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2010 Annual Science Report

Montana State University Reporting  |  SEP 2009 – AUG 2010

Functional Based Habitability – Defining the Environmental Factors That Constrain Modes of Microbial Metabolism

Project Summary

To set the stage for space exploration and the search for life in the universe, it is necessary to establish the boundaries that define habiltability on Earth. Previous studies have emphasized using simple binary parameters to establish where life occurs and where life does not occur on Earth. We are attempting to take this to another level and establish through mutlivariable statistics the parameters that not only constrain the life but what parameters constrain the set of metabolic processes that sustain life as a function of environment.

4 Institutions
3 Teams
10 Publications
6 Field Sites
Field Sites

Project Progress

In parallel to our evolutionary studies, we are examining the distribution and diversity of genes involved in aspects of hydrogen metabolism, nitrogen fixation, photosynthesis, methanogenesis, ammonia oxidation, and nitrate reduction in extreme environments. Such environments include the geothermal springs in Yellowstone National Park, Wyoming, various saline environments in Utah and Northern Mexico. The work dovetails nicely with the work on subglacial methanogenesis that is reported on separately as this is a project spearheaded by NAI Postdoctoral Program Fellow, Dr. Eric Boyd. In work in Guerrero Negro in Baja, Mexico we have been able to show that numerous enzymes involved in hydrogen metabolism and fermentation are found in the upper layer of dense microbial mats. This upper layer of the microbial mat is characterized by a high microbial diversiry and dominated by oxygenic phototrophs and our results suggest that during the dark that many fermentative organisms that presumably grow using the reduced carbon metabolic end products of oxygenic phototrophs use hydrogenases to recycle electron carriers. This indicates that the mat upper layer cycles between being an oxic environment during the day and anoxic during the dark and that fermentative organisms in this environment have adapted to tolerate during periods of high oxygen tension. Similar results have been obtained in the water column of the Great Salt Lake where the region of the water column that presumably cycles between high levels of oxygen and anaerobicity, again are characterized by high levels of microbial diversity and clear evidence for fermentative metabolisms involving hydrogenases as a mechanism to recycle electron carriers. Our work in Yellowstone National Park (YNP) has perhaps been most significant in this area and most insightful in terms of the goals of our NAI research and the NAI Roadmap. We have been examining a large number of sites within YNP that as a whole represent large ranges of temperatures, pH, and mineral contents. 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 the specific gene products involved in the aforementioned metabolic processes. For example, in a recent report we have been able to show by examining amplified sequences of a structural gene involved in hydrogen metabolism that the occurrence and diversity of [FeFe]-hydrogenases is constrained by pH and geographic distance. In the next year of support we will examine the environmental factors that drive the occurrence of other metabolic processes we can place as being paramount in early life and relate the ecology as a function of metabolism to the traditional taxonomic indicators of microbial ecology to gain insights into the environmental factors that perhaps constrained aspects of the metabolism of early life on Earth.

Major Research Sites for Fuctional Based Habitability

Major research sites for our examination of the environmental factors which constrain the distribution and diversity of modes of hydrogen metabolism, nitrogen cycling, and photosynthesis. The hypersaline environments of the Guerrero Negro stratified mats, the Great Salt Lake salt saturated aqueous environments, and the pH, temperature, and mineral diversity of the hot springs environments in Yellowstone National Park.

Characteristics and Diversity of HydA ([FeFe]-hydrogenase) Sequences in Guerrero NegroMats

Phylogenetic tree based on deduced putative HydA amino acid sequences from Guerrero Negro and reference HydA sequences. Nodes with posterior probabilities of <50% were collapsed in this analysis (posterior probabilities of 100 are denoted by asterisks). Bar, one substitution per 10 sites. (B) Partial-length deduced amino acid sequences of environmental and reference deduced HydA sequences illustrating the phylogenetic coherence of novel substitutions and insertions in and upstream of L1 sequence motif.

Distribution of [FeFe]-Hydrogenase and Photosynthesis Genes in Yellowstone Hot Springs

Distribution of hydA (a) and bchL (b) in sediment and mat sampled from 65 geothermal springs from four geographic locations in Yellowstone National Park as a function of spring water pH and temperature. Red squares denote environments where amplicons were detected and blue triangles denote environments where amplicons were not detected.

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

  • 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

  • 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

  • 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

  • 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

  • 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

  • Inskeep, W. P., Rusch, D. B., Jay, Z. J., Herrgard, M. J., Kozubal, M. A., Richardson, T. H., … Frazier, M. (2010). Metagenomes from High-Temperature Chemotrophic Systems Reveal Geochemical Controls on Microbial Community Structure and Function. PLoS ONE, 5(3), e9773. doi:10.1371/journal.pone.0009773

  • 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

  • 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.
  • 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.
  • PROJECT INVESTIGATORS:
  • PROJECT MEMBERS:
    Eric Boyd
    Project Investigator

    John Peters
    Project Investigator

    Trinity Hamilton
    Doctoral Student

    Rachel Lange
    Undergraduate Student

  • RELATED OBJECTIVES:
    Objective 5.1
    Environment-dependent, molecular evolution in microorganisms

    Objective 5.2
    Co-evolution of microbial communities

    Objective 5.3
    Biochemical adaptation to extreme environments

    Objective 6.1
    Effects of environmental changes on microbial ecosystems

    Objective 6.2
    Adaptation and evolution of life beyond Earth