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2008 Annual Science Report

Montana State University Reporting  |  JUL 2007 – JUN 2008

Executive Summary

The Astrobiology Biogeocatalysis Research Center at Montana State University

Fe-S compounds are common in both biological and geological systems. The adaptation of Fe-S clusters from the abiotic world to the biological world may have been an early event in the development of life on Earth and possibly a common feature of life elsewhere in the universe. We propose to establish a research and education effort that will investigate and compare the physical and catalytic properties of naturally occurring Fe-S minerals and complex Fe-S enzymes. The studies will be aimed at providing the structural and chemical determinants that define the catalytic properties of Fe-S based mineral and biological catalysis using hydrogen and nitrogen activation as model reactions. One goal of the Center will be to provide new insights into the process by which Fe-S chemistry was adapted from the abiotic to biotic world. The results of the center’s efforts will support the mission of NASA in the area of prebiotic chemistry and the development of signatures for terrestrial and extraterrestrial life.

The Astrobiology Biogeocatalysis Research Center at Montana State University fills a unique niche in the NASA Astrobiology Institute. The ABRC will focus on the abiotic chemical interconversions that result in the formation of the raw materials or reactants necessary for condensation reactions form of the basic building blocks for life. The ABRC’s efforts are focused mainly on laying the fundamental groundwork for Goal 3 of the NASA Astrobiology Roadmap (Understaind how life emerges from cosmic and planetary precursors) of the NASA Astrobiology Roadmap, however, ABRC research will directly impact the objectives of Goals 2 (Determine any past or present habitable environments, prebiotic chemistry and signs of life elsewhere in our Solar System), 4 (Understand how life on Earth and its planetary environment have co-evolved through geological time), & 5 (Understand the evolutionary mechanisms and environmental limits of life) as well . The ABRC’s research focus provides a logical and ideal complement to research efforts of the existing Astrobiology Research Centers.

ABRC research is focused on investigating (bio)synthesis, structure, and reactivity of Fe-S motifs and is divided into three major thrusts areas including 1) Fe-S mineral catalysis, 2) Fe-S enzyme catalysis, and 3) a synthetic or mimetic thrust that is aimed at bridging our understanding of the relationships between structure and reactivity at the active sites of Fe-S enzymes and the structure and reactivity of Fe-S minerals. The ultimate goal of these activities is to examine the potential role of Fe-S motifs at the transition between the non-living and the living Earth and we are complementing our scientific investigations with activities that evaluate both metaphysical and philosophical implications of the origin of life. In addition, we have developed strong education and public outreach components taking full advantage of nearby Yellowstone National Park with its numerous thermal features, often considered as analogs of early Earth, as a means to engage public audience of all ages. These activities are aimed at educating public audiences on the mission of NASA Astrobiology and illustrating important fundamental principles of chemistry and biology.

Specific research activities in the three research areas are described below:

1. Detailed studies on Fe-S enzymes are being conducted in order to evaluate the connection among Fe-S-based catalysis in minerals, clusters, and biocatalysts. The emphasis of this work has been the biological mechanisms for Fe-S cluster synthesis and the role in radical chemistry in this process together with the characterization of the structural, physical and catalytic properties of complex Fe-S-containing hydrogenases and nitrogenases

2. Catalysis at Fe-S mineral surfaces is being investigated in aqueous and gas phase systems as models of prebiotic chemical transformations. The emphasis of this thrust is to probe the properties of synthetic mineralized surfaces, the impact of surface defects and modifications on the physical and catalytic properties of an Fe-S mineral surface, the effect of energy (photo, redox, thermal, mechanical), pH, concentration, partial pressure of gases, surface area, and length scale on the structural, physical, and catalytic properties of Fe-S clusters, particles and minerals, and materials studied by beam/surface collision experiments, and the spectroscopic analyses and structural modeling of mineral surface defects by integrated computational density functional theory/molecular orbital/molecular mechanical.

3. Synthetic approaches are being utilized to bridge the gap between Fe-S minerals and highly evolved biological Fe-S metalloenzymes. These studies are focusing on organic template (protein) mediated cluster assembly (biomineralization), probing properties of synthetic clusters, both as homogeneous and heterogeneous catalysts, investigating the impact of size scale on the properties of synthetic Fe-S clusters, and computational modeling of the structure and catalytic properties of synthetic Fe-S nanoparticles in the 5-50 nm range.

ABRC Research

In the Fe-S enzyme research thrust key insights have been obtained on 1) the [FeFe]-hydrogenase H cluster structure 2) the mechanism of H cluster biosynthesis and 3) the structure of a central component of dark chlorophyll biosynthesis that serves as a key evolutionary link between photosynthesis and nitrogen fixation. A unique feature of the [FeFe]-hydrogenase H cluster is a non protein dithiolate ligand that bridges the two Fe atoms and is essential to the structural integrity of the cluster and without question impacts the electronic structure and influences catalysis. Combining experimental structure determination using X-ray diffraction methods with computational chemistry in collaborative work of the Peters and Szilagyi research groups we have presented results suggesting that the composition of the ligand is dithiomethylether (right). This result challenged the previous suggestion that the central group of the ligand is an amine and that this amine group is directly involved in catalysis as a proton donor/acceptor group. Our results indicate that the participation of an amine group in this ligand as a donor/acceptor group is very unlikely. The results provide the basis to revisit mechanistic schemes for reversible hydrogen oxidation at the H cluster and also to consider oxygen containing metabolites as precursors for the ligand for its biosynthesis.

