Imidazole catalyzed silica synthesis: Progress toward
understanding the role of histidine in (bio)silicification
Mei-Keat Liang and Siddharth V. Patwardhan
Biomolecular and Materials Interface Research Group, School of Science and Technology,
Nottingham Trent University, Nottingham NG11 8NS, United Kingdom
Elena N. Danilovtseva and Vadim V. Annenkov
Limnological Institute of Siberian Branch of Russian Academy of Sciences, Irkutsk 664033, Russia
Carole C. Perry
a)
Biomolecular and Materials Interface Research Group, School of Science and Technology,
Nottingham Trent University, Nottingham NG11 8NS, United Kingdom
(Received 26 September 2008; accepted 25 November 2008)
Histidine is an amino acid present in proteins involved in biosilica formation and often
found in peptides identified during phage display studies but its role(s) and the extent of
its involvement in the silica precipitation process is not fully understood. In this
contribution we describe results from an in vitro silicification study conducted using
poly-histidine (P-His) and a series of different molecular weight synthetic polymers
containing the imidazole functionality (polyvinylimidazole, PVI) for comparison. We
show that the presence of imidazole from PVI or P-His is able to catalyze silicic acid
condensation; the effect being greater for P-His. The catalytic mechanism is proposed to
involve the dual features of the imidazole group—its ability to form hydrogen bonds with
silicic acid and electrostatic attraction toward oligomeric silicic acid species.
I. INTRODUCTION
The intricate and highly repeatable biosilica structures
exhibited by marine organisms demonstrate the magnif-
icence of construction control exerted by life. Studies of
these organisms have revealed that organic biomole-
cules including proteins are associated with the growth
of biosilica structures; however the role(s) of these bio-
molecules at the molecular level are not yet fully under-
stood. Silicatein proteins extracted from sponges such
as T. aurantia and S. domuncula have high sequence
homology with cathepsin-L that has a hydrolytic func-
tion in the lysosome.
1,2
A site-directed mutagenesis
study of silicatein has shown that Ser-26 and His-165
residues present at the active site of silicatein are neces-
sary to catalyze the hydrolysis of tetraethylorthosilicate
(TEOS), a silica precursor used in vitro.
3
The necessity
for two functional groups in close proximity (app-
roximately 6.8 A
˚
)
1,4
to each other for the catalyzed
hydrolysis of TEOS has support from an in vitro study
using bifunctional small molecules.
5
As a consequence
of these studies, the hypothesis that hydrogen bond for-
mation between the hydroxyl group of Ser-26 and the
imidazole of His-165 is important in silicification was
proposed and has support from an ab initio density-
functional theory study using a gas-phase model.
6
This
latter study has shown that the imidazole group of
His-165 is free to rotate and hence able to form a hydro-
gen bond with the –OH of Ser-26. When a similar simu-
lation was performed in the presence of monosilicic
acid, the binding energy (BE) and formation energy
(FE) values obtained showed that polycondensation
between orthosilicic acid molecules was energetically
favorable in the presence of silicatein,
6
thus further sup-
porting the importance of the hydrogen-bonding abil-
ity of histidine in silica formation. In other studies of
silica formation, combinatorial phage display methods
have been used to identify silica-binding peptides.
7
Many silica-binding peptides that were also capable
of facilitating silica formation contain high numbers of
histidine residues.
7,8
From the studies reviewed above, it is highly likely
that the presence of histidine-containing biomolecules in
reaction environments where silica is formed is simply
not fortuitous. However, no direct evidence has been
presented that shows that histidine catalyzes the conden-
sation of silicic acid molecules.
3
Model studies of silica
formation in the presence of poly-histidine have gener-
ated conflicting results with one in vitro study on silica
formation from tetramethoxysilane (TMOS)
9
at neutral
pH precipitating silica in the presence of poly-histidine
whereas in another study using TEOS as the silica pre-
cursor, poly-histidine alone was not active.
10
a)
Address all correspondence to this author.
e-mail: Carole.Perry@ntu.ac.uk
DOI: 10.1557/JMR.2009.0223
J. Mater. Res., Vol. 24, No. 5, May 2009 © 2009 Materials Research Society 1700