Background: Why study life in the cold? 

Despite the fact that >80% of the biosphere (by volume) is permanently below 5°C and most of the biomass is microbial, very little is known about the biology of microorganisms inhabiting permanently cold environments.   Recent discoveries of microbial life in deep glacier ice and subglacial environments have extended the known boundaries for life into icy realms.  The discovery of active microbial assemblages beneath glaciers and realization that large quantities of liquid water exist beneath polar ice sheets has resulted in a new paradigm in the study of life on Earth.  Considering this, it is vital to understand the biogeochemical contributions and role of permanently cold ecosystems in the biosphere.

The study of ecosystems in the cold deep biosphere also has implications for the natural history and evolution of life on Earth.  Geological evidence indicates that a long period of low latitude pervasive global glaciation occurred during the late Proterozoic, referred to as a “Snowball Earth” .  It is believed that the planet was completely covered in ice for at least 10 million years and liquid water only existed in the ocean under a thick ice cover. If this scenario is accurate, such a long period of global freeze would have had drastic consequences on ecosystems established prior to this event, and glacial and subglacial environments may have provided an important refuge for life during such an extended ice age. 

Microbial life appeared on Earth's surface rapidly after conditions were permissive (at least 3.9 billion years ago), and this coupled with an awareness of the tenacity life implies that geological and physical settings in the universe similar to those on Earth may also harbor life.  Polar ice caps composed of water ice exist on Mars, there is evidence for glaciers at lower latitudes during times of higher obliquity, and the jovian moon Europa is thought to maintain a 50-100 km deep liquid ocean under a 3-4 km ice shell. Thus, the study of cold, dark, subglacial environments on Earth will provide insight as to the likelihood of microbial life surviving and persisting in icy extraterrestrial environments. Furthermore, the challenge of identifying appropriate extraterrestrial sites for exploration and developing technology to sample icy subsurface environs will directly benefit from the experience gained by studying earthly analogs.

Current Research in the Christner Laboratory:

Microbial Activity in Solid Ice: Implications for Modifying the CO2 Record in Ice Cores 
Recent studies of microbial longevity in ancient glacial ice indicate that bacteria remain viable for hundreds of thousands of years while frozen. In the absence of metabolic activity, macromolecular damage must accumulate through amino acid racemization, DNA depurination, and exposure to natural ionizing radiation (e.g., 40K). Perhaps the species recovered are particularly successful at surviving metabolic dormancy over extended time frames, but it is also possible that such entrapped microbes might carry out a slow rate of metabolism to repair incurred macromolecular damage. We are examining the ability of bacteria isolated from glaciated environments to metabolize and respire CO2 in the liquid fraction of artificially constructed ice matrices. Experiments are underway to examine the influence of temperature and unfrozen water chemistry on microbial activity under frozen conditions. In addition, we are also studying the physiology of cells entrapped in ice by quantifying the fraction of viable and respiring cells and characterizing the genes and proteins expressed under frozen conditions. The presence of microbes within the aqueous fraction of the ice is fundamental to our research hypotheses, and we are using light and scanning electron microscopic analysis of the ice to determine the partitioning of both cells (visually) and solutes (elemental mapping) between the veins and the ice matrix. Importantly, the proposed research represents the first attempt to measure microbial CO2 respiration and macromolecular synthesis under environmental conditions (–5 to -20°C) in which elevated CO2 concentrations have been reported in glacial ice cores and basal ice from cold based glaciers.
Funding: National Science Foundation, Research in Biogeosciences

Biogeochemistry and Geomicrobiology of Taylor Glacier Basal Ice
To examine if microorganisms are metabolically active in glacier ice, we are conducting a comprehensive assessment of the biogeochemistry and geomicrobiology of Taylor Glacier (McMurdo Dry Valleys, Antarctica) basal ice via a combination of field measurements and laboratory experiments. A key component of the study is the ability extract parallel large volume samples (~10 kg) for analysis of nutrients, gas composition, d13C-CO2, cell density, metabolic activity, genomic DNA, and nucleotide ratios. Importantly, these large ice samples provide biomass (106-108 total cells) and CO2 in quantities ~100x greater than typically available using ice core materials, permitting experiments that are difficult or unfeasible with ice core archives, such as measuring the isotopic composition of CO2, nucleic acid characterization, and parallel biogeochemical and microbiological analyses.  Using this approach, we are able to connect nutrient availability, geochemical composition, and gas composition with microbial cell density, diversity and metabolic status in the basal ice sequence. Multi-sample analysis of the same ice facies is the best available method to understand the chemical and microbial process linkages in basal ice and the manner by which microbes may modify gas compositions in situ.
Funding: National Science Foundation, Office of Polar Programs

ICIBASE tunnellers: Top (l-r) Timothy Brox, Scott Montross, and Shawn Doyle. Bottom (l-r) Pierre Amato and Brent Christner.

Biological Ice Nuclei: is There a Bioprecipitation Cycle?  
Several species of plant-associated bacteria are known to have the capacity to freeze supercooled water at temperatures as warm as -1° C, which is catalyzed by a protein in the outer membrane of the bacterial cell. Due to the relatively warm temperatures at which ice-nucleating bacteria can function as freeze catalysts, these particles may impact meteorological processes by inducing precipitation (i.e., natural cloud seeding). The heterogeneous nucleation of supercooled water in clouds initiates ice crystal formation, and when the crystals become large enough, the particles precipitate out forming snow or rain. We are currently examining the distribution of biogenic ice nuclei in precipitation deposited under known environmental conditions from Louisiana, Montana, Wyoming, France, the Arctic, and Antarctica. Snowfall accumulated over long periods and transformed into glacier ice records samples of the atmospheric constituents in a chronological sequence. Through analysis of ice core samples, the occurrence of biogenic ice nuclei from known times and environmental conditions in the past can be examined. This study represents the first attempt to examine a direct link between atmospheric biogenic ice nuclei and the hydrological cycle.
Funding: Louisiana State University, Office of Research and Economic Development

Collaborations:

L. DeWayne Cecil (United States Geological Survey)
Christine Foreman (Montana State University)
Cindy Morris (Institut National de la Recerche Agronomique, France)
John Priscu (Montana State University)
James Raymond (University of Nevada at Las Vegas)
David Sands (Montana State University)
Stephan Schuster (Pennsylvania State University)
Mark Skidmore (Montana State University)
Todd Sowers (Pennsylvania State University)
Jean-Louis Tison (Free University, Belgium)
 
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