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Eric Boyd
Montana State University

Research Activities

The emergence of metalloenzymes capable of activating substrates such as CO, N2, and H2, were significant advancements in biochemical reactivity and in the evolution of complex life. Examples of such enzymes include [FeFe]- and [NiFe]-hydrogenase that function in H2 metabolism and Mo-, V-, and Fe-nitrogenases that function in N2 reduction. Many of these metalloenzymes have closely related paralogs that catalyze distinctly different chemistries, an example being nitrogenase and its closely related paralog protochlorophyllide reductase that functions in the biosynthesis of bacteriochlorophyll (photosynthesis). While the amino acid composition of these closely related paralogs are often similar, their biochemical reactivity and substrate specificity are often quite different. This phenomenon is a direct consequence of the composition and molecular structure of the active site metallocluster, which requires a number of accessory proteins to synthesize. By specifically focusing on the origin and subsequent evolution of these metallocluster biosynthesis proteins in relation to paralogous proteins that have left clear evidence in the geological record (photosynthesis and the rise of O2), we have been able to obtain significant insight into the origin and evolution of these functional processes, and to place these events in evolutionary time. In parallel to our evolutionary studies, we are examining the distribution and diversity of genes that encode for these proteins in environments with physical and chemical properties that are thought to be analogous to early Earth. Such environments include the geothermal springs in Yellowstone National Park, Wyoming and various saline environments in Utah and Northern Mexico. Using a number of computational approaches, we have been able to deduce the primary environmental parameters that constrain the distribution of these functional processes and which underpin their diversity. Such information is central to constraining the parameter space of environment types that are likely to have facilitated the emergence of these metal-based biocatalysts.

Selected Publications

Meuser, J.E., E.S Boyd, G. Ananyev, D. Karns, N.U.M. Murthy, R. Radakovits, , M.L. Ghirardi, J.W. Peters, and M.C. Posewitz. 2011. Evolutionary significance of an algal gene encoding an [FeFe]-hydrogenase with F-domain homology and hydrogenase activity in Chlorella variabilis NC64A. In press.

Hamilton, T.L., R.K. Lange, E.S. Boyd* and J.W. Peters. 2011. Biological nitrogen fixation in acidic high temperature geothermal springs in Yellowstone National Park, Wyoming. Environ. Microbiol. doi: 10.1111/j.1462-2920.2011.02475.x.

Hamilton, T.L., E.S. Boyd, and J.W. Peters. 2011. Environmental constraints underpin the distribution
and phylogenetic diversity of nifH in the Yellowstone geothermal complex. Microbiol. Ecol. doi: 10.1007/s00248-011-9824-9.

Boyd, E.S., A.D. Anbar, S.R. Miller, T.L. Hamilton, M. Lavin, and J.W. Peters. 2011. A late methanogen origin for the molybdenum-dependent nitrogenase. Geobiology. 9(3):221-232.

Shepard, E.M., E.S. Boyd, J.B. Broderick, and J.W. Peters. 2011. Biosynthesis of complex iron-sulfur enzymes. Curr Opin Chem Biol. 15(2):319-27.

Boyd, E.S., T.L. Hamilton, J.R. Spear, M. Lavin, and J.W. Peters. 2010. [FeFe]-hydrogenase in Yellowstone National Park: evidence of dispersal limitation and phylogenetic niche conservatism. ISME J. 4:1485–1495.

Barkay, T., K. Kritee, E.S. Boyd, and G.G. Geesey. 2010. A thermophilic bacterial origin and subsequent constraints by redox, light, and salinity on the evolution of the microbial mercuric reductase. Environ. Microbiol. 12(11):2904-2917.

Mulder, D.M., E.S. Boyd, R. Sarma, J.A. Endrizzi, R. Lange, J.B. Broderick and J.W. Peters. 2010. Structure of HydA?EFG, a key intermediate in [FeFe]-hydrogenase H-cluster biosynthesis. Nature. 465: 248-252.

