Biological Electron Transfer Chains: Genetics, Composition and Mode of Operation

289 Pages·1998·10.67 MB·English

by  P. L. Dutton, X. Chen, C. C. Page, S. Huang, T. Ohnishi, C. C. Moser (auth.), G. W. Canters, E. Vijgenboom (eds.)

Biological Electron Transfer Chains:
Genetics, Composition and Mode of Operation
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Series C: Mathematical and Physical Sciences - Vol. 512
Biological Electron
Transfer Chains:
Genetics, Composition
and Mode of Operation
edited by
G. W. Canters
and
E. Vjjgenboom
Leiden Institute of Chemistry,
Leiden University, Leiden, The Netherlands
Springer-Science+Business Media, B.V.
Proceedings of the NATO Advanced Research Workshop an
Biological Electron Transfer Chains: Genetics, Composition and Mode of Operation
Tamar, Portugal
May 3-7, 1997
A C.I.P. Catalogue record for this book is available from the Library of Congress.
ISBN 978-94-010-6158-2 ISBN 978-94-011-5133-7 (eBook)
DOI 10.1007/978-94-011-5133-7
Printed an acid-free paper
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© 1998 Springer Science+Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 1998
Softcover reprint of the hardcover 1s t edition 1998
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TABLE OF CONTENTS
Preface .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii
Chapter 1. Biological Electron Transfer. . . • . . . . . • . . . • • . . . • . . . . . . . . . . . . .• 1
Respiratory Electron Transfer Chains
e.e.
P.L. Dutton, X Chen, C.e. Page, S. Huang, T. Ohnishi and Moser ........ 3
Protein-Mediated Electron Transfer: Pathways, Orbital Interactions, and
Contact-Maps. Structure-Function Relations for Protein Electron Transfer
D.N Beratan and S.S. Skourtis ......................................... 9
Coupling of Electron Transfer and Protein Dynamics
A.I Kotelnikov, v.R. Vogel, A. V. Pastuchov, V.L. Voskoboinikovand
E.S. Medvedev .................................................... 29
Recent Surprises in the Study of Photoinduced Electron Transfer: Covalent
versus Non-Covalent Pathways
J.W Verhoeven, M KoebergandMR. Roest ............................ 51
Mechanisms and Control of Electron Transfer Processes in Proteins
O. Farver and 1 Pecht .............................................. 63
Chapter 2. Redox Chains: Composition and Control .......•..........•.. 75
The Paracoccus Denitrificans Electron Transport System: Aspects of
Organisation, Structures and Biogenesis
S.J. Ferguson ..................................................... 77
Genetics and Regulation of C 1 Metabolism in Methylotrophs
ME. Lidstrom, L. Chistoserdova, S. Stolyar and A.L. Springer .............. 89
Hierarchical Control of Electron-Transfer
H V. Westerhoff, P.R. Jensen, L. Egger, we. van Heeswijk,
R. van Spanning, B.N Kholodenko and J.L. Snoep ........................ 99
On the Mechanism of Nitrite Reductase: Complex between Pseudoazurin
and Nitrite Reductase from A. Cycloclastes
Michael E.P. Murphy, Stewart Turley and Elinor T. Adman ................ 115
Structural Research on the Methylamine Dehydrogenase Redox Chain of
Paracoccus Denitrificans
F.S. Matthews, Z.-W Chen, R.e.E. Durley, V.L. Davidson, L.H Jones,
ME. Graichen, J.H Hosler, A. Merli, D.E. Brodersen and G.L. Rossi ........ 129
vi
Chapter 3. Oxido-Reductases: Structure and Function ................... 147
Microbial Amine Oxidoreductases. Their Diversity, Role, Structure and Mechanism
1.A. Duine and A. Hacisalihoglu ..................................... 149
Flavocytochromes: Nature's Electrical Transformers
s.K. Chapman, G.A. ReidandA.W. Munro ............................. 165
The Chemistry of Biological Denitrification. spectroscopic Studies Provide Insights
into the Mechanism of Dissimilatory Heme cd and Copper-Containing Nitride Reductases
l
B.A. Averill, Y. Wang, 1. 0. Ka, IN Roublevskaia and 1.M Tiedje ........... 185
Cytochrome c Nitrite Reductase from Sulforospirillum Deleyianum and
Wolinella Succinogenes. Molecular and Spectroscopic Properties of the Multihaem Enzyme
0. Eins/e. W Schumacher. E.Kurun. U Nath and P.M.H. Kroneck .......................... 197
Molecular Basis for Energy Transduction: Mechanisms of Cooperativity in
Multihaem Cytochromes
R.o. Louro, T. Catarino, C.A. Salgueiro, 1. LeGall, D.L. Turner and
A. V. Xavier ...................................................... 209
The Solution Structure of Redox Proteins and Beyond
L. Bianei, I Bertini, P. Turano and C. Luchinat ......................... 225
