Concerto catalysis - Harmonising [NiFe]hydrogenase and NiRu model catalysts

Article abstract of DOI:10.1039/b926061g

This communication reports the successful merging of the chemical properties of a natural [NiFe]hydrogenase (Desulfovibrio vulgaris Miyazaki F) and our previously reported [NiRu] hydrogenase-mimic. The catalytic activity of both the natural enzyme and the mimic is almost identical, with the exception of working pH ranges, and this allows us to use them simultaneously in the same reaction flask. In such a manner, isotope exchange between D₂ and H₂O could be conducted over an extended pH range (about 2-10) in one pot under mild conditions at ambient temperature and pressure.

Full text of DOI:10.1039/b926061g

View Online / Journal Homepage / Table of Contents for this issue
This paper is published as part of a Dalton Transactions themed issue on:
Bioinspired Catalysis
Guest Editor Seiji Ogo
Kyushu University, Japan
Published in issue 12, 2010 of Dalton Transactions
Image reproduced with permission of Seiji Ogo
Articles published in this issue include:
PERSPECTIVES:
Mimicking Nitrogenase
Ian Dance
Dalton Trans., 2010, DOI: 10.1039/b922606k
Dual functions of NifEN: insights into the evolution and mechanism of nitrogenase
Yilin Hu, Aaron W. Fay, Chi Chung Lee, Jared A. Wiig and Markus W. Ribbe
Dalton Trans., 2010, DOI: 10.1039/b922555b
Quest for metal/NH bifunctional biomimetic catalysis in a dinuclear platform
Takao Ikariya and Shigeki Kuwata
Dalton Trans., 2010, DOI: 10.1039/b927357c
COMMUNICATION:
Chemiluminescence enhancement and energy transfer by the aluminium(III) complex of an
amphiphilic/bipolar and cell-penetrating corrole
Atif Mahammed and Zeev Gross
Dalton Trans., 2010, DOI: 10.1039/b916590h
Visit the Dalton Transactions website for more cutting-edge inorganic and bioinorganic research
www.rsc.org/dalton

Dalton
Transactions
An international journal of inorganic chemistry
www.rsc.org/dalton
Volume 39 | Number 12 | 28 March 2010 | Pages 2949–3136
Themed issue on Bioinspired Catalysis
ISSN 1477-9226
COMMUNICATION
Ogo et al.
Concerto catalysis—harmonising [NiFe] PERSPECTIVE
hydrogenase and
NiRu model catalysts
Dance
Mimicking nitrogenase
1477-9226(2010)39:12;1-A

