2009 Annual Science Report

Montana State University Reporting  |  JUL 2008 – AUG 2009

Executive Summary

Iron-sulfur clusters are ubiquitous in biology and possess features that are reminiscent of the features of iron-sulfur minerals. The structure/reactivity relationships between iron-sulfur metalloenzymes and iron-sulfur minerals has been noted by a number of investigators and is the basis for aspects of a “Metabolism First” origin of life scenario and more specifically for the “Iron Sulfur World”. These provide a framework for the research being conducted at the Astrobiology Biogeocatalysis Research Center with a focus on revealing the connection between iron-sulfur minerals and iron-sulfur metalloenzymes. The adaptation of iron-sulfur motifs from the abiotic world to the biological world may have been an early event in the generation of the building blocks of life on Earth and possibly a common feature of life elsewhere in the universe. ABRC research is aimed at providing the structural and chemical determinants that define the catalytic properties of iron-sulfur-based minerals and biological catalysts using the examples of hydrogen activation and evolution, and nitrogen reduction as model reactions. An overarching goal of the ABRC is to provide new insights into processes by which iron-sulfur motifs may have transitioned 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 has the potential to contribute significantly in the development of mineral signatures for terrestrial and extraterrestrial life.

The ABRC is a unique and important component of the NASA Astrobiology Institute. The ABRC focuses on the abiotic chemical interconversions that result in the formation of the raw materials or reactants necessary for various condensation reactions that can result in the formation of the basic building blocks of life. The ABRC’s efforts are focused mainly on laying the fundamental groundwork for Goal 3 of the NASA Astrobiology Roadmap (Understand how life emerges from cosmic and planetary precursors) of the NASA Astrobiology Roadmap. Furthermore, ABRC research directly impacts the objectives of Goals 2 (Determine any past or present habitable environments, prebiotic chemistry and signs of life elsewhere in our Solar System), and 4 (Understand how life on Earth and its planetary environment have co-evolved through geological time). The outcomes of the research will also provide the basis for aspects of Goal 7 (Determine how to recognize signatures of life on other worlds and on early Earth). Our recently developed experimental thrust in developing new approaches for examining iron-sulfur enzyme evolution will contribute significantly to Goal 5 (Understand the evolutionary mechanisms and environmental limits of life) as well. The ABRC's research focus provides a logical and synergistic complement to research efforts of other Astrobiology Research Centers.

Specifically, ABRC research is focused on investigating (bio)synthesis, structure, and reactivity at iron-sulfur motifs and is divided into three major thrust areas including 1) iron-sulfur mineral catalysis, 2) iron-sulfur enzyme catalysis, and a 3) 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. During the current year of support we have developed a complementary project examining iron-sulfur enzyme evolution by examining the evolutionary trajectory of genes involved in iron-sulfur cluster biosynthesis. Coupling the examination of the evolutionary trajectory of multiple gene loci in the context of gene duplication and fusion events provides a robust means to assign evolutionary paths and evolutionary origins of processes catalyzed by iron-sulfur enzymes. In some cases, there are clear prospects for tying these evolutionary relationships to the geologic record with a promise for gaining significant insights into the nature of life on early Earth. In sum, these activities are aimed at examining the potential role of iron-sulfur motifs at the transition between the non-living and the living Earth. Moreover, we complement our scientific investigations with activities that evaluate both metaphysical and philosophical implications of the origin of life. In addition, a strong education and public outreach component with activities associated with nearby Yellowstone National Park with its numerous thermal features having characteristics often associated with 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 illustrate important fundamental principles of chemistry and biology.

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

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

2. Catalysis at iron-sulfur 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 iron-sulfur 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 iron-sulfur clusters, particles and minerals, and materials studied by beam/surface collision experiments, advanced spectroscopic techniques, and structural modeling of mineral surface defects by integrated quantum chemical methods.

3. Synthetic approaches are being utilized to bridge the gap between iron-sulfur minerals and highly evolved biological iron-sulfur 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 iron-sulfur clusters, and computational modeling of the structure and catalytic properties of synthetic iron-sulfur nanoparticles in the 5-50 nm range.

ABRC Research Highlights

In this second year of support we have made significant progress and made great strides in terms of integrating the various efforts of ABRC team members. The ABRC has a well-defined focus and within the three thrust areas described above, natural synergies have evolved to an even greater and more productive extent than we had envisioned in our original proposal. In addition, we have developed a strong theoretical component lead by Robert Szilagyi, which effectively bridges the thrust areas and provides the basis to think about the transition of iron-sulfur motifs between the abitoic and biotic systems as occurring along some sort of continuum (Figure 1).

