Research on the lakes of the McMurdo Dry Valleys (MCM) began with the advent of the International Geophysical Year (IGY) in the late 1950's (e.g., Ragotzkie and Likens 1964). IGY research revealed the physical/chemical nature of the lakes, showed that they were the only year-round liquid water environments on the continent, and inferred that the biological systems in the permanently icecovered lakes must possess novel physiological strategies that allow them to survive at low temperature and under extended darkness (Goldman 1964, Goldman et al. 1967). The seminal studies during IGY provided the framework for subsequent hypotheses driven research which now forms the basis for the ongoing MCM Long Term Ecological Research (LTER) lake program (now in its 15th season; www.mcmlter.org) and the MCM dry valley lake Microbial Observatory (MO, mcm-dvlakesmo.montana.edu). Data collected on Lakes Bonney, Hoare and Fryxell (all in the Taylor Valley) as part of these long term studies have now shown that most organisms in the lakes are not just "surviving the extremes" but are actively feeding, growing and reproducing (e.g., Priscu 1987a,b, Takacs and Priscu 1998, Laybourn-Parry et al. 2005). As such, they are ecosystems in which we can identify and begin to understand physiological and genomic adaptations in the context of one of the most extreme environments on our planet. Unfortunately, almost all "hands-on" research on the MCM lakes has been restricted to the austral spring and early summer (~October through January) when logistical support has allowed access to the area. Although studies during the spring-summer period have yielded a quantum increase in our understanding of the lakes, the unique aspects of physiological adaptation, biodiversity and ecosystem function during the permanently cold and prolonged darkness of the Antarctic winter will never be understood without extended season research (Priscu 1999, Priscu et al. 1999, NRC 2003). The U.S. component of "International Polar Year 2007-2008" (IPY), through the research initiative "Adaptations to life in extreme cold and prolonged darkness," now provides an important framework in which to study biological adaptation/acclimation by plankton to extreme cold and prolonged darkness at the cellular, genomic and ecosystem level. We propose to study lakes within the Taylor Valley during the transition to polar night to test the overarching hypothesis that the onset of darkness induces a cascade of physiological changes that alters the functional roles of autotrophic and heterotrophic microplankton within the lakes. This overarching theme will be addressed through an interdisciplinary study of selected biological components of the lakes using genomic and physiological tools to understand not only how individual organisms survive, but how they control ecosystem function during this seasonal transition. This theme is directly relevant to IPY objectives, and the data will be critical to our knowledge of how polar organisms survive and function within high latitude ecosystems characterized by extreme cold and prolonged darkness.

The extended season research we propose as part of the IPY initiative will allow us to build upon a large body of published field work and laboratory studies that have generated multiple hypotheses and predictions about a lengthy, but poorly understood, period of the annual cycle.

We propose to:

  1. extend the routine measurements that are part of the MCM LTER and MO projects beyond January to early April in Lakes Bonney, Hoare and Fryxell, and
  2. to conduct experiments designed to examine the physiological and biochemical changes that occur in selected components of the food web during the transition to polar night.

The proposed experiments will utilize physiological and genomic tools to test hypotheses derived from summer and winter-summer data collections. These new activities have been planned to optimize the potential for synthesis with existing long-term data sets, thus maximizing our efforts to understand the relationships between microbial adaptation and ecosystem function in the cold and prolonged dark environments found in the MCM lakes. Examination of multiple food web components and their linkages will make efficient use of the intense logistical efforts that will be required to extend the research season while providing seminal data to drive the curiosity of future researchers.

Hypotheses

Overarching Hypothesis:

Polar night induces a cascade of physiological changes that alters the functional roles of autotrophic and heterotropic microplankton within the lakes.

Specific Hypotheses:

  1. Primary production during the transition to polar night will be significantly higher than predicted from measured sub-ice irradiance and models based on spring photophysiology parameters.
  2. Functional downregulation of the photochemical apparatus during the summer-winter transition is integral to the overwintering strategy of phytoplankton.
  3. The photosynthetic process will be structurally altered at the level of gene expression in phototrophic communities during the summer-winter transition.
  4. Phytoplankton capable of mixotrophy survive the winter by becoming progressively more heterotrophic during the transition to polar night.
  5. Bacterial activity and metabolic diversity will decrease in response to a diminished source of fresh carbon as phytoplankton photosynthesis declines during the onset of winter darkness.
  6. Chemoautotrophic bacterial production provides a source of primary production to the ecosystem during polar night.