COMMUNICATION
www.rsc.org/dalton | Dalton Transactions
Concerto catalysis—harmonising [NiFe]hydrogenase and NiRu model
catalysts†
Koji Ichikawa, Kyoshiro Nonaka, Takahiro Matsumoto, Bunsho Kure,a,b Ki-Seok Yoon,a,b
a
a
a,b
b,c
d
a,b
Yoshiki Higuchi, Tatsuhiko Yagi and Seiji Ogo*
Received 10th December 2009, Accepted 5th January 2010
First published as an Advance Article on the web 12th January 2010
DOI: 10.1039/b926061g
This communication reports the successful merging of the
chemical properties of a natural [NiFe]hydrogenase (Desul-
fovibrio vulgaris Miyazaki F) and our previously reported
produces the three chemically significant properties of natural
3,5
[NiFe]H
2
ases and we have proposed a detailed mechanism in
4
a previous report.
[
NiRu] hydrogenase-mimic. The catalytic activity of both the
Concerto catalysis also incorporates the concept of making
use of harmonious properties of complementary catalysts. In
this communication, we present the complementary, simultaneous
natural enzyme and the mimic is almost identical, with the
exception of working pH ranges, and this allows us to use
them simultaneously in the same reaction flask. In such a
manner, isotope exchange between D
conducted over an extended pH range (about 2–10) in one pot
under mild conditions at ambient temperature and pressure.
action of the natural [NiFe]H
Miyazaki F) and our catalyst 1 (Fig. 1). This harmonious action
results in the simultaneous exchange of D and H O over a wide
2
ase (from Desulfovibrio vulgaris
2
and H O could be
2
2
2
range of pH at ambient temperature and pressure in a one-pot
system. The complementary properties of the individual catalysts
result in a more versatile catalytic system.
‘Concerto catalysis’ is a new way of thinking in catalysis that
unites all scales of catalytic assemblies. These assemblies could
be in the form of bulk, solid-phase catalysts; discrete biological
macromolecules—weighing thousands of Daltons—or down to
small ‘micro’ molecules—weighing only a few hundred Daltons.
Traditionally, these three scales form distinct fields of research with
little or no interdisciplinary communication. Concerto catalysis,
however, enables us to build a conceptual framework to unite
common concepts across these fields, which will lead to the
development of new, exciting catalysts.
The concepts of concerto catalysis have helped us to develop
a small scale mimic of [NiFe]hydrogenases ([NiFe]H
2
ases). As
the name implies, [NiFe]H ases are based around an active NiFe
2
1-3
bimetallic core and such knowledge translates readily to the
environs of the inorganic chemical laboratory. By replacing the
Fe centre with a Ru ion and mimicking the chemical environment
of the natural NiFe centre with artificial ligands, we were able
II
to make the water-soluble, acid-stable complex [Ni L(H
2
O)(m-
Fig. 1 pH-dependent hydrogen isotope exchange reaction between
gaseous isotopes and medium isotopes catalysed by the Ni(m-H)Ru
complex 1 and [NiFe]H ase.
2
II
6
H)Ru (h -C
6
Me
6
)](NO
3
) {[1](NO
3
), L = N,N¢-dimethyl-N,N¢-
4
bis(2-mercaptoethyl)-1,3-propanediamine}. This compound re-
a
To investigate the possibility of combining the artificial and
natural catalysts, we first performed isotope exchange experiments
Department of Chemistry and Biochemistry, Graduate School of Engineer-
ing, Kyushu University, 744 Moto-oka, Nishi-ku, Fukuoka, 819-0395, Japan.
E-mail: ogotcm@mail.cstm.kyushu-u.ac.jp; Fax: 81 92 802 3307; Tel: 81 92
using the NiRu complex 1. In this case, D
a solution of 1 in H O and the volumes of the generated gases, H
and HD, were measured. The results of this analysis are shown in
Fig. 2, which depicts the pH-dependent generation of H (closed
circle) and HD (open circle) in the reaction of 1 with D in H O at
2
was bubbled through
8
02 2818
2
2
b
Core Research for Evolutional Science and Technology (CREST), Japan
Science and Technology Agency (JST), Kawaguchi Center Building, 4-1-8
Honcho, Kawaguchi-shi, Saitama, 332-0012, Japan
2
c
Department of Life Science, Graduate School of Life Science, University of
2
2
Hyogo, Koto, Kamigori, Hyogo, 678-1297, Japan
◦
3
7 C for 1 h. There are three points of note, specifically, that the
generation of H and HD are simultaneous, as found in natural
ases, that the maximum activity occurs at about pH 4 and that
d
Shizuoka University, 836 Oya, Shizuoka, 422-8529, Japan
2
†
Electronic supplementary information (ESI) available: Experimental de-
tails for materials and methods, synthesis and characterisation of [1](NO ),
typical procedure for hydrogen isotope exchange reaction between gaseous
isotopes and medium isotopes catalysed by [1](NO ), [NiFe]H ase and
·H ase {[1](NO ) and [NiFe]H ase} and reaction of methyl viologen
[MV] ) with H catalysed by [1](NO ) (Fig. S1a), [NiFe]H ase (Fig.
S1b) and 1·H ase {[1](NO ) and [NiFe]H ase} (Fig. S1c). See DOI:
0.1039/b926061g
H
2
3
the working pH range of the system is about 2 to 5.
Thereafter, isotope exchange experiments were performed using
3
2
1
(
2
3
2
the natural [NiFe]H
2
ase. This natural H ase showed almost
2
2+
2
3
2
identical behaviour to that of the artificial catalyst with the
exception of a broader working pH range and a shift in maximum
2
3
2
1
This journal is © The Royal Society of Chemistry 2010
Dalton Trans., 2010, 39, 2993–2994 | 2993