Chapter 4. The Cytochrome c Oxidase Family ..•....................•.. 239
Exploring the Proton Channels of Cytochrome Oxidase
Robert B. Gennis ................................................. 241
Control of Electron Transfer to the Binuclear Center in Cu-Heme Oxidases
M Brunori, A. Giuffre, F Malatesta, E. D'ltri and P. Sarti ................ 251
Chimeric Quinol Oxidases Expressed in Paracoccus Denitrifieans
C. Winterstein, o.-MH Richter and B. Ludwig ......................... 259
Superfamily of Cytochrome Oxidases
Matti Saraste, Antony Warne and Ulrich Gohlke ......................... 271
The Electron Transfer Centers of Nitric Oxide Reductase: Homology with the
Heme-Copper Oxidase Family
A. Kannt, H Michel, MR. Cheesmann, A.1. Thomson, A.B. Dreusch,
H Korner and w.G. ZumJt .......................................... 279
Preface
From May 3-7,1997, the NATO Advanced Research Workshop on 'Biological Electron
Transfer Chains' was organized in Tomar, Portugal. In the application for support the
choice of the topic was justified as follows: "[Until recently efforts] have concentrated
on the study of the structure and function of individual redox enzymes and proteins.
Enough information is now available to make a start with the study of biological
electron transfer (E1) at the next higher level of organization, that of the complete ET
chain." The interest in the workshop was high: the majority of participants had
registered before the workshop was formally announced, which illustrates the popularity
of the topic within the biochemical and biophysical communities. The present volume
contains a number of reports based on the lectures presented by the key speakers during
the meeting.
The workshop dealt with the following three themes:
a) Electron transfer, which is the subject of Chapter 1. The analysis of ET at the
molecular level is still fundamental for an understanding of how ET chains operate in
vivo. After 40 years of research the contours of the subject are becoming clear now.
b) Bacterial redox chains. This is the subject of Chapter 2. Its contents show how
complicated these chains can be, often involving a number of gene clusters. Our
understanding of the regulatory aspects and control mechanisms of these chains is only
in its beginning.
c) Structure and function of redox proteins. Structural information on proteins remains
indispensable for a proper understanding of their function and of the context in which
they operate. It is not surprising, therefore, that the two final chapters of these
proceedings are devoted to this subject. Chapter 3 deals with oxido-reductases in
general, while Chapter 4 treats the cytochrome oxidase family.
It may be interesting to briefly reflect on the contents of the various contributions.
A concept that figures prominently in the contributions on ETis that of 'Pathways'. The
problem of electronic conduction in the cell has been solved in the course of evolution
by the embedding of redox centres at edge-edge distances of 5-15 A in a non
conducting protein matrix. For mobile ET carriers the ET in an encounter complex takes
place over similar distances. The question that has kept many investigators busy is
whether in the course of evolution redox proteins and enzymes have evolved such that
they offer an electron a well defined and recognizable pathway when it traverses the
protein matrix from one redox site to another.
In a semi-empirical manner Beratan and colleagues have attempted to implement the
so-called pathway concept to account for the effect of the protein structure on individual
ET rates. Their approach has enjoyed a large popularity but the shortcomings of the
model are recognised by Beratan himself in his present contribution. They derive from
the fact that the pathway model can not account for the phase that is a vital part of the
wave description of the electron: when there appears to be more than one viable
pathway ('tubes of several pathways') interference may occur, while also reflections at
'dead ends' may be difficult to account for. The way out is to treat the problem
quantum-mechanically and determine the electronic coupling between donor and
acceptor by calculating the Hamiltonian matrix for the whole protein. It is conceivable
vii
viii
that in the structure of this matrix and from the configuration of the non-zero matrix
elements a 'path' is recognizable, but the matrix structure may also have a more diffuse
character in which case a 'path' may be more difficult to trace.