Current Projects

Photos

NAI Project Collaborators

Publications

  • Barkay, T., Kritee, K., Boyd, E., & Geesey, G. (2010). A thermophilic bacterial origin and subsequent constraints by redox, light and salinity on the evolution of the microbial mercuric reductase. Environmental Microbiology, 12(11), 2904–2917. doi:10.1111/j.1462-2920.2010.02260.x

    See Project

  • Boyd, E. S., Anbar, A. D., Miller, S., Hamilton, T. L., Lavin, M., & Peters, J. W. (2011). A late methanogen origin for molybdenum-dependent nitrogenase. Geobiology, 9(3), 221–232. doi:10.1111/j.1472-4669.2011.00278.x

    See Project See Project See Project See Project See Project See Project

  • Boyd, E. S., Fecteau, K. M., Havig, J. R., Shock, E. L., & Peters, J. W. (2012). Modeling the Habitat Range of Phototrophs in Yellowstone National Park: Toward the Development of a Comprehensive Fitness Landscape. Frontiers in Microbiology, 3. doi:10.3389/fmicb.2012.00221

    See Project See Project

  • Boyd, E. S., Hamilton, T. L., & Peters, J. W. (2011). An Alternative Path for the Evolution of Biological Nitrogen Fixation. Frontiers in Microbiology, 2. doi:10.3389/fmicb.2011.00205

    See Project See Project See Project See Project

  • Boyd, E. S., Hamilton, T. L., Spear, J. R., Lavin, M., & Peters, J. W. (2010). -hydrogenase in Yellowstone National Park: evidence for dispersal limitation and phylogenetic niche conservatism. ISME J, 4(12), 1485–1495. doi:10.1038/ismej.2010.76

    See Project

  • Boyd, E. S., Lange, R. K., Mitchell, A. C., Havig, J. R., Hamilton, T. L., Lafreniere, M. J., … Skidmore, M. (2011). Diversity, Abundance, and Potential Activity of Nitrifying and Nitrate-Reducing Microbial Assemblages in a Subglacial Ecosystem. Applied and Environmental Microbiology, 77(14), 4778–4787. doi:10.1128/aem.00376-11

    See Project See Project See Project

  • Boyd, E. S., Pearson, A., Pi, Y., Li, W-J., Zhang, Y. G., He, L., … Geesey, G. G. (2010). Temperature and pH controls on glycerol dibiphytanyl glycerol tetraether lipid composition in the hyperthermophilic crenarchaeon Acidilobus sulfurireducens. Extremophiles, 15(1), 59–65. doi:10.1007/s00792-010-0339-y

    See Project

  • Boyd, E. S., Skidmore, M., Mitchell, A. C., Bakermans, C., & Peters, J. W. (2010). Methanogenesis in subglacial sediments. Environmental Microbiology Reports, 2(5), 685–692. doi:10.1111/j.1758-2229.2010.00162.x

    See Project

  • Boyd, E. S., Spear, J. R., & Peters, J. W. (2009). [FeFe] Hydrogenase Genetic Diversity Provides Insight into Molecular Adaptation in a Saline Microbial Mat Community. Applied and Environmental Microbiology, 75(13), 4620–4623. doi:10.1128/aem.00582-09

    See Project See Project

  • Brown, I. I., Bryant, D. A., Casamatta, D., Thomas-Keprta, K. L., Sarkisova, S. A., Shen, G., … McKay, D. S. (2010). Polyphasic Characterization of a Thermotolerant Siderophilic Filamentous Cyanobacterium That Produces Intracellular Iron Deposits. Applied and Environmental Microbiology, 76(19), 6664–6672. doi:10.1128/aem.00662-10

    See Project

  • Driesener, R. C., Challand, M. R., McGlynn, S. E., Shepard, E. M., Boyd, E. S., Broderick, J. B., … Roach, P. L. (2010). -Hydrogenase Cyanide Ligands Derived From S-Adenosylmethionine-Dependent Cleavage of Tyrosine. Angewandte Chemie International Edition, 49(9), 1687–1690. doi:10.1002/anie.200907047