Objectives

Our hypotheses are based to a large degree on results from models, experiments on cultures, and what we learned during our past study of the winter to summer transition. We will focus on selected components of the plankton in the MCM lakes with the objective of elucidating those aspects of their genetics, biochemistry and metabolism that are critical to understanding their transition to the permanently cold and prolonged darkness of polar winter. Our overall objectives are presented here as they relate to our specific hypotheses:

Specific Objective (with hypothesis addressed):

  1. (all Hypotheses) Characterize physical, chemical and biological conditions in the lakes through early April by employing methods currently used by the MCM LTER and MO.
  2. (H1) Characterize phytoplankton photosynthesis in terms of quantum yields, light harvesting, saturation, and quenching, then develop a model based on these data to estimate annual primary production.
  3. (H2) Determine the photochemical function and modulations in major photosynthetic proteins in natural phytoplankton populations, and monocultures of C. raudensis UWO 241 returned to its natural environment.
  4. (H3)Construct cDNA libraries of environmental and field incubated monocultures of C. raudensis RNA samples, then probe the libraries with primers that target transcripts of major photosynthetic genes.
  5. (H3) Quantify global protein levels in field incubated monocultures of C. raudensis
  6. (H4) Conduct simultaneous grazing and photosynthesis experiments to derive mixotrophy vs. irradiance relationships.
  7. (H5) Identify phylotype specific changes in microbial activity during the summer-winter transition.
  8. (H6) Differentiate chemoautotrophic and heterotrophic bacterial metabolism through the transition from summer to polar night.

Significance

Relevance to IPY

  1. The year 2007 will mark the 125th anniversary of the First International Polar Year (1882-1883), the75th anniversary of the Second Polar Year (1932-1933), and the 50th anniversary of the International Geophysical Year (1957-1958). The IPYs and IGY were major initiatives, which resulted in significant new insights into global processes, and led ultimately to decades of invaluable polar research. The last global polar research effort (IGY) exploited technologies developed during World War II. The present IPY provides the opportunity to exploit modern technological advances in both logistics and science. Despite the investment of substantial effort in polar exploration and research over the years, the relative inaccessibility and harsh environment of the polar regions have left them less well studied than other areas of the planet. At a time of growing evidence that human activities are driving planetary processes into a previously unexplored state, especially in the polar regions, this crucial knowledge gap must be filled. Our proposed research addresses the U.S. IPY emphasis area: "Examine biological adaptations at the cellular and genomic level to life in extreme cold and prolonged darkness." Although year-round access is needed to understand biological adaptations in the MCM lakes, our proposed studies during the transition from summer to polar night, in concert with ongoing spring-summer research, is the logical (and most logistically feasible) next step to provide important new information toward our understanding of winter processes.
  2. The International Council for Science's outline for IPY (ICSU 2004) states that projects should be multidisciplinary, international, and able to promote the next generation of polar scientists. Our proposal brings scientists together with backgrounds in limnology, molecular biology, photobiology, microbiology and protozoology to address biological adaptations to cold and prolonged darkness. The United Kingdom will be represented in our project by the esteemed Johanna Laybourn-Parry who will examine physiological strategies to darkness, a topic she has examined in lakes on other parts of the Antarctic continent for many years. Our project will also promote two of the most promising female new investigators in polar biology, Rachael Morgan-Kiss and Jill Mikucki, to carry the legacy of IPY into the future.
  3. The MCM lakes have been the focus of intensive long-term studies by NSF funded LTER and MO projects. Frustration exists among scientists working on these projects because of the short field season, which has not allowed them to collect the year-round samples and data needed to understand how organisms adapt to prolonged darkness and how they function within the ecosystem. These two projects will be active through IPY and will collect important data that will be used to support the research proposed here. As such, the LTER, MO and IPY efforts will provide a synergistic data set that will compliment each project while yielding important new data on biological adaptation and ecosystem function during the transition to polar night.
  4. Our results will be directly relevant to the IPY and SCAR programs SALE-UNITED and SCAR-SALE (salepo.tamu.edu), which are developing scientific plans for the eventual sampling of life in cold nd dark subglacial environments (see attached letter from M. Kennicutt). Priscu, as a member of SALE-UNITED (and convener of SCAR-SALE), is entitled to all privileges and recognition availed by its designation as an IPY program. These strong international ties and Priscu's participation in these programs provide an invaluable network of multidisciplinary scientists to interact with in our proposed dry valley IPY project.