Collaborative work of the Broderick and Peters research groups has focused on H cluster biosynthesis and the functions of the H cluster maturation enzymes. In work recently published in FEBS Letters, we report that the accessory protein HydF functions as a scaffold in H cluster biosynthesis. This is the first function ascribed to an accessory enzyme in H cluster biosynthesis and the result provides the basis to systematically investigate the function of the remaining accessory proteins and to screen metabolic precursors of the unique nonprotein ligands. In other work in collaboration with the research group of Lance Seefeldt at Utah State University we have determined the three-dimensional structure of BchL, a component of protochlorophyllide reductase involved in bacteriochlorophyll biosynthesis. We have shown in this work that BchL is structurally very similar to the nitrogenase Fe proteins but have been able to identify structural differences that likely discriminate their respective functional roles.

Research within the Fe-S mineral thrust has focused on how metal sulfides may have promoted dinitrogen reduction, a process in biology that is catalyzed by the complex FeS enzyme nitrogenase. An interdisciplinary ABRC team is addressing this question using an array of complementary techniques to gain molecular-level insight into the key elementary steps in this reaction, the role of mineral defects in the reaction, as well as rate data based on batch experiments. In this first year suitable model systems have been defined, methods refined, and a first set of experimental observations collected.

The reduction of dinitrogen to ammonia driven by the conversion of pyrrhotite to pyrite (FeS + H2S → FeS2 + 2H+ + 2e-) has been the subject of several earlier studies, however, the yield was low and the mechanism remains unknown. Using a vibrational spectroscopic technique (Attenuated Total Reflection Fourier Transform Infra-Red), ABRC researchers have been able to study this system for the first time in situ. Experiments conducted at 120°C show the formation of a nitrogen-containing species (above). More experiments are underway to resolve the nature of this species, which is most likely bound to the mineral surface.

It is generally accepted that surface-mediated reactions occur on defect sites. The role of defects in the formation of ammonia is evaluated using molecular beam-surface scattering experiments in which a deuterium atom plasma source was used to hydrogenate a pyrite surface with D atoms. The hydrogenated surface was subsequently bombarded with a molecular beam of energetic N2 molecules. Thus far, no ammonia (ND3) product has been unambiguously detected when a N2 beam with 30 kcal/mol of translational energy was directed at the D-bombarded pyrite surface. However, many experimental parameters need to be adjusted before conclusions can be drawn about the reactivity of incident N2 molecules with a hydrogenated and defected pyrite surface.

While earlier hydrothermal experiments have shown that the presence of FeS promotes the reduction of dinitrogen to ammonia, it remains unclear how important this process would have been in the Hadean compared to other abiotic, mineral-mediated reactions. The corollary question is why biology recruited the Fe-S system. To provide a basis for comparison hydrothermal batch experiments were conducted to gain insight into the rate of nitrogen reduction in the presence of iron-bearing minerals, alloys, and metals. These phases are relevant in meteorites as well as komatiites. The experiments are conducted under similar conditions as the work by Schoonen and Xu. Several hydrothermal experiments with Cr metal, NiCrFe and Ni-doped chromite have been completed and all show reactivity toward N2.

The biomimetic/synthetic thrust of the project focuses on exploring the influence of the hard (inorganic) -soft (organic) interface on reactivity of mineral based catalysis. We have demonstrated a direct templating interaction between a virus capsid and an inorganic minerals — both oxide and sulfide that are important in the origin of life context. Proteins that form cage-like quaternary structures such as ferritins and viruses, define constrained reaction environments where mineral deposition can be directed, through hard-soft interactions, and sequestered for the exterior environment. We have directed the synthesis of protein cage encapsulated metal sulfides either through a direct synthetic method or via the transformation of a preformed metal oxide material. Furthermore, iron, titanium, cobalt, molybdenum, and lanthanide oxides have also been synthesized within the confines of these protein cage architectures. The iron and molybdenum oxides can be readily transformed into corresponding sulfide minerals through a corrosion/reprecipitation process that is confined to the interior of the cage and does not involve the bulk medium. The exposure of a 500 atom Fe2O3 nanocluster to H2S over a range of temperatures, as monitored by UV/Vis spectroscopy is shown (right). In particular, the protein encapsulated MoSx nano-materials show catalytic activity for H+ reduction to form H2, the activity of the FexSy are being investigated.

Origin of Life Philosophy Focus Group

We have organized a focus group to examine the philosophical implications of our research in the context of the evolution of catalysis and the origin of life. The group consists of Prasanta Bandyopadhyay, Gordon Brittan, Regents Professor of Philosophy at MSU, Eric Schneider, author of the Into the Cool (with Dorion Sagan), and several ABRC students. Among other interests the group is examining the idea that the emergence of specific and efficient catalysts was precipitated in part via the action of quantum decoherence, and that this quantum sensing phenomenon makes more rational the emergence of the chemistry of life in an appropriate time frame following planetary formation. This idea is compatible with and adds to current metabolism-first models and yields insight as to the operation of extant biological systems and the physical behavior that underlies them.

Education and Public Outreach

ABRC E/PO efforts included conducting a workshop for teachers as part of annual school district training, for organized groups of teachers within rural communities across Montana, Great Falls and Billings (July 2008). ABRC co-sponsored the Montana Education Association Annual Statewide Conference with the Montana Science Teachers Association in October 2007 and gave seven oral presentations on Astrobiology-related science and conducted an all-day field trip to Yellowstone National Park for 40 Montana Teachers. The ABRC together with the MSU NASA-supported Thermal Biology Institute hosted two graduate level courses for practicing teachers through the Master’s in Science of Science Education program at MSU. ABRC was involved directly in a wide variety of summer programs conducted in 2007-2008, totaling 33 days of programming, including three summer camps for middle school kids in collaboration with the Montana Outdoor Science School.