    See Project See Project See Project

  • Hamilton, T. L., Boyd, E. S., & Peters, J. W. (2011). Environmental Constraints Underpin the Distribution and Phylogenetic Diversity of nifH in the Yellowstone Geothermal Complex. Microbial Ecology, 61(4), 860–870. doi:10.1007/s00248-011-9824-9

    See Project

  • Hamilton, T. L., Lange, R. K., Boyd, E. S., & Peters, J. W. (2011). Biological nitrogen fixation in acidic high-temperature geothermal springs in Yellowstone National Park, Wyoming. Environmental Microbiology, 13(8), 2204–2215. doi:10.1111/j.1462-2920.2011.02475.x

    See Project See Project See Project

  • Hamilton, T. L., Vogl, K., Bryant, D. A., Boyd, E. S., & Peters, J. W. (2011). Environmental constraints defining the distribution, composition, and evolution of chlorophototrophs in thermal features of Yellowstone National Park. Geobiology, 10(3), 236–249. doi:10.1111/j.1472-4669.2011.00296.x

    See Project See Project

  • McGlynn, S. E., Boyd, E. S., Shepard, E. M., Lange, R. K., Gerlach, R., Broderick, J. B., & Peters, J. W. (2009). Identification and Characterization of a Novel Member of the Radical AdoMet Enzyme Superfamily and Implications for the Biosynthesis of the Hmd Hydrogenase Active Site Cofactor. Journal of Bacteriology, 192(2), 595–598. doi:10.1128/jb.01125-09

    See Project See Project

  • McGlynn, S. E., Boyd, E. S., Shepard, E. M., Lange, R. K., Gerlach, R., Broderick, J. B., & Peters, J. W. (2009). Identification and Characterization of a Novel Member of the Radical AdoMet Enzyme Superfamily and Implications for the Biosynthesis of the Hmd Hydrogenase Active Site Cofactor. Journal of Bacteriology, 192(2), 595–598. doi:10.1128/jb.01125-09

    See Project See Project See Project See Project See Project

  • Meuser, J. E., Boyd, E. S., Ananyev, G., Karns, D., Radakovits, R., Narayana Murthy, U. M., … Posewitz, M. C. (2011). Evolutionary significance of an algal gene encoding an [FeFe]-hydrogenase with F-domain homology and hydrogenase activity in Chlorella variabilis NC64A. Planta, 234(4), 829–843. doi:10.1007/s00425-011-1431-y

    See Project

  • Mulder, D. W., Boyd, E. S., Sarma, R., Lange, R. K., Endrizzi, J. A., Broderick, J. B., & Peters, J. W. (2010). Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG. Nature, 465(7295), 248–251. doi:10.1038/nature08993

    See Project See Project See Project See Project See Project See Project

  • Peters, J. W., Boyd, E. S., D’Adamo, S., Mulder, D. W., Therien, J., & Posewitz, M. C. (2012). Hydrogenases, Nitrogenases, Anoxia, and H2 Production in Water-Oxidizing Phototrophs. Algae for Biofuels and Energy, None, 37–75. doi:10.1007/978-94-007-5479-9_3

    See Project

  • Schut, G. J., Boyd, E. S., Peters, J. W., & Adams, M. W. W. (2013). The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications. FEMS Microbiol Rev, 37(2), 182–203. doi:10.1111/j.1574-6976.2012.00346.x

    See Project

  • Shepard, E. M., Boyd, E. S., Broderick, J. B., & Peters, J. W. (2011). Biosynthesis of complex iron–sulfur enzymes. Current Opinion in Chemical Biology, 15(2), 319–327. doi:10.1016/j.cbpa.2011.02.012

    See Project See Project See Project See Project See Project See Project See Project