During the second year of support we have made significant progress in the iron-sulfur enzyme thrust in understanding the stepwise biosynthesis of the [FeFe]-hydrogenase H cluster. We have determined that H cluster biosynthesis that the different subclusters of the H cluster are synthesized by different biosynthetic machinery on protein scaffolds and then inserted separately in a sequential manner. The results are highly significant and have interesting common features with known aspects of the complex iron-sulfur enzyme nitrogenase providing the basis to establish a common paradigm for cluster synthesis in these evolutionarily unrelated enzymes. We have harnessed our extensive knowledge of complex iron-sulfur biosynthesis to establish a complementary line of ABRC research probing evolutionary relationships and evolutionary origins of complex iron-sulfur enzymes. Since multiple gene products are required for synthesis of cofactors such as the hydrogenase H cluster and the nitrogenase FeMo-cofactor we can analyze phylogenic relationships by the analysis of suites of genes instead of single loci. Using this approach we have established that Mo-nitrogenase emerged in methanogenic archaea and have provided insight into the emergence of Mo-dependent nitrogenase relative to anoxygenic and oxygenic photosynthesis.

Synthetic, spectroscopic, and computational approaches are being utilized to uncover the link between Fe-S minerals, particles, and molecular clusters of metalloenzymes. During the second year of funding the mineral, biomineral, and computational thrust areas began to converge on important structure/function features of Fe-S motifs that may have lead to the adaptation of Fe-S motifs from the abiotic world to the biological world. A key progress toward this end is the initial mapping of an enormous parameter space with respect of chemical composition, preparation protocol, short and long range orders of atoms, presence of surface defect sites, etc. The importance of surface modifications is being investigated using molecular beam-surface scattering using hydrogen atom plasma bombardment of pyrite surfaces. Combined surface characterization techniques, mass spectrometric, and X-ray absorption spectroscopic data suggest the formation of a reduced Fe-S phase, which is poised for breaking the first N-N bond or activating hydrogen gas toward forming electrons and proton gradients. Results from protein-mediated particle assembly revealed that synthetic Fe-S nanoparticles in the 5-50 nm range form a distorted mackinawite structure, with a sub-nanometer size crystalline domain. These experimental results are now being tied together with computational chemical simulations employing coordination chemistry-based surface/interface models that provide a cohesive molecular link through bridging the enzymatic/mineral catalysis and molecular structure/chemical reactivity via fundamental physico-chemical properties.

Origin of Life Philosophy Discussion Group

The ABRC philosophy group holds a strong interest in astrobiology as an emerging science and is well poised to undertake critical analyses of the problems and controversy encountered by scientists in this rapidly advancing field. The expertise of group members have lead to the development of two major lines of inquiry including i) quantum measuring/decoherence effects at metal based catalytic sites and ii) analyses of theories of life in an effort to compare and contrast groups of scientific thought from epistemological grounds. The group consists of core members that meet weekly for discussion of topics and group progress and has two new additions from the Philosophy Department (Sara Waller and Kristin Intemann) as well as an additional graduate student (Trevor Beard) from the Department of Chemistry. In addition to holding weekly meetings and having submitted a hypothesis for publication, the group has also hosted Carol Cleland, a philosopher from U.C. Boulder who delivered an ABRC seminar to standing room only attendance.

Education and Public Outreach

ABRC E/PO provided a very rich program, targeting all audience levels including; the general public, teachers, K-12 students, and undergraduate students as well as international audiences. A major portion of the effort includes conducting monthly academies for teachers in two school districts in Montana for the academic year 2009-2010. These face-to-face and online modules are content rich in Astrobiology-related topics and are followed with classroom observations of science lessons for the 55 participating teachers. Participating teachers are earning 12 graduate credits for the full year program. ABRC together with the MSU NASA supported Thermal Biology Institute (TBI) hosted two graduate level summer 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 spring and summer programs conducted in 2009, totaling 16 days of programming in schools and field trips to Yellowstone National Park. ABRC and TBI provided two community lectures at the Emerson Cultural Center, in downtown Bozeman attracting 500 people.

We have worked to establish a formal curriculum at the undergraduate and graduate level at Montana State University. We offered a graduate course in Astrobiology and prebiotic chemistry through the Department of Chemistry and Biochemistry at MSU. This course involved all the coPIs of the ABRC team and was conducted by videoconference in order to allow team members (students and PIs) at Stony Brook University and Temple to participate. The course was very successful and resulted in enhanced coordination and cross-fertilization of research activities between coPIs laboratories. We have also made plans to formalize this course and it will be offered as a limited enrollment undergraduate/graduate seminar course in Origin of Life Philosophy. We have submitted a proposal to the MSU administration to establish a minor in Astrobiology consisting of coursework in Chemistry, Earth Science, Microbiology, Philosophy, and Physics and will establish two new courses, a gateway course offered by the History and Philosophy and a cross-listed capstone course in Astrobiology. We are working with MSU Extended University to adapt the latter courses to a distance-learning format to allow other academic institutions to offer Astrobiology Minors without having to develop additional coursework.