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Summary As we enter the twenty-first century, the polar biological sciences stand well poised to address numerous important issues, many of which were unrecognized as little as 10 years ago. From the effects of global warming and elevated ultraviolet radiation on polar organisms to the potential for life in subglacial Lake Vostok, the opportunities to advance our understanding of polar ecosystems are unprecedented. At the same time, the biological sciences are in the midst of a major change in techno- logical capabilities. The era of "genome-enabled" biology is upon us, and these new technologies will allow us to examine polar biological ques- tions of unprecedented scope and to do so with extraordinary depth and . . preclslon. All polar biological disciplines with applicability to polar regions, including systematics, microbiology, ecology, evolutionary biology, physiology, biochemistry, and molecular biology, will be transformed by exploiting the new technologies available to biologists. These genome- enabled methods will allow us to examine the genomic structure of organisms and communities, monitor changes in the expression of genes, and obtain detailed images of how the physiologies of organisms are affected by natural or anthropogenic changes in the environment. Complementing the broad array of technologies associated with genomics are other new enabling technologies, such as platforms equipped to monitor blames in real time and autonomous underwater vehicles that will expand our spatial and temporal understanding of marine and ter- restrial communities and their dynamics. The new approaches and tools

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2 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA are not ends in themselves but pathways into a new frontier of science opportunities. The Committee on Frontiers in Polar Biology (see Appendix A for committee membership) examined the opportunities and challenges of using the new technologies and methods of biology to conduct research on key questions related to Arctic and Antarctic organisms. Specifically, the study committee was given the following charge: Identify high-priority research questions that can benefit most from the new tools of biology in polar regions and recommend ways to facili- tate and accelerate the transfer and use of genomic technologies to answer fundamental questions about Arctic and Antarctic organisms. Discuss the potential applications of genomic sciences and func- tional genomics to molecular biology, microbiology, biochemistry, physi- ology, evolutionary processes, and microbial ecology in polar regions and identify the need for development of new technologies or methods spe- cifically for polar regions. Seek ways to facilitate increased interaction between biological sci- entists working in polar regions and other biological scientists. Assess impediments to the conduct of polar genomic research, such as issues related to facilities, infrastructure, and maintenance of biological sample collections and issues related to manpower and education needs. The committee conducted its analysis in a series of meetings. To gather input from the wider scientific community, the committee orga- nized a special two-day Workshop on Frontiers in Polar Biology (see Appendixes B and C for workshop agenda and list of participants). Workshop participants included biologists with expertise in microbial, protistan, soil, plant, invertebrate, fish, bird, and mammalian systems; in paleobiology and astrobiology; in genomics