Polar Ecology

  1. The MCM lakes are poised near a significant threshold; any small change in climate can lead to major ecosystem responses (Doran et al. 2002). These responses provide a sensitive barometer of environmental change and represent a signal with significant global consequences. The proposed work will contribute to our understanding of the importance of life in extreme environments to the global system, and how this life responds to changes in climate. Extended season datasets will allow an assessment of immediate ecosystem response to climate change, and provide information to understand how adaptation/acclimation and ecosystem biocomplexity are related to these changes.
  2. The MCM lakes are biologically simple compared to most aquatic ecosystems. The layers of biological complexity are relatively few and thus the power with which the functioning of biological processes can be understood is very high. Consequently, data obtained from the proposed research will provide unique insights into biological adaptation to cold and dark conditions.
  3. Results from our study will add to the growing body of literature on the physical, chemical and microbial dynamics of cold systems on our planet. Despite the fact that most of the biosphere on Earth is cold (Psenner et al. 1999, 2002, Priscu and Christner 2004) and most biomass is microbial (Whitman et al. 1998), relatively little is known about the biology of microorganisms in cold ecosystems, particularly during winter. Our collaboration with J. Laybourn-Parry, who has examined physiological strategies to darkness in Arctic and Antarctic lakes (e.g. Laybourn-Parry et al. 2005), will allow us to expand results from the proposed study to global polar scales.

Biological Diversity and Function

  1. Combining novel molecular approaches with traditional labeled-enrichment experiments will allow us to address questions of structure-function associations among the bacterial assemblages. Specifically, we will examine the importance of chemoautotrophic carbon fixation as a source of primary carbon production to the MCM lakes, which could fuel heterotrophic processes during polar darkness. Chemotrophy has been proposed to be an important source of new carbon beneath the sea ice in McMurdo Sound (Priscu et al. 1990) and may also be significant beneath the ice in the MCM lakes, particularly during winter.
  2. Our results will expand what is known about microbial biogeography to relatively understudied high latitude systems (Ben-Ari 2002, Chase and Leibold 2002).
  3. A recent NRC report (NRC 2003) specifically mentioned C. raudensis UWO 241 as an important candidate for total genome analysis. While genome sequencing is an important step in understanding the adaptation of an organism to life in its environment, the sequence data must be complemented with in situ metabolism and the functional role of the organism in an ecosystem to apply biological relevance to the code. The research we propose using this organism, originally isolated from Lake Bonney, will provide important ecological information with which to evaluate its adaptability to low temperature and prolonged darkness. The chloroplast genome for this organism will be sequenced by Morgan-Kiss within the next year and a proposal is in preparation for DOE to sequence the entire genome of this novel organism within the next 3 years.

Biogeochemistry

  1. The dry valley lakes lend themselves uniquely to studies of both how the environment controls the diversity of organisms and how diversity itself controls the functioning of ecosystems. Tackling this question with LTER, MO and IPY-based research will multiply the ecological contribution of research in the dry valleys. By working together with MCM LTER and MO PI's, we will form a very diverse group representing fields that have not often worked together in the past (glaciologists, geochemists, hydrologists, meteorologists, microbial ecologists, molecular biologists, photobiologists, traditional microbiologists, modelers). Given the sensitive and relatively simple biology in the dry valleys, our integrated approach will serve as a model for a broader integration of genomic and biogeosciences.
  2. Very few high latitude ecosystems have been studied intensively enough to describe annual patterns in biogeochemical sources and sinks. The spring-summer bias in data collection is not unique to the MCM lakes, and has its equivalents in polar oceanography and terrestrial ecology (Priscu 1999). Completion of this project will expand our understanding of the seasonal patterns in MCM lake biogeochemistry to the entire sunlit period, and provide a rare measurement-based assessment of annual photosynthetic carbon fixation for a high latitude ecosystem.