  • Soboh, B., Boyd, E. S., Zhao, D., Peters, J. W., & Rubio, L. M. (2010). Substrate specificity and evolutionary implications of a NifDK enzyme carrying NifB-co at its active site. FEBS Letters, 584(8), 1487–1492. doi:10.1016/j.febslet.2010.02.064

    See Project See Project See Project See Project See Project See Project

  • Wang, Y., Boyd, E., Crane, S., Lu-Irving, P., Krabbenhoft, D., King, S., … Barkay, T. (2011). Environmental Conditions Constrain the Distribution and Diversity of Archaeal merA in Yellowstone National Park, Wyoming, U.S.A.. Microbial Ecology, 62(4), 739–752. doi:10.1007/s00248-011-9890-z

    See Project

  • Zadvornyy, O. A., Allen, M., Brumfield, S. K., Varpness, Z., Boyd, E. S., Zorin, N. A., … Peters, J. W. (2010). Hydrogen Enhances Nickel Tolerance in the Purple Sulfur Bacterium Thiocapsa roseopersicina. Environ. Sci. Technol., 44(2), 834–840. doi:10.1021/es901580n

    See Project
  • Anbar, A.D., Boyd, E.S., Buick, R., Claire, M., Des Marais, D., Domagal-Goldman, S., Eigenbrode, J., Erwin, D., Freeman, K., Hazen, R., Johnson, C., Lyons, T., Meadows, V., Ohmoto, H., Ono, S., Peters, J.W., Shapiro, B., Summons, R. & Walter, M.  (2010).  An Archean biosphere initiative [abstract 5593]. Astrobiology Science Conference 2010. See Project
  • Arslan, B., Boyd, E.S., Dolci, W., Dodson, E., Boldt, M. & Pilcher, C.  (2011).  Workshop without walls: Broadening access to science around the world.  PLOS Biology, 9.  doi:e1001118 See Project
  • Arslan, B.K., Boyd, E.S., Dolci, W.W., Dodson, K.E., Boldt, M.S. & Pilcher, C.B.  (2011).  Workshop without Walls: Broadening access to science around the world.  PLoS Biol, 8: e1001118. See Project
  • Boyd, E.S. & Druschel, G.K.  (In Review).  The role of intermediate sulfur compounds in the reduction of elemental sulfur by Acidilobus sulfurireducens. See Project
  • Boyd, E.S., Anbar, A.D., Miller, S., Hamilton, T.L., Lavin, M. & Peters, J.W.  (Submitted).  An early origin for Molybdenum-nitrogenase.  Science. See Project
  • Boyd, E.S., Pearson, A., Pi, Y., Li, W-J., Zhang, Y.G., He, L., Zhang, C.L. & Geesey, G.G.  (2011).  Physicochemical influences on glycerol dialkyl glycerol tetraether lipid composition in the crenarchaeote Acidilobus sulfurireducens.  Extremophiles, 15(1): 59–65. See Project
  • Glass, J.B., Boyd, E.S., Romaniello, S. & Anbar, A.D.  (2010).  Evolutionary metallomics: A nickel for nitrogenase.  Nature Geoscience. See Project
  • Glass, J.B., Boyd, E.S., Romaniello, S.J. & Anbar, A.D.  (2010).  Evolutionary metallomics: a nickel for nitrogenase.  In review. See Project
  • Hamilton, T.L., Boyd, E.S. & Peters, J.W.  (2010).  Geochemical controls on the phylogenetic structure and composition of NifH in Yellowstone National Park.  In review. See Project
  • Meuser, J.E., Boyd, E.S., Ananyev, G., Karns, D., Murthy, N.U.M., Radakovits, R., Dismukes, G.C., Ghirardi, M.L., Peters, J.W. & Posewitz, M.C.  (2010).  Presence of F-clusters in the Chlorella NC64A [FeFe]-hydrogenases provides new details into the evolution and diversity of algal hydrogen metabolism.  Planta, Revision requested. See Project
  • View all 34 publications

Past NAI Teams