In this connection it is interesting to note the study by Farver and Pecht. From the
effect of point mutations on the internal ET rate in azurin they conclude that there is a
recognizable pathway leading from the cystine disulfide at the 'south end' of the protein
to the redox active Cu centre .at the 'north end'. On the other hand, Verhoeven and
coworkers in their elegant studies of ET in a series of covalently linked D-A complexes,
find that ET through a stochastically disordered solvent can be more efficient then via
a well defined covalent through-bond path. The study of protein complexes with well
defined geometries may help us further in dissecting the role of the protein matrix on
ET rates. There are only few examples of these, besides the photosynthetic reaction
centre, but in the contributions by Adman C.S. and Mathews C.S. two promising cases
are presented. Especially the binary and ternary complexes studied by Mathews,
although their physiological relevance in part is subject to discussion (see contributions
by Duine and Ferguson), offer beautiful opportunities for further study. When electronic
interference effects become important, the electronic D-A coupling may become very
sensitive to the detailed nuclear configuration of the protein and thus to vibrational
effects. Kotelnikov and coworkers stress this point by arguing that the way ~t varies
with temperature may give a clue as to whether the adiabatic limit possibly obtains.
A useful concept to understand the organization and operation of biological redox
chains is that of 'Control'. As Dutton C.S. in their contribution argue, an uphill ET step
in a redox chain may function as a point of control of the electron flow. The
contributions of Ferguson and Lidstrom also illustrate the complicated network of
promoters, signalling cascades, redox sensors and the like that a cell uses to stay in
control of its metabolic processes under varying external conditions. The point is
emphasized by Westerhoff c.s., who show that metabolic control analysis is just
beginning to scratch the surface of the metabolic complexity of the cell.
While the chapter on biological ET focuses on the mechanism of ET, it is at the
level of the individual oxido-reductase that we can see the actual biological redox
chemistry at work. There is a bewildering diversity and individuality that confronts us
here, as is shown by Duine in his review of amine oxido-reductases, and by Ferguson
in his discussion of the respiratory pathways of the organism Paracoccus denitrificans
that has since long been considered a close relative to the primordial endosymbionth
from which our mitochondrion derives. The flavocytochromes that are studied by
Chapman and coworkers provide beautiful model systems to study the combination of
intra-protein ET and all sorts of interesting redox chemistries. Averill c.s. and Kroneck
c.s. both concentrate on recent findings with respect to structure and function of nitrite
reductases, while Bertini and Xavier and their associates show how the paramagnetism
of haem proteins can be used to one's advantage in structure/function research. An
interesting property of the cytochrome C3 studied by Xavier is that it couples electron
and proton transfer and may be considered a 'proton thruster' which is operational in
energy transduction.
The justification for the final chapter being entirely devoted to the superfamily of
the cytochrome c oxidases is firstly, that cytochrome c oxidase (COX) over the years
IX
has played a prominent role in the research on biological ET chains, and secondly that
the recently published structures of COX from two different sources have provided an
extra impulse to the research on this key enzyme. The recently acquired insights on the
proton pumping mechanism of COX are reviewed by Gennis, while Brunori c.s. discuss
the question whether the internal ET from the haem a to the dinuclear haem ~-CUB
centre is the rate limiting step in enzyme turn-over. Ludwig explores the structural and
functional relationships between the subunits of cytochrome oxidases from different
sources and the evolutionary origin they share with quinol oxidases. The evolutionary
aspects are further analysed by Saraste c.s. who argue that COX and the present-day NO
reductase share a common ancestor. The contribution by Zumft et al. focuses entirely
on the later enzyme. They argue convincingly that the catalytically active site of NO
reductase is strongly reminiscent of the active site of COX in that the CUB site is
occupied by a non-haem iron.
The workshop owed its success not only to the presentations by the key speakers,
but also to the contributions by the junior speakers and the chairmen, as well as to the
participants in the poster sessions. Finally it should be mentioned that the workshop
would have been impossible without the generous support of NATO provided through
her Special Programme on Supramolecular Chemistry. Important financial assistance was
also provided by the Metals in Biology Progamme of the European Science Foundation.
We thank both sponsors for their generous help. In addition we gratefully acknowledge
support from the Junta Nacional de Investigarrao Cientifica e Techno16gica, Portugal;
the Institute ITQB, Lisboa; Bruker, France; the Camara Municipal de Tomar, Portugal;
and the BIOMAC Graduate School, Leiden.
G.W. Canters
E. Vijgenboom
Leiden, February 1, 1998
Chapter 1
Biological Electron Transfer