Fig. 2 pH-dependent generation of H
2
(closed circle) and HD (open
Fig. 4 pH-dependent generation of H
circle) in the reaction of [1](NO ) (1.0 mmol) and [NiFe]H
with D (2.3 mL 0.10 MPa) in H
2
(closed circle) and HD (open
circle) in the reaction of [1](NO
in H
3
) (1.0 mmol) with D
2
(2.3 mL, 0.10 MPa)
3
2
ase (0.10 nmol)
◦
◦
2
O buffer solution (1.0 mL) at 37 C for 1 h.
2
2
O buffer solution (1.0 mL) at 37 C for
1
h.
activity to about pH 7 (Fig. 3). This system has a working pH
range of about 4 to 10.
“
Development of the Foundation for Nano-Interface Technology”
from JST, Japan.
References
1
(a) A. Volbeda, M. H. Charon, C. Piras, E. C. Hatchikian, M. Frey and
J. C. Fontecilla-Camps, Nature, 1995, 373, 580–587; (b) A. Volbeda, E.
Garcin, C. Piras, A. L. de Lacy, E. C. Hatchikian, M. Frey and J. C.
Fontecilla-Camps, J. Am. Chem. Soc., 1996, 118, 12989–12996.
2
3
Y. Higuchi, T. Yagi and N. Yasuoka, Structure, 1997, 5, 1671–1680.
(a) C. Tard and C. J. Pickett, Chem. Rev., 2009, 109, 2245–2274; (b) F. A.
Armstrong, N. A. Belsey, J. A. Cracknell, G. Goldet, A. Parkin, E.
Reisner, K. A. Vincent and A. F. Wait, Chem. Soc. Rev., 2009, 38, 36–
5
6
3
4
2
1; (c) M. R. DuBois and D. L. DuBois, Chem. Soc. Rev., 2009, 38,
2–72; (d) F. Gloaguen and T. B. Rauchufuss, Chem. Soc. Rev., 2009,
8, 100–108; (e) S. Groysman and R. H. Holm, Biochemistry, 2009,
8, 2310–2320; (f) H. Ogata, W. Lubitz and Y. Higuchi, Dalton Trans.,
009, 7577–7587; (g) W. Lubitz, E. Reijerse and M. van Gastel, Chem.
Rev., 2007, 107, 4331–4365; (h) A. L. de Lacey, V. M. Fern a´ ndez, M.
Rousset and R. Cammack, Chem. Rev., 2007, 107, 4304–4330; (i) P. E. M.
Siegbahn, J. W. Tye and M. B. Hall, Chem. Rev., 2007, 107, 4414–4435;
2
Fig. 3 pH-dependent generation of H (closed circle) and HD (open
circle) in the reaction of [NiFe]H
.10 MPa) in H
2
ase (0.10 nmol) with D
2
(2.3 mL,
(
j) M. Bruschi, G. Zampella, P. Fantucci and L. de Gioia, Coord. Chem.
◦
0
2
O buffer solution (1.0 mL) at 37 C for 1 h.
Rev., 2005, 249, 1620–1640; (k) V. Artero and M. Fontecave, Coord.
Chem. Rev., 2005, 249, 1518–1535.
Given the compatibility and complementarity of these two
ase system
4 (a) S. Ogo, R. Kabe, K. Uehara, B. Kure, T. Nishimura, S. C. Menon,
R. Harada, S. Fukuzumi, Y. Higuchi, T. Ohhara, T. Tamada and R.
Kuroki, Science, 2007, 316, 585–587; (b) B. Kure, T. Matsumoto, K.
Ichikawa, S. Fukuzumi, Y. Higuchi, T. Yagi and S. Ogo, Dalton Trans.,
2008, 4747–4755; (c) T. Matsumoto, B. Kure and S. Ogo, Chem. Lett.,
2008, 37, 970–971; (d) S. Ogo, Chem. Commun., 2009, 3317–3325.
catalysts, isotope exchange experiments using a 1·H
2
became imperative. The results are depicted in Fig. 4 and it is
immediately apparent that the two catalysts system shows the
6
benefits of both catalysts combined. That is, the working pH
5
(a) T. Yagi, M. Tsuda and H. Inokuchi, J. Biochem., 1973, 73, 1069–
081; (b) D. G. Fauque, Y. M. Berlier, M. H. Czechowski, B. Dimon,
range, has now been extended to cover pHs from about 2 to 10.
In conclusion, we have shown that, combining the comple-
mentary properties of artificial and natural enzymes can make
more robust and versatile catalytic systems. We hope that future
cross-scale assemblies—concerto catalysis—will lead to the further
development of remarkable catalytic systems.
1
P. A. Lespinat and J. LeGall, J. Ind. Microbiol., 1987, 2, 15–23; (c) N. A.
Zorin, B. Dimon, J. Gagnon, J. Gaillard, P. Carrier and P. M. Vignais,
Eur. J. Biochem., 1996, 241, 675–681; (d) M. Bernhard, T. Buhrke, B.
Bleijlevens, A. L. de Lacey, V. M. Fern a´ ndez, S. P. J. Albracht and B.
Friedrich, J. Biol. Chem., 2001, 276, 15592–15597; (e) P. M. Vignais, L.
Cournac, E. C. Hatchikian, S. Elsen, L. Serebryakova, N. Zorin and B.
Dimon, Int. J. Hydrogen Energy, 2002, 27, 1441–1448; (f) P. M. Vignais,
B. Dimon, L. Cournac, N. Zorin, M. Tomiyama and A. Colbeau,
J. Bacteriol., 2000, 182, 5997–6004; (g) L. Cournac, G. Guedeney, G.
Peltier and P. M. Vignais, J. Bacteriol., 2004, 186, 1737–1746; (h) S. Vogt,
E. J. Lyon, S. Shima and R. K. Thauer, JBIC, J. Biol. Inorg. Chem., 2008,
Acknowledgements
This work was supported by grants-in-aid: 17350027, 17655027,
8033041 and 18065017 (Chemistry of Concerto Catalysis), the
Global COE Program, “Science for Future Molecular Systems”
from the Ministry of Education, Culture, Sports, Science and Tech-
nology, Japan and the Basic Research Programs CREST Type,
1
3, 97–106.
1
2
+
+
6
It was confirmed that the reduction of [MV] to [MV] was catalysed
◦
by the [NiFe]H
2
ase using H
2
in H
2
O buffer solution at pH 7 at 37
C
for 1 h whether 1 was present or not, which was monitored by UV-vis
spectroscopy (Fig. S1 in ESI†).
2
994 | Dalton Trans., 2010, 39, 2993–2994
This journal is © The Royal Society of Chemistry 2010