: (i) −x + 1, −y + 1, −z + 1; (ii) x − 1, y, z.

In the Eu2PQQ2 com­plex, the Eu ions are coordinated in a similar fashion by PQQ. The bonds to Eu are up to 0.141 Å longer than to Ca1 and Ca3. The CN of Eu in the com­plex is 9, which corresponds to an ionic radius of 1.12 Å according to Shannon (1976[Shannon, R. D. (1976). Acta Cryst. A32, 751-767.]), while the ionic radius of Ca is 1.06 Å for a CN of 7 and 1.12 Å for a CN of 8. Therefore, the larger bond lengths to Eu can hardly be explained by different ionic radii, which are overall similar, but by differences in the CNs and different participation in coordination of a second PQQ mol­ecule.

The IR spectra of the precipitated Ca–PQQ amorphous solid, Eu2PQQ2 and Ca3PQQ2 crystals were recorded and com­pared (Fig. 4[link]). The spectra can be roughly divided into two areas. While PQQ C=O stretching vibrations of the carboxylate and quinone groups absorb in the range 1750–1600 cm−1 (Zhejiang Hisun Pharmaceutical Co. Ltd, 2020[Zhejiang Hisun Pharmaceutical Co. Ltd (2020). GRAS Exemption Claim for Pyrrolo­quinoline Quinone (PQQ) Disodium Salt; https://www.fda.gov/downloads/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm508141.pdf.]), the peaks with smaller wavenumbers are largely related to PQQ lattice vibrations. While the heights of the large absorption bands in the range 3600–2600 cm−1 are a direct result of the different amounts and coordination modes of cocrystallized water, the differences in the area 1750–1550 cm−1 further indicate the different coordination modes already depicted in the crystal structures.

[Figure 4]
Figure 4
Normalized IR absorption spectra of the Ca3PQQ2 com­plex in black, the 1:1 Ca–PQQ precipitate in grey and the Eu2PQQ2 com­plex in blue. Inset: close-up of the PQQ-related IR absorption peaks.

4. Conclusion

We present here the first crystal structure of PQQ with the biologically relevant metal ion calcium. The com­plex consists of PQQ and the metal ion alone, unlike previously reported structures with other metal ions. Those com­plexes often needed additional co-ligands, which limited the use of the structures for com­parison with the biologically active site. However, in particular, the use of methyl­ated PQQMe3 (with all three carboxyl groups esterified) prevented participation of (nonbiogenic) carboxyl groups in com­plexation. This is not the case in the presented structure, where calcium is coordinated by PQQ in the same pocket as in MDH, in addition to further carboxyl-group participation, spanning a three-dimensional coordination network. However, considering the few crystal structures of PQQ com­plexes reported over the years, we are confident that the presented structure will help to better explain the coordination behaviour of PQQ outside the MDH enzyme and help guide the design of mononuclear model com­plexes for these fascinating enzymes.

Supporting information


Computing details top

Data collection: APEX3 (Bruker, 2016); cell refinement: SAINT (Bruker, 2017); data reduction: SAINT (Bruker, 2017); program(s) used to solve structure: SHELXT2014 (Sheldrick, 2015a); program(s) used to refine structure: SHELXL2018 (Sheldrick, 2015b); molecular graphics: ORTEP-3 (Farrugia, 2012); software used to prepare material for publication: SHELXL2018 (Sheldrick, 2015b).

Poly[[undecaaquabis(µ-4,5-dioxo-4,5-dihydro-1H-pyrrolo[2,3-f]quinoline-2,7,9-tricarboxylato)tricalcium(II)] dihydrate] top
Crystal data top
[Ca3(C14H3N2O8)2(H2O)11]·2H2OZ = 2
Mr = 1008.81F(000) = 1040
Triclinic, P1Dx = 1.802 Mg m3
a = 6.9363 (3) ÅMo Kα radiation, λ = 0.71073 Å
b = 15.9791 (7) ÅCell parameters from 9854 reflections
c = 16.9786 (7) Åθ = 2.7–27.1°
α = 90.844 (1)°µ = 0.56 mm1
β = 93.106 (1)°T = 109 K
γ = 98.296 (2)°Rod, brown
V = 1858.93 (14) Å30.10 × 0.02 × 0.01 mm
Data collection top
Bruker D8 Venture TXS
diffractometer
8166 independent reflections
Radiation source: rotating anode (TXS), Bruker TXS7023 reflections with I > 2σ(I)
Focusing mirrors monochromatorRint = 0.043
Detector resolution: 7.3910 pixels mm-1θmax = 27.1°, θmin = 2.9°
mix of phi and ω scansh = 88
Absorption correction: multi-scan
(SADABS; Bruker, 2016)
k = 2020
Tmin = 0.88, Tmax = 0.99l = 2121
33048 measured reflections
Refinement top
Refinement on F2Primary atom site location: structure-invariant direct methods
Least-squares matrix: fullHydrogen site location: mixed
R[F2 > 2σ(F2)] = 0.031H atoms treated by a mixture of independent and constrained refinement
wR(F2) = 0.072 w = 1/[σ2(Fo2) + (0.0198P)2 + 1.5469P]
where P = (Fo2 + 2Fc2)/3
S = 1.04(Δ/σ)max < 0.001
8166 reflectionsΔρmax = 0.39 e Å3
689 parametersΔρmin = 0.28 e Å3
0 restraints
Special details top

Geometry. All esds (except the esd in the dihedral angle between two l.s. planes) are estimated using the full covariance matrix. The cell esds are taken into account individually in the estimation of esds in distances, angles and torsion angles; correlations between esds in cell parameters are only used when they are defined by crystal symmetry. An approximate (isotropic) treatment of cell esds is used for estimating esds involving l.s. planes.

Refinement. H(C) constr, H(O,N) refall

The X-ray intensity data of Ca3PQQ2.13H2O were measured on a Bruker D8 Venture TXS system equipped with a multilayer mirror monochromator and an Mo Kα rotating anode X-ray tube (λ = 0.71073 Å). The frames were integrated with the Bruker SAINT software package (Bruker, 2012). Data were corrected for absorption effects using the multi-scan method (SADABS; Sheldrick, 1996). The structure was solved and refined using the Bruker SHELXTL software package (Sheldrick, 2015).

The figures have been drawn at the 50% ellipsoid probability level (Farrugia, 2012). CCDC reference number 2019890 contains the supplementary crystallographic data for this compound. These data can be obtained free of charge from The Cambridge Crystallographic Data Centre via https://www.ccdc.cam.ac.uk/structures/.

Fractional atomic coordinates and isotropic or equivalent isotropic displacement parameters (Å2) top
xyzUiso*/Ueq
C10.0551 (2)0.15843 (11)0.45568 (10)0.0109 (3)
C20.0302 (2)0.23438 (11)0.50409 (10)0.0109 (3)
C30.0676 (3)0.24585 (11)0.58398 (10)0.0118 (3)
H30.0449890.2040500.6229530.014*
C40.1464 (2)0.33192 (10)0.59713 (10)0.0106 (3)
C50.2090 (3)0.37785 (11)0.67020 (10)0.0112 (3)
C60.2975 (2)0.47079 (11)0.66033 (10)0.0101 (3)
C70.2934 (2)0.50827 (10)0.57991 (10)0.0093 (3)
C80.3650 (2)0.63184 (10)0.51260 (10)0.0092 (3)
C90.2907 (2)0.59109 (10)0.44200 (10)0.0097 (3)
H9A0.2860910.6224330.3949920.012*
C100.2233 (2)0.50464 (11)0.43996 (10)0.0095 (3)
C110.2231 (2)0.46006 (10)0.51131 (10)0.0085 (3)
C120.1552 (2)0.37072 (11)0.52343 (10)0.0095 (3)
C130.4498 (2)0.72499 (10)0.51886 (10)0.0096 (3)
C140.1589 (2)0.46574 (10)0.35822 (10)0.0092 (3)
C150.8745 (2)0.19201 (10)0.04981 (10)0.0101 (3)
C160.8334 (2)0.10395 (10)0.06229 (10)0.0091 (3)
C170.8475 (2)0.05705 (10)0.12909 (10)0.0097 (3)
H170.8815600.0752530.1793380.012*
C180.8015 (2)0.02382 (11)0.10895 (10)0.0096 (3)
C190.7972 (2)0.09630 (11)0.15653 (10)0.0107 (3)
C200.7502 (2)0.17425 (11)0.11221 (9)0.0095 (3)
C210.6921 (2)0.16752 (10)0.02863 (9)0.0083 (3)
C220.5978 (2)0.24379 (10)0.07438 (9)0.0089 (3)
C230.6126 (2)0.17681 (10)0.12466 (10)0.0099 (3)
H230.5843510.1823540.1784550.012*
C240.6684 (2)0.10142 (10)0.09720 (10)0.0088 (3)
C250.7027 (2)0.09418 (10)0.01609 (9)0.0077 (3)
C260.7593 (2)0.02301 (10)0.02847 (9)0.0085 (3)
C270.5362 (2)0.32716 (10)0.09921 (9)0.0093 (3)
C280.6930 (2)0.03531 (11)0.15995 (10)0.0098 (3)
N10.0833 (2)0.31067 (9)0.46858 (9)0.0101 (3)
N20.3651 (2)0.59035 (9)0.58038 (8)0.0090 (3)
H20.084 (3)0.3176 (13)0.4186 (13)0.015 (5)*
N30.7800 (2)0.05460 (9)0.00212 (8)0.0086 (3)
N40.6427 (2)0.23938 (9)0.00095 (8)0.0086 (3)
H40.748 (4)0.0682 (15)0.0449 (15)0.030 (6)*
O10.06633 (18)0.16506 (7)0.38093 (7)0.0128 (3)
O20.11654 (18)0.09119 (7)0.48944 (7)0.0136 (3)
O30.2007 (2)0.34951 (8)0.73630 (7)0.0169 (3)
O40.37574 (18)0.51241 (7)0.71690 (7)0.0127 (3)
O50.52358 (18)0.75182 (7)0.58571 (7)0.0120 (2)
O60.4405 (2)0.76768 (8)0.45848 (7)0.0164 (3)
O70.06140 (18)0.50722 (8)0.31437 (7)0.0130 (3)
O80.21731 (18)0.39705 (7)0.34077 (7)0.0125 (3)
O90.87842 (18)0.21856 (8)0.01978 (7)0.0136 (3)
O100.90747 (19)0.23220 (8)0.11050 (7)0.0151 (3)
O110.8269 (2)0.10239 (8)0.22705 (7)0.0171 (3)
O120.76438 (18)0.24116 (7)0.14539 (7)0.0125 (3)
O130.53948 (18)0.38361 (7)0.04724 (7)0.0123 (3)
O140.48287 (18)0.33522 (7)0.16717 (7)0.0122 (2)
O150.74044 (19)0.06498 (8)0.22821 (7)0.0151 (3)
O160.66342 (19)0.04197 (7)0.14100 (7)0.0134 (3)
O170.2228 (2)0.21676 (8)0.26500 (8)0.0155 (3)
H1710.173 (4)0.2165 (17)0.2180 (17)0.042 (8)*
H1720.130 (4)0.1974 (16)0.2943 (15)0.032 (7)*
O180.7774 (2)0.29042 (9)0.29412 (8)0.0191 (3)
H1810.851 (4)0.3119 (16)0.2567 (16)0.035 (7)*
H1820.823 (4)0.2513 (19)0.3180 (17)0.048 (8)*
O190.4610 (2)0.08055 (9)0.37538 (8)0.0166 (3)
H1910.352 (4)0.0580 (17)0.3624 (15)0.038 (8)*
H1920.460 (4)0.1327 (18)0.3851 (15)0.037 (7)*
O201.07981 (19)0.01918 (8)0.36462 (8)0.0138 (3)
H2011.099 (4)0.0466 (18)0.3251 (18)0.049 (9)*
H2021.095 (4)0.0465 (17)0.4056 (17)0.041 (8)*
O210.6842 (2)0.11057 (9)0.28711 (8)0.0191 (3)
H2110.601 (4)0.1501 (18)0.2910 (15)0.037 (8)*
H2120.679 (4)0.0997 (17)0.2380 (17)0.042 (8)*
O220.6175 (2)0.07062 (9)0.45523 (8)0.0218 (3)
H2210.616 (4)0.0567 (18)0.4984 (18)0.048 (9)*
H2220.563 (4)0.1236 (19)0.4537 (16)0.047 (8)*
O230.3675 (2)0.26664 (9)0.13577 (9)0.0155 (3)
H2310.307 (4)0.2808 (16)0.1708 (16)0.033 (7)*
H2320.291 (4)0.2457 (17)0.1028 (16)0.039 (8)*
O240.6812 (2)0.39272 (9)0.22016 (8)0.0182 (3)
H2410.768 (4)0.4241 (17)0.2383 (15)0.036 (8)*
H2420.678 (4)0.3485 (19)0.2459 (16)0.043 (8)*
O250.34868 (19)0.45056 (8)0.11501 (8)0.0143 (3)
H2510.367 (4)0.5014 (18)0.0984 (16)0.040 (8)*
H2520.336 (4)0.4522 (17)0.1628 (18)0.043 (8)*
O260.7643 (2)0.51788 (8)0.07189 (8)0.0177 (3)
H2610.865 (5)0.5441 (19)0.0459 (18)0.054 (9)*
H2620.684 (4)0.5490 (17)0.0700 (15)0.035 (7)*
O270.9930 (2)0.37549 (9)0.04551 (8)0.0152 (3)
H2711.082 (4)0.3989 (18)0.0735 (16)0.043 (8)*
H2721.021 (4)0.3284 (17)0.0340 (14)0.031 (7)*
O280.9475 (2)0.36727 (10)0.17111 (9)0.0212 (3)
H2811.013 (5)0.333 (2)0.1450 (19)0.067 (10)*
H2821.030 (5)0.409 (2)0.182 (2)0.069 (11)*
O290.6350 (2)0.24139 (9)0.30317 (9)0.0210 (3)
H2910.640 (4)0.2383 (16)0.3524 (16)0.034 (7)*
H2920.711 (4)0.2134 (17)0.2848 (16)0.039 (8)*
Ca10.47149 (5)0.33132 (2)0.29935 (2)0.00881 (8)
Ca20.75264 (5)0.02017 (2)0.35950 (2)0.00913 (8)
Ca30.63978 (5)0.37014 (2)0.08465 (2)0.00934 (8)
Atomic displacement parameters (Å2) top
U11U22U33U12U13U23
C10.0099 (8)0.0095 (8)0.0132 (8)0.0014 (7)0.0000 (6)0.0006 (6)
C20.0104 (8)0.0087 (8)0.0134 (8)0.0004 (7)0.0022 (6)0.0016 (6)
C30.0136 (8)0.0088 (8)0.0126 (8)0.0004 (7)0.0013 (7)0.0009 (6)
C40.0111 (8)0.0075 (8)0.0126 (8)0.0004 (6)0.0009 (7)0.0013 (6)
C50.0119 (8)0.0090 (8)0.0126 (8)0.0011 (7)0.0006 (7)0.0010 (6)
C60.0095 (8)0.0113 (8)0.0096 (8)0.0026 (7)0.0007 (6)0.0005 (6)
C70.0081 (8)0.0078 (8)0.0119 (8)0.0010 (6)0.0006 (6)0.0012 (6)
C80.0093 (8)0.0074 (8)0.0109 (8)0.0009 (6)0.0011 (6)0.0008 (6)
C90.0099 (8)0.0101 (8)0.0090 (8)0.0013 (7)0.0001 (6)0.0016 (6)
C100.0071 (8)0.0105 (8)0.0108 (8)0.0013 (6)0.0004 (6)0.0003 (6)
C110.0068 (8)0.0077 (8)0.0108 (8)0.0003 (6)0.0004 (6)0.0002 (6)
C120.0071 (8)0.0093 (8)0.0117 (8)0.0005 (6)0.0005 (6)0.0013 (6)
C130.0094 (8)0.0081 (8)0.0110 (8)0.0002 (6)0.0019 (6)0.0007 (6)
C140.0083 (8)0.0085 (8)0.0096 (8)0.0034 (6)0.0022 (6)0.0003 (6)
C150.0061 (8)0.0084 (8)0.0152 (8)0.0010 (6)0.0001 (6)0.0000 (6)
C160.0072 (8)0.0095 (8)0.0103 (8)0.0008 (6)0.0006 (6)0.0024 (6)
C170.0080 (8)0.0093 (8)0.0115 (8)0.0009 (6)0.0000 (6)0.0024 (6)
C180.0090 (8)0.0105 (8)0.0091 (8)0.0012 (6)0.0012 (6)0.0011 (6)
C190.0117 (8)0.0113 (8)0.0091 (8)0.0023 (7)0.0001 (6)0.0011 (6)
C200.0094 (8)0.0107 (8)0.0082 (8)0.0014 (6)0.0012 (6)0.0001 (6)
C210.0070 (8)0.0081 (8)0.0091 (8)0.0007 (6)0.0009 (6)0.0010 (6)
C220.0086 (8)0.0083 (8)0.0093 (8)0.0001 (6)0.0005 (6)0.0001 (6)
C230.0112 (8)0.0102 (8)0.0079 (8)0.0003 (7)0.0003 (6)0.0005 (6)
C240.0071 (8)0.0095 (8)0.0093 (8)0.0002 (6)0.0011 (6)0.0004 (6)
C250.0054 (7)0.0079 (8)0.0093 (8)0.0002 (6)0.0011 (6)0.0009 (6)
C260.0064 (8)0.0090 (8)0.0098 (8)0.0004 (6)0.0008 (6)0.0003 (6)
C270.0090 (8)0.0087 (8)0.0093 (8)0.0008 (6)0.0012 (6)0.0009 (6)
C280.0100 (8)0.0106 (8)0.0089 (8)0.0006 (7)0.0024 (6)0.0017 (6)
N10.0122 (7)0.0086 (7)0.0087 (7)0.0003 (6)0.0002 (6)0.0008 (6)
N20.0079 (7)0.0079 (7)0.0112 (7)0.0008 (5)0.0001 (5)0.0004 (5)
N30.0103 (7)0.0074 (7)0.0080 (7)0.0004 (6)0.0005 (5)0.0004 (5)
N40.0086 (7)0.0084 (7)0.0088 (7)0.0015 (5)0.0003 (5)0.0003 (5)
O10.0168 (6)0.0104 (6)0.0104 (6)0.0005 (5)0.0003 (5)0.0006 (5)
O20.0190 (7)0.0086 (6)0.0117 (6)0.0022 (5)0.0001 (5)0.0010 (5)
O30.0247 (7)0.0132 (6)0.0115 (6)0.0004 (5)0.0031 (5)0.0037 (5)
O40.0152 (6)0.0110 (6)0.0111 (6)0.0003 (5)0.0018 (5)0.0002 (5)
O50.0172 (6)0.0082 (6)0.0096 (6)0.0005 (5)0.0016 (5)0.0004 (5)
O60.0270 (7)0.0093 (6)0.0108 (6)0.0036 (5)0.0029 (5)0.0029 (5)
O70.0153 (6)0.0127 (6)0.0108 (6)0.0022 (5)0.0022 (5)0.0006 (5)
O80.0133 (6)0.0115 (6)0.0126 (6)0.0020 (5)0.0008 (5)0.0026 (5)
O90.0154 (6)0.0116 (6)0.0142 (6)0.0027 (5)0.0016 (5)0.0039 (5)
O100.0199 (7)0.0110 (6)0.0150 (6)0.0052 (5)0.0014 (5)0.0032 (5)
O110.0295 (7)0.0152 (6)0.0085 (6)0.0080 (6)0.0053 (5)0.0013 (5)
O120.0185 (6)0.0098 (6)0.0095 (6)0.0028 (5)0.0014 (5)0.0024 (5)
O130.0193 (7)0.0092 (6)0.0096 (6)0.0051 (5)0.0026 (5)0.0015 (5)
O140.0161 (6)0.0120 (6)0.0088 (6)0.0022 (5)0.0024 (5)0.0006 (5)
O150.0236 (7)0.0125 (6)0.0092 (6)0.0029 (5)0.0010 (5)0.0009 (5)
O160.0206 (7)0.0088 (6)0.0108 (6)0.0020 (5)0.0022 (5)0.0016 (5)
O170.0171 (7)0.0154 (7)0.0123 (6)0.0029 (5)0.0003 (6)0.0010 (5)
O180.0175 (7)0.0242 (8)0.0178 (7)0.0091 (6)0.0042 (6)0.0068 (6)
O190.0143 (7)0.0103 (7)0.0247 (7)0.0012 (6)0.0002 (6)0.0026 (5)
O200.0164 (7)0.0133 (6)0.0116 (6)0.0024 (5)0.0001 (5)0.0013 (5)
O210.0323 (8)0.0115 (7)0.0108 (7)0.0053 (6)0.0008 (6)0.0016 (5)
O220.0384 (9)0.0119 (7)0.0127 (7)0.0064 (6)0.0073 (6)0.0008 (5)
O230.0165 (7)0.0166 (7)0.0128 (7)0.0001 (6)0.0001 (6)0.0041 (5)
O240.0285 (8)0.0130 (7)0.0132 (6)0.0013 (6)0.0066 (6)0.0013 (6)
O250.0204 (7)0.0112 (7)0.0114 (7)0.0028 (5)0.0005 (5)0.0005 (5)
O260.0158 (7)0.0117 (6)0.0255 (7)0.0033 (6)0.0026 (6)0.0011 (6)
O270.0145 (7)0.0110 (6)0.0204 (7)0.0026 (5)0.0013 (5)0.0024 (5)
O280.0222 (8)0.0179 (7)0.0239 (7)0.0028 (6)0.0040 (6)0.0008 (6)
O290.0337 (9)0.0179 (7)0.0101 (7)0.0007 (6)0.0029 (6)0.0014 (5)
Ca10.01094 (16)0.00795 (16)0.00727 (16)0.00073 (13)0.00000 (12)0.00028 (12)
Ca20.01122 (17)0.00735 (16)0.00825 (16)0.00045 (13)0.00028 (12)0.00033 (12)
Ca30.01280 (17)0.00742 (16)0.00802 (16)0.00195 (13)0.00126 (13)0.00085 (12)
Geometric parameters (Å, º) top
C1—O21.256 (2)C28—O151.255 (2)
C1—O11.274 (2)C28—O161.256 (2)
C1—C21.486 (2)N1—H20.86 (2)
C1—Ca2i2.8519 (17)N2—Ca1ii2.5069 (14)
C2—C31.372 (2)N3—H40.86 (2)
C2—N11.379 (2)N4—Ca32.5460 (14)
C3—C41.415 (2)O1—Ca2i2.4812 (12)
C3—H30.9500O2—Ca2i2.5279 (12)
C4—C121.405 (2)O4—Ca1ii2.5928 (12)
C4—C51.445 (2)O5—Ca1ii2.3784 (12)
C5—O31.217 (2)O8—Ca12.3137 (12)
C5—C61.538 (2)O12—Ca32.5703 (12)
C6—O41.216 (2)O13—Ca32.3963 (12)
C6—C71.500 (2)O14—Ca12.2514 (12)
C7—N21.334 (2)O15—Ca22.3522 (12)
C7—C111.411 (2)O17—Ca12.3694 (13)
C8—N21.337 (2)O17—H1710.85 (3)
C8—C91.393 (2)O17—H1720.86 (3)
C8—C131.520 (2)O18—Ca12.3145 (14)
C9—C101.392 (2)O18—H1810.88 (3)
C9—H9A0.9500O18—H1820.84 (3)
C10—C111.414 (2)O19—Ca22.3894 (14)
C10—C141.529 (2)O19—H1910.81 (3)
C11—C121.458 (2)O19—H1920.85 (3)
C12—N11.350 (2)O20—Ca22.4382 (13)
C13—O61.244 (2)O20—H2010.82 (3)
C13—O51.262 (2)O20—H2020.84 (3)
C14—O71.241 (2)O21—Ca22.3824 (14)
C14—O81.260 (2)O21—H2110.80 (3)
C15—O101.255 (2)O21—H2120.85 (3)
C15—O91.261 (2)O22—Ca22.3383 (14)
C15—C161.491 (2)O22—H2210.76 (3)
C16—C171.369 (2)O22—H2220.87 (3)
C16—N31.380 (2)O23—Ca32.4362 (14)
C17—C181.416 (2)O23—H2310.76 (3)
C17—H170.9500O23—H2320.83 (3)
C18—C261.413 (2)O24—Ca32.3607 (13)
C18—C191.425 (2)O24—H2410.81 (3)
C19—O111.229 (2)O24—H2420.82 (3)
C19—C201.530 (2)O25—Ca32.5787 (14)
C20—O121.210 (2)O25—H2510.85 (3)
C20—C211.497 (2)O25—H2520.81 (3)
C21—N41.331 (2)O26—Ca32.3962 (14)
C21—C251.414 (2)O26—H2610.86 (3)
C22—N41.336 (2)O26—H2620.80 (3)
C22—C231.391 (2)O27—Ca32.4924 (14)
C22—C271.517 (2)O27—H2710.85 (3)
C23—C241.399 (2)O27—H2720.83 (3)
C23—H230.9500O28—H2810.89 (4)
C24—C251.416 (2)O28—H2820.83 (4)
C24—C281.531 (2)O29—H2910.84 (3)
C25—C261.468 (2)O29—H2920.79 (3)
C26—N31.349 (2)Ca2—H2122.77 (3)
C27—O141.241 (2)Ca3—H2422.79 (3)
C27—O131.270 (2)
O2—C1—O1122.57 (16)Ca2—O20—H202108.7 (19)
O2—C1—C2119.37 (15)H201—O20—H202111 (3)
O1—C1—C2118.05 (15)Ca2—O21—H211131.1 (19)
O2—C1—Ca2i62.38 (9)Ca2—O21—H212108.2 (18)
O1—C1—Ca2i60.30 (9)H211—O21—H212104 (2)
C2—C1—Ca2i174.96 (12)Ca2—O22—H221122 (2)
C3—C2—N1108.35 (15)Ca2—O22—H222133.1 (18)
C3—C2—C1131.39 (16)H221—O22—H222105 (3)
N1—C2—C1120.24 (15)Ca3—O23—H231115.6 (19)
C2—C3—C4106.75 (15)Ca3—O23—H232116.1 (18)
C2—C3—H3126.6H231—O23—H232108 (3)
C4—C3—H3126.6Ca3—O24—H241125.7 (19)
C12—C4—C3107.73 (15)Ca3—O24—H242113.0 (19)
C12—C4—C5122.41 (15)H241—O24—H242104 (3)
C3—C4—C5129.85 (15)Ca3—O25—H251114.2 (18)
O3—C5—C4126.34 (16)Ca3—O25—H252106 (2)
O3—C5—C6118.97 (15)H251—O25—H252106 (3)
C4—C5—C6114.67 (14)Ca3—O26—H261131 (2)
O4—C6—C7120.52 (15)Ca3—O26—H262115.5 (19)
O4—C6—C5120.10 (15)H261—O26—H262105 (3)
C7—C6—C5119.34 (14)Ca3—O27—H271122.3 (18)
N2—C7—C11124.30 (15)Ca3—O27—H272112.4 (17)
N2—C7—C6113.14 (14)H271—O27—H272107 (2)
C11—C7—C6122.55 (15)H281—O28—H282103 (3)
N2—C8—C9121.27 (15)H291—O29—H292107 (3)
N2—C8—C13115.32 (14)O14—Ca1—O8110.58 (4)
C9—C8—C13123.41 (15)O14—Ca1—O1883.93 (5)
C10—C9—C8120.33 (15)O8—Ca1—O18160.87 (5)
C10—C9—H9A119.8O14—Ca1—O1781.08 (5)
C8—C9—H9A119.8O8—Ca1—O1784.33 (5)
C9—C10—C11118.83 (15)O18—Ca1—O17110.98 (5)
C9—C10—C14115.60 (14)O14—Ca1—O5ii147.08 (4)
C11—C10—C14125.56 (15)O8—Ca1—O5ii92.68 (4)
C7—C11—C10116.10 (15)O18—Ca1—O5ii79.85 (5)
C7—C11—C12115.64 (14)O17—Ca1—O5ii78.35 (4)
C10—C11—C12128.24 (15)O14—Ca1—N2ii139.18 (5)
N1—C12—C4106.95 (15)O8—Ca1—N2ii80.01 (4)
N1—C12—C11127.93 (15)O18—Ca1—N2ii80.87 (5)
C4—C12—C11125.07 (15)O17—Ca1—N2ii139.74 (5)
O6—C13—O5126.02 (15)O5ii—Ca1—N2ii65.71 (4)
O6—C13—C8117.71 (14)O14—Ca1—O4ii79.80 (4)
O5—C13—C8116.27 (14)O8—Ca1—O4ii80.92 (4)
O7—C14—O8126.49 (15)O18—Ca1—O4ii89.87 (5)
O7—C14—C10116.37 (15)O17—Ca1—O4ii149.89 (4)
O8—C14—C10117.05 (14)O5ii—Ca1—O4ii128.25 (4)
O10—C15—O9126.01 (16)N2ii—Ca1—O4ii62.59 (4)
O10—C15—C16115.89 (15)O22—Ca2—O15148.18 (5)
O9—C15—C16118.07 (15)O22—Ca2—O2178.62 (5)
C17—C16—N3108.57 (14)O15—Ca2—O2177.75 (5)
C17—C16—C15129.10 (15)O22—Ca2—O1981.60 (5)
N3—C16—C15122.28 (15)O15—Ca2—O1987.27 (5)
C16—C17—C18106.85 (15)O21—Ca2—O19110.91 (5)
C16—C17—H17126.6O22—Ca2—O2098.71 (5)
C18—C17—H17126.6O15—Ca2—O2098.27 (5)
C26—C18—C17107.48 (14)O21—Ca2—O2080.94 (5)
C26—C18—C19122.96 (15)O19—Ca2—O20167.84 (5)
C17—C18—C19129.55 (15)O22—Ca2—O1iii127.21 (5)
O11—C19—C18127.61 (16)O15—Ca2—O1iii81.48 (4)
O11—C19—C20118.19 (15)O21—Ca2—O1iii151.55 (5)
C18—C19—C20114.20 (14)O19—Ca2—O1iii87.10 (5)
O12—C20—C21121.02 (15)O20—Ca2—O1iii83.06 (4)
O12—C20—C19118.84 (15)O22—Ca2—O2iii75.46 (5)
C21—C20—C19120.12 (14)O15—Ca2—O2iii133.97 (4)
N4—C21—C25124.89 (15)O21—Ca2—O2iii145.39 (5)
N4—C21—C20112.30 (14)O19—Ca2—O2iii87.61 (5)
C25—C21—C20122.68 (15)O20—Ca2—O2iii80.74 (4)
N4—C22—C23121.19 (15)O1iii—Ca2—O2iii52.58 (4)
N4—C22—C27114.53 (14)O22—Ca2—C1iii101.03 (5)
C23—C22—C27124.27 (15)O15—Ca2—C1iii107.87 (5)
C22—C23—C24120.98 (15)O21—Ca2—C1iii162.54 (5)
C22—C23—H23119.5O19—Ca2—C1iii86.13 (5)
C24—C23—H23119.5O20—Ca2—C1iii81.88 (5)
C23—C24—C25118.04 (15)O1iii—Ca2—C1iii26.49 (4)
C23—C24—C28115.57 (14)O2iii—Ca2—C1iii26.12 (4)
C25—C24—C28126.36 (14)O22—Ca2—H21294.6 (6)
C21—C25—C24115.99 (15)O15—Ca2—H21260.7 (6)
C21—C25—C26114.23 (14)O21—Ca2—H21217.0 (6)
C24—C25—C26129.67 (15)O19—Ca2—H212107.9 (6)
N3—C26—C18106.92 (14)O20—Ca2—H21284.2 (6)
N3—C26—C25127.74 (15)O1iii—Ca2—H212137.7 (6)
C18—C26—C25125.34 (15)O2iii—Ca2—H212160.4 (6)
O14—C27—O13124.61 (15)C1iii—Ca2—H212160.5 (6)
O14—C27—C22118.79 (14)O24—Ca3—O2683.48 (5)
O13—C27—C22116.58 (14)O24—Ca3—O13161.79 (5)
O15—C28—O16125.31 (15)O26—Ca3—O1385.73 (5)
O15—C28—C24114.92 (14)O24—Ca3—O2382.50 (5)
O16—C28—C24119.76 (14)O26—Ca3—O23144.90 (5)
C12—N1—C2110.20 (15)O13—Ca3—O2398.26 (5)
C12—N1—H2124.5 (14)O24—Ca3—O2796.15 (5)
C2—N1—H2124.9 (14)O26—Ca3—O2775.13 (5)
C7—N2—C8119.04 (14)O13—Ca3—O2795.21 (4)
C7—N2—Ca1ii123.03 (11)O23—Ca3—O27138.35 (5)
C8—N2—Ca1ii117.70 (11)O24—Ca3—N4132.11 (5)
C26—N3—C16110.18 (14)O26—Ca3—N4137.02 (5)
C26—N3—H4119.6 (16)O13—Ca3—N464.53 (4)
C16—N3—H4129.8 (16)O23—Ca3—N473.39 (5)
C21—N4—C22118.67 (14)O27—Ca3—N477.41 (5)
C21—N4—Ca3122.66 (11)O24—Ca3—O1270.98 (4)
C22—N4—Ca3118.65 (11)O26—Ca3—O12134.27 (5)
C1—O1—Ca2i93.21 (10)O13—Ca3—O12126.46 (4)
C1—O2—Ca2i91.50 (10)O23—Ca3—O1269.44 (4)
C6—O4—Ca1ii120.35 (11)O27—Ca3—O1270.85 (4)
C13—O5—Ca1ii124.78 (10)N4—Ca3—O1262.01 (4)
C14—O8—Ca1146.93 (11)O24—Ca3—O2581.28 (5)
C20—O12—Ca3121.20 (11)O26—Ca3—O2573.38 (5)
C27—O13—Ca3125.58 (10)O13—Ca3—O2581.59 (4)
C27—O14—Ca1161.86 (11)O23—Ca3—O2572.78 (5)
C28—O15—Ca2139.74 (11)O27—Ca3—O25148.49 (5)
Ca1—O17—H171115.5 (18)N4—Ca3—O25127.07 (4)
Ca1—O17—H172125.2 (16)O12—Ca3—O25135.26 (4)
H171—O17—H172107 (2)O24—Ca3—H24215.8 (6)
Ca1—O18—H181117.1 (16)O26—Ca3—H24298.7 (6)
Ca1—O18—H182129 (2)O13—Ca3—H242168.8 (6)
H181—O18—H182113 (3)O23—Ca3—H24272.2 (6)
Ca2—O19—H191125.4 (19)O27—Ca3—H24295.9 (6)
Ca2—O19—H192123.7 (18)N4—Ca3—H242116.6 (6)
H191—O19—H192109 (3)O12—Ca3—H24256.6 (6)
Ca2—O20—H201112 (2)O25—Ca3—H24289.7 (6)
O2—C1—C2—C34.2 (3)C27—C22—C23—C24179.30 (15)
O1—C1—C2—C3177.26 (18)C22—C23—C24—C252.2 (2)
O2—C1—C2—N1174.51 (15)C22—C23—C24—C28175.81 (15)
O1—C1—C2—N14.0 (2)N4—C21—C25—C243.8 (2)
N1—C2—C3—C40.1 (2)C20—C21—C25—C24171.68 (15)
C1—C2—C3—C4178.94 (18)N4—C21—C25—C26179.55 (15)
C2—C3—C4—C120.2 (2)C20—C21—C25—C265.0 (2)
C2—C3—C4—C5179.25 (18)C23—C24—C25—C214.9 (2)
C12—C4—C5—O3177.69 (17)C28—C24—C25—C21172.84 (15)
C3—C4—C5—O31.7 (3)C23—C24—C25—C26179.05 (16)
C12—C4—C5—C63.6 (2)C28—C24—C25—C263.2 (3)
C3—C4—C5—C6176.96 (17)C17—C18—C26—N30.23 (19)
O3—C5—C6—O47.4 (3)C19—C18—C26—N3179.13 (15)
C4—C5—C6—O4171.33 (16)C17—C18—C26—C25179.41 (15)
O3—C5—C6—C7174.98 (16)C19—C18—C26—C251.2 (3)
C4—C5—C6—C76.2 (2)C21—C25—C26—N3179.48 (16)
O4—C6—C7—N25.9 (2)C24—C25—C26—N34.4 (3)
C5—C6—C7—N2176.54 (14)C21—C25—C26—C180.1 (2)
O4—C6—C7—C11173.13 (16)C24—C25—C26—C18176.01 (16)
C5—C6—C7—C114.4 (2)N4—C22—C27—O14176.56 (15)
N2—C8—C9—C103.1 (3)C23—C22—C27—O144.9 (2)
C13—C8—C9—C10177.06 (15)N4—C22—C27—O132.0 (2)
C8—C9—C10—C113.0 (2)C23—C22—C27—O13176.54 (15)
C8—C9—C10—C14175.77 (15)C23—C24—C28—O1528.3 (2)
N2—C7—C11—C102.8 (3)C25—C24—C28—O15149.54 (17)
C6—C7—C11—C10178.32 (15)C23—C24—C28—O16150.92 (16)
N2—C7—C11—C12178.55 (15)C25—C24—C28—O1631.3 (2)
C6—C7—C11—C120.4 (2)C4—C12—N1—C20.58 (19)
C9—C10—C11—C70.2 (2)C11—C12—N1—C2178.32 (16)
C14—C10—C11—C7178.43 (15)C3—C2—N1—C120.5 (2)
C9—C10—C11—C12178.31 (16)C1—C2—N1—C12179.42 (15)
C14—C10—C11—C123.1 (3)C11—C7—N2—C82.7 (3)
C3—C4—C12—N10.49 (19)C6—C7—N2—C8178.26 (14)
C5—C4—C12—N1179.02 (16)C11—C7—N2—Ca1ii171.66 (12)
C3—C4—C12—C11178.31 (16)C6—C7—N2—Ca1ii7.34 (19)
C5—C4—C12—C111.2 (3)C9—C8—N2—C70.3 (2)
C7—C11—C12—N1179.28 (16)C13—C8—N2—C7179.89 (15)
C10—C11—C12—N12.2 (3)C9—C8—N2—Ca1ii175.00 (12)
C7—C11—C12—C43.4 (2)C13—C8—N2—Ca1ii5.19 (19)
C10—C11—C12—C4175.13 (17)C18—C26—N3—C160.16 (19)
N2—C8—C13—O6175.07 (15)C25—C26—N3—C16179.48 (16)
C9—C8—C13—O64.7 (3)C17—C16—N3—C260.02 (19)
N2—C8—C13—O54.8 (2)C15—C16—N3—C26177.55 (15)
C9—C8—C13—O5175.37 (16)C25—C21—N4—C220.5 (2)
C9—C10—C14—O742.5 (2)C20—C21—N4—C22176.42 (14)
C11—C10—C14—O7138.90 (17)C25—C21—N4—Ca3177.66 (12)
C9—C10—C14—O8134.37 (16)C20—C21—N4—Ca31.78 (18)
C11—C10—C14—O844.3 (2)C23—C22—N4—C213.7 (2)
O10—C15—C16—C178.1 (3)C27—C22—N4—C21177.79 (14)
O9—C15—C16—C17170.08 (16)C23—C22—N4—Ca3174.62 (12)
O10—C15—C16—N3174.93 (15)C27—C22—N4—Ca33.93 (18)
O9—C15—C16—N36.9 (2)O2—C1—O1—Ca2i3.95 (18)
N3—C16—C17—C180.13 (18)C2—C1—O1—Ca2i174.56 (14)
C15—C16—C17—C18177.18 (16)O1—C1—O2—Ca2i3.87 (17)
C16—C17—C18—C260.22 (19)C2—C1—O2—Ca2i174.62 (14)
C16—C17—C18—C19179.08 (17)C7—C6—O4—Ca1ii1.8 (2)
C26—C18—C19—O11178.07 (17)C5—C6—O4—Ca1ii179.39 (11)
C17—C18—C19—O112.7 (3)O6—C13—O5—Ca1ii177.84 (13)
C26—C18—C19—C202.1 (2)C8—C13—O5—Ca1ii2.1 (2)
C17—C18—C19—C20177.06 (16)O7—C14—O8—Ca197.5 (2)
O11—C19—C20—O127.9 (2)C10—C14—O8—Ca179.0 (2)
C18—C19—C20—O12171.94 (15)C21—C20—O12—Ca310.8 (2)
O11—C19—C20—C21173.47 (15)C19—C20—O12—Ca3170.58 (11)
C18—C19—C20—C216.7 (2)O14—C27—O13—Ca3179.65 (12)
O12—C20—C21—N46.0 (2)C22—C27—O13—Ca31.2 (2)
C19—C20—C21—N4175.40 (14)O13—C27—O14—Ca1135.4 (3)
O12—C20—C21—C25170.03 (15)C22—C27—O14—Ca146.2 (4)
C19—C20—C21—C258.6 (2)O16—C28—O15—Ca214.3 (3)
N4—C22—C23—C242.3 (3)C24—C28—O15—Ca2164.88 (12)
Symmetry codes: (i) x1, y, z; (ii) x+1, y+1, z+1; (iii) x+1, y, z.
Hydrogen-bond geometry (Å, º) top
D—H···AD—HH···AD···AD—H···A
N1—H2···O80.86 (2)2.01 (2)2.7232 (19)139.6 (19)
N3—H4···O160.86 (2)1.83 (2)2.6163 (19)151 (2)
O17—H171···O10iv0.85 (3)1.91 (3)2.7543 (18)170 (3)
O17—H172···O10.86 (3)2.08 (3)2.9287 (19)170 (2)
O18—H181···O280.88 (3)1.82 (3)2.681 (2)166 (2)
O18—H182···O1iii0.84 (3)1.97 (3)2.8107 (19)176 (3)
O19—H191···O20i0.81 (3)2.10 (3)2.8789 (19)161 (3)
O19—H192···O5ii0.85 (3)1.89 (3)2.7350 (18)174 (3)
O20—H201···O11v0.82 (3)2.00 (3)2.8221 (18)173 (3)
O20—H202···O2vi0.84 (3)1.94 (3)2.7620 (18)169 (3)
O21—H211···O29iv0.80 (3)2.05 (3)2.845 (2)173 (3)
O21—H212···O160.85 (3)1.90 (3)2.7320 (18)163 (3)
O22—H221···O19vi0.76 (3)2.26 (3)2.958 (2)152 (3)
O22—H222···O6vii0.87 (3)1.83 (3)2.6985 (19)175 (3)
O23—H231···O3viii0.76 (3)2.10 (3)2.8398 (19)164 (3)
O23—H232···O9iv0.83 (3)1.90 (3)2.7217 (19)169 (3)
O24—H241···O7ix0.81 (3)2.03 (3)2.8040 (19)163 (3)
O24—H242···O290.82 (3)1.93 (3)2.750 (2)172 (3)
O25—H251···O13ix0.85 (3)2.02 (3)2.8578 (18)168 (3)
O25—H252···O3viii0.81 (3)2.41 (3)3.0258 (19)133 (2)
O25—H252···O4viii0.81 (3)2.28 (3)3.0405 (18)155 (3)
O26—H261···O27x0.86 (3)2.11 (3)2.9018 (19)154 (3)
O26—H262···O13ix0.80 (3)2.06 (3)2.8506 (19)170 (3)
O27—H271···O25iii0.85 (3)2.08 (3)2.9022 (19)164 (3)
O27—H272···O9v0.83 (3)1.99 (3)2.8125 (18)171 (2)
O28—H281···O10v0.89 (4)1.88 (4)2.721 (2)159 (3)
O28—H282···O26x0.83 (4)2.59 (3)3.098 (2)121 (3)
O29—H291···O6ix0.84 (3)1.85 (3)2.6582 (19)160 (3)
O29—H292···O110.79 (3)2.27 (3)3.021 (2)159 (3)
O29—H292···O120.79 (3)2.40 (3)2.7789 (19)110 (2)
Symmetry codes: (i) x1, y, z; (ii) x+1, y+1, z+1; (iii) x+1, y, z; (iv) x+1, y, z; (v) x+2, y, z; (vi) x+1, y, z+1; (vii) x, y1, z; (viii) x, y, z1; (ix) x+1, y+1, z; (x) x+2, y+1, z.
Selected bond lengths (Å) of the Ca3PQQ2.13H2O complex in comparison with the previously published Eu2PQQ2.12H2O structure top
For symmetry data for Eu2PQQ2.12H2O, please see (Lumpe et al., 2020).
Ca3PQQ2.13H2OEu2PQQ2.12H2O
Ca1i—O42.5928 (12)Eu1—O42.584 (2)
Ca1i—N22.5069 (14)Eu1—N22.648 (2)
Ca1i—O52.3784 (12)Eu1—O52.440 (2)
Ca1—O142.2514 (12)Eu1—O12.409 (2)
Ca1—O82.3137 (12)Eu1—Owater (5 bonds)2.389 (2)–2.464 (2)
Ca1—O172.3694 (13)
Ca1—O182.3145 (14)Ca3—O122.5703 (12)
Ca2ii—O12.4812 (12)Ca3—N42.5460 (14)
Ca2ii—O22.5279 (12)Ca3—O132.3963 (12)
Ca2—O152.3522 (12)Ca3—O232.4362 (14)
Ca2—O192.3894 (14)Ca3—O242.3607 (13)
Ca2—O202.4382 (13)Ca3—O252.5787 (14)
Ca2—O212.3824 (14)Ca3—O262.3962 (14)
Ca2—O222.3383 (14)Ca3—O272.4924 (14)
Symmetry codes: (i) -x+1, -y+1, -z+1; (ii) x-1, y, z.
 

Footnotes

1Dedicated to Professor Wolfgang Kaim on the occasion of his 70th birthday.

Acknowledgements

Open access funding enabled and organized by Projekt DEAL.

Funding information

Funding for this research was provided by: Deutsche Forschungsgemeinschaft (grant No. 392552271 to LJD).

References

First citationAnthony, C. & Zatman, L. J. (1964a). Biochem. J. 92, 609–614.  CrossRef CAS PubMed Web of Science Google Scholar
First citationAnthony, C. & Zatman, L. J. (1964b). Biochem. J. 92, 614–621.  CrossRef CAS PubMed Web of Science Google Scholar
First citationBlake, C. C. F., Ghosh, M., Harlos, K., Avezoux, A. & Anthony, C. (1994). Nat. Struct. Mol. Biol. 1, 102–105.  CrossRef CAS Web of Science Google Scholar
First citationBogart, J. A., Lewis, A. J. & Schelter, E. J. (2015). Chem. Eur. J. 21, 1743–1748.  Web of Science CrossRef CAS PubMed Google Scholar
First citationBruker (2016). APEX3 and SADABS. Bruker AXS Inc., Madison, Wisconsin, USA.  Google Scholar
First citationBruker (2017). SAINT. Bruker AXS Inc., Madison, Wisconsin, USA.  Google Scholar
First citationCheisson, T. & Schelter, E. J. (2019). Science, 363, 489–493.  Web of Science CrossRef CAS PubMed Google Scholar
First citationChistoserdova, L. (2019). Mol. Microbiol. 111, 1127–1131.  Web of Science CrossRef CAS PubMed Google Scholar
First citationCorey, E. J. & Tramontano, A. (1981). J. Am. Chem. Soc. 103, 5599–5600.  CrossRef CAS Web of Science Google Scholar
First citationCotruvo, J. A. (2019). ACS Cent. Sci. 9, 1496–1506.  Web of Science CrossRef Google Scholar
First citationDaumann, L. J. (2019). Angew. Chem. Int. Ed. 58, 12795–12802.  Web of Science CrossRef CAS Google Scholar
First citationDekker, R. H., Duine, J. A., Frank, J., Verwiel, P. E. J. & Westerling, J. (1982). Eur. J. Biochem. 125, 69–73.  CrossRef CAS PubMed Web of Science Google Scholar
First citationDuine, J. A., Frank, J. & Westerling, J. (1978). Biochim. Biophys. Acta Enzymol. 524, 277–287.  CrossRef CAS Web of Science Google Scholar
First citationEckert, T. S., Bruice, T. C., Gainor, J. A. & Weinreb, S. M. (1982). Proc. Natl Acad. Sci. USA, 79, 2533–2536.  CrossRef CAS PubMed Web of Science Google Scholar
First citationFarrugia, L. J. (2012). J. Appl. Cryst. 45, 849–854.  Web of Science CrossRef CAS IUCr Journals Google Scholar
First citationIkemoto, K., Sakamoto, H. & Nakano, M. (2012). Chem. Cent. J. 6, 57.  Web of Science CSD CrossRef PubMed Google Scholar
First citationIkemoto, K., Sakamoto, Y., Tanaka, R., Ogata, K., Matsushita, N. & Nakamura, S. (2017). Cryst. Growth Des. 17, 4118–4123.  Web of Science CSD CrossRef CAS Google Scholar
First citationIshida, T., Doi, M., Tomita, K., Hayashi, H., Inoue, M. & Urakami, T. (1989). J. Am. Chem. Soc. 111, 6822–6828.  CSD CrossRef CAS Web of Science Google Scholar
First citationItoh, S., Kawakami, H. & Fukuzumi, S. (1997). J. Am. Chem. Soc. 119, 439–440.  CrossRef CAS Web of Science Google Scholar
First citationItoh, S., Kawakami, H. & Fukuzumi, S. (1998). Biochemistry, 37, 6562–6571.  Web of Science CrossRef CAS PubMed Google Scholar
First citationItoh, S., Kawakami, H. & Fukuzumi, S. (2000). J. Mol. Catal. B Enzym. 8, 85–94.  Web of Science CrossRef CAS Google Scholar
First citationKeltjens, J. T., Pol, A., Reimann, J. & Op den Camp, H. J. M. (2014). Appl. Microbiol. Biotechnol. 98, 6163–6183.  Web of Science CrossRef CAS PubMed Google Scholar
First citationKoningsveld, H. van, Jansen, J. C., Jongejan, J. A., Frank, J. Jzn. & Duine, J. A. (1985). Acta Cryst. C41, 89–92.  CSD CrossRef Web of Science IUCr Journals Google Scholar
First citationLumpe, H. & Daumann, L. J. (2019). Inorg. Chem. 58, 8432–8441.  Web of Science CrossRef CAS PubMed Google Scholar
First citationLumpe, H., Menke, A., Haisch, C., Mayer, P., Kabelitz, A., Yusenko, K. V., Guilherme Buzanich, A., Block, T., Pöttgen, R., Emmerling, F. & Daumann, L. J. (2020). Chem. Eur. J. 26, 10133–10139.  CSD CrossRef CAS PubMed Google Scholar
First citationLumpe, H., Pol, A., Op den Camp, H. J. M. & Daumann, L. J. (2018). Dalton Trans. 47, 10463–10472.  Web of Science CrossRef CAS PubMed Google Scholar
First citationMitome, H., Ishizuka, T., Shiota, Y., Yoshizawa, K. & Kojima, T. (2013). Inorg. Chem. 52, 2274–2276.  Web of Science CSD CrossRef CAS PubMed Google Scholar
First citationMitome, H., Ishizuka, T., Shiota, Y., Yoshizawa, K. & Kojima, T. (2015). Dalton Trans. 44, 3151–3158.  Web of Science CSD CrossRef CAS PubMed Google Scholar
First citationNakamura, N., Kohzuma, T., Kuma, H. & Suzuki, S. (1994). Inorg. Chem. 33, 1594–1599.  CSD CrossRef CAS Web of Science Google Scholar
First citationNoar, J. B., Rodriguez, E. J. & Bruice, T. C. (1985). J. Am. Chem. Soc. 107, 7198–7199.  CrossRef CAS Web of Science Google Scholar
First citationPicone, N. & Op den Camp, H. J. M. (2019). Curr. Opin. Chem. Biol. 49, 39–44.  Web of Science CrossRef CAS PubMed Google Scholar
First citationPol, A., Barends, T. R. M., Dietl, A., Khadem, A. F., Eygensteyn, J., Jetten, M. S. M. & Op den Camp, H. J. M. (2014). Environ. Microbiol. 16, 255–264.  Web of Science CrossRef CAS PubMed Google Scholar
First citationRamachandran, A. & Walsh, D. A. (2015). FEMS Microbiol. Ecol. 91, fiv105/1–fiv105/10.  Google Scholar
First citationSalisbury, S. A., Forrest, H. S., Cruse, W. B. T. & Kennard, O. (1979). Nature, 280, 843–844.  CrossRef CAS PubMed Web of Science Google Scholar
First citationSemrau, J. D., DiSpirito, A. A., Gu, W. & Yoon, S. (2018). Appl. Environ. Microbiol. 84, e02289-17.  Web of Science CrossRef PubMed Google Scholar
First citationShannon, R. D. (1976). Acta Cryst. A32, 751–767.  CrossRef CAS IUCr Journals Web of Science Google Scholar
First citationSheldrick, G. M. (2015). Acta Cryst. C71, 3–8.  Web of Science CrossRef IUCr Journals Google Scholar
First citationSkovran, E. & Martinez-Gomez, N. C. (2015). Science, 348, 862–863.  Web of Science CrossRef CAS PubMed Google Scholar
First citationTaubert, M., Grob, C., Howat, A. M., Burns, O. J., Dixon, J. L., Chen, Y. & Murrell, J. C. (2015). Environ. Microbiol. 17, 3937–3948.  Web of Science CrossRef CAS PubMed Google Scholar
First citationTommasi, L., Shechter-Barloy, L., Varech, D., Battioni, J. P., Donnadieu, B., Verelst, M., Bousseksou, A., Mansuy, D. & Tuchagues, J. P. (1995). Inorg. Chem. 34, 1514–1523.  CSD CrossRef CAS Web of Science Google Scholar
First citationWanner, M., Sixt, T., Klinkhammer, K.-W. & Kaim, W. (1999). Inorg. Chem. 38, 2753–2755.  Web of Science CSD CrossRef CAS Google Scholar
First citationWesterling, J., Frank, J. & Duine, J. A. (1979). Biochem. Biophys. Res. Commun. 87, 719–724.  CrossRef CAS PubMed Web of Science Google Scholar
First citationWilliams, P. A., Coates, L., Mohammed, F., Gill, R., Erskine, P. T., Coker, A., Wood, S. P., Anthony, C. & Cooper, J. B. (2005). Acta Cryst. D61, 75–79.  Web of Science CrossRef CAS IUCr Journals Google Scholar
First citationZhejiang Hisun Pharmaceutical Co. Ltd (2020). GRAS Exemption Claim for Pyrrolo­quinoline Quinone (PQQ) Disodium Salt; https://www.fda.gov/downloads/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm508141.pdfGoogle Scholar

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