Special Issue Preface pubs.acs.org/JPCB
Tribute to Wolfgang Lubitz separation in bacterial and plant photosynthesis, the most important electron-transfer process on Earth. This success was achieved by studying the cofactor radicals and transition-metal complexes, radical pairs, and triplet states embedded in their protein matrix. In recent years, his research focus has shifted to hydrogenases, enzymes that play a central role in hydrogen metabolism, and to the manganese cluster in the water-splitting complex of plant photosynthesis (see Cover picture). Wolfgang Lubitz is member of a dozen scientific organizations, for example, the Gesellschaft Deutscher Chemiker, the Deutsche Gesellschaft für Biophysik, the Biophysical Society (USA), the International Society for Bioinorganic Chemistry, the International Society of Photosynthesis Research, and the International Society of Magnetic Resonance. Wolfgang was the President of the International EPR/ESR Society in 2005−2008. In addition to many other awards and fellowships, Wolfgang Lubitz received the Zavoisky Award (Russia, 2002) and the Bruker Lecturer Prize (UK, 2003). He became Fellow of the Royal Society of Chemistry (UK, 2004) and received the Gold Medal of the International EPR/ESR Society (2005). He received an Honorary Doctorate from the University of Uppsala (Sweden, 2008) as well as an Honorary Doctorate from the University d’Aix-Marseille (France, 2014). He was honored to present the Malcolm Dole Distinguished Summer Lectures in Physical Chemistry at Northwestern University (Evanston, USA) in 2009. In this year, he also became a Fellow of the International Society of Magnetic Resonance. In 2012, he was elected Foreign Member of the Tatarstan Academy of Sciences. Since 2015, Wolfgang Lubitz has been Vice-President of the Council of the Lindau Nobel Laureate Meetings. In the early 1970s, Wolfgang Lubitz started his academic research career at the Free University Berlin by applying the then rather new liquid-state electron−nuclear double resonance technique (ENDOR-in-solution) to obtain spin density maps of paramagnetic organic species by measuring nuclear hyperfine couplings. He expanded the method to a series of magnetic nonproton nuclei.13 [The reference numbers correspond to those of Wolfgang Lubitz’s List of Publications also published in this issue (DOI: 10.1021/acs.jpcb.5b08586)]. His systematic work paved the way for many applications to interesting radicals in chemical and biological systems, as summarized in a monograph.44 A prominent biological example is the first ENDOR study of a membrane protein under physiological conditions in solutionthe bacterial reaction center (RC).15 His work was expanded later to the investigation of RC single crystals.72 This and related work on genetically modified RCs confirmed the previously proposed chlorophyll dimer model for the primary donor and explained its function in photosynthetic electron transfer.182 He also applied time-resolved transient, pulsed, and high field EPR techniques to all the electron acceptors, and to triplet states and radical pairs created in the RC by pulsed laser excitation.182 This led to a profound understanding of the
Photo by Thomas Hobirk
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t is a distinct honor and great pleasure to dedicate this special issue of The Journal of Physical Chemistry B to Professor Wolfgang Lubitz on the occasion of his 65th birthday (July 23, 2014). This Festschrif t continues the longstanding academic tradition of honoring scientists who have had a major impact on an important field. Of the 100 of Wolfgang’s colleagues from around the world that were invited to participate in this Festschrif t, most have contributed to the more than 50 papers it contains. Their work in areas of his interest in physical chemistry, biochemistry, and biophysics thereby honors Wolfgang’s scientific achievements in applying advanced analytical methods including multifrequency EPR spectroscopy, X-ray crystallography, and molecular engineeringto a broad range of subjects. The original papers of this Festschrif t from well-known research groups provide typical examples of applications and methodological developments in a field where Wolfgang has left so many distinctive footprints. Such a collection of papers will not only be appreciated by Wolfgang Lubitz, his co-workers, and colleagues, but it also will be of great interest to a wide audience of junior and senior scientists from physical chemistry and structural biology. From 1975 until mid 2015, Wolfgang Lubitz (co)authored about 420 publications in premier scientific journals and books. His numerous review articles are a delight to read both for experts and newcomers. He and his co-workers have significantly contributed to the understanding of light-induced charge © 2015 American Chemical Society
Special Issue: Wolfgang Lubitz Festschrift Published: October 29, 2015 13475
DOI: 10.1021/acs.jpcb.5b08583 J. Phys. Chem. B 2015, 119, 13475−13477
The Journal of Physical Chemistry B
Special Issue Preface
spectroscopy and by X-ray crystallography. This development led to structural data of exceptionally high quality. In the recent work on a reduced standard [NiFe] hydrogenase, a resolution of 0.89 Å was obtained, in which the hydrogens could be assigned also near the metal centers, e.g., the hydride bridging Ni and Fe.399 Wolfgang Lubitz and co-workers also studied the oxygen tolerance observed in specific [NiFe] hydrogenases. They found that this is not related to a change of the catalytically active site but to a specific proximal iron sulfur cluster, which is involved in electron transfer. EPR-monitored redox titrations showed that this special [4Fe] cluster is surprisingly able to perform two single electron transitions in a narrow potential range.323 This protects the active site against oxygen attack, probably by reducing O2 to water. Thus, these hydrogenases seem to also act as oxidases when exposed to oxygen. Recent electrochemical experiments performed together with Wolfgang Schuhmann (Bochum) showed that a shield against oxygen can also be achieved by embedding the hydrogenase in a protective matrix (redox polymer), which also has other advantages, e.g., avoiding high potential deactivation.391 This approach therefore eliminates the two major problems that have so far prevented the use of hydrogenases in biotechnology, e.g., (bio)fuel cells. In parallel to its experimental work, the Lubitz group has used quantum chemical approaches to calculate spectroscopic parameters based on energy minimized structures of the intermediates in the reaction cycle and the activation/deactivation cycles of [NiFe] hydrogenases.211 This has now led to a deep understanding of hydrogenase function and inhibition. Similar experimental and theoretical work has also been carried out by Lubitz and co-workers for [FeFe] hydrogenases. By pulsed EPR, a nitrogen was detected in the dithiolate bridge in the active site of this enzyme that acts as a base in H2 splitting/formation.289 This finding has been very important for understanding the catalytic mechanism and for the chemical synthesis of functional hydrogenase models. The presence of nitrogen in the bridge has been confirmed in 2013 by work performed in collaboration with Marc Fontecave and Vincent Artero (Paris/Grenoble) and Thomas Happe (Bochum). In these experiments, completely synthetic biomimetic [2Fe] complexes were inserted into the apoprotein of bacterial and algal hydrogenases.367,375 Over the years, Wolfgang Lubitz has mentored 49 Ph.D. students and postdocs, many of whom are now actively working as professional scientists, be it at universities, research laboratories, industry, or research institutions. Speaking on behalf of all of his former mentees, they sincerely thank Wolfgang for his scientific and personal guidance through the years: his influence on their lives has been towering. Wolfgang Lubitz’s research accomplishments, past, present, and future, will continue to have a profound impact on generations of young and senior scientists working in biochemistry and structural biology. Collaborating and interacting with him has been a privilege, allowing for enjoyable discussions on issues of science and the humanities. It has also been a privilege to share his standards of scientific rigor and visions in chemistry and molecular biology, his passion for sustainable solar energy conversion, and his attention to the details when it comes to lecturing and publication. We want to thank all the authors of this special issue, who have reacted so positively, some even enthusiastically, to our invitation. This series of excellent contributed articles reflects the diverse areas of research that have been influenced and stimulated by Wolfgang Lubitz.
relationship between the electronic structure of the cofactors, their interaction with the protein environment, and their biological function in the primary electron transfer process. Subsequently, similar work focused on the two photosystems of oxygenic photosynthesis in liquid and frozen solutions as well as to the first available single crystals of the photosystems PS I and PS II of oxygenic photosynthesis.162,166,199 A detailed understanding of these photosystems is of major importance for mankind, in the quest to convert and store the sun’s energy in chemical compounds. At the Technical University Berlin and, later, at the Max Planck Institute for Bioinorganic Chemistry in Mülheim (in 2012, renamed Max Planck Institute for Chemical Energy Conversion), Wolfgang Lubitz started to work on light-induced water oxidation and oxygen release in oxygenic photosynthesis in PS II. With the advent of an atomic level X-ray structure of PS II from Japan in 2011 and with the development of high-resolution/ high-sensitivity magnetic resonance techniques and novel quantum chemical approaches in Mülheim, the field has witnessed an explosion of research activity. In several key papers,223,251 the Lubitz group successfully advanced earlier work, with multifrequency pulsed EPR and 55Mn ENDOR on the active center of the water-splitting complex (a Mn4O5Ca cluster) in various states of the catalytic cycle. In this way, the site oxidation and spin states of the individual Mn ions and their interactions with each other could be determined for all intermediate states of the complex.403 The function of the Ca could be elucidated by replacement with Sr and Ca removal.322,345 Furthermore, the binding of the first substrate water molecule and its incorporation into the Mn cluster could be assessed by using isotopically labeled water (H217O) in measurements via the novel double resonance technique W-band high magnetic field ELDOR-detected NMR.346 Very recently, the Lubitz group was able to spectroscopically characterize the last metastable state of the water-splitting cycle prior to O−O bond formation.394 The joint spectroscopic and theoretical results gave information on the binding mode and location of the second substrate water molecule and thus allowed conclusions to be made on the mechanism of dioxygen formation. These results constitute a major breakthrough in this important research field and allow the development of a highly probable mechanism for the complete water oxidation cycle. After more than a decade of focused work on hydrogenases and (bio)hydrogen, the Mülheim laboratory has become a major player in this field worldwide. In 2007, Wolfgang Lubitz edited the 100th anniversary issue of Chemical Reviews on “Hydrogen” together with William Tumas (Los Alamos) and contributed an overview article about his work.253 In 2014, a comprehensive review on hydrogenases appeared in Chemical Reviews in an issue dedicated to “Bioinorganic Enzymology”.385 The highlights of his work in this field encompass the full characterization of the geometric and electronic structure of the [NiFe] and [FeFe] hydrogenases using magnetic resonance in combination with isotope labeling (H/D, 13C, 17O, 61Ni, and 57Fe) and many other methods, in particular FTIR, spectro-electrochemistry, Mössbauer, and synchrotron-based techniques (XES/XAS, NRVS). The application of advanced EPR techniques has, for example, enabled the characterization of a bound hydride in the reduced state of [NiFe] hydrogenase.204 This advance on earlier work was of key importance for understanding the hydrogen conversion mechanism in this class of enzymes. The Lubitz group has further designed purification and crystallization techniques to study well-defined states of the catalytic cycle of hydrogenases in single crystals both by EPR 13476
DOI: 10.1021/acs.jpcb.5b08583 J. Phys. Chem. B 2015, 119, 13475−13477
The Journal of Physical Chemistry B
Special Issue Preface
We wish Wolfgang Lubitz and his family the very best and look forward to his continued contributions to scienceand more.
Brian M. Hoffman Northwestern University
Klaus Möbius
Free University Berlin and Max Planck Institute for Chemical Energy Conversion
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DOI: 10.1021/acs.jpcb.5b08583 J. Phys. Chem. B 2015, 119, 13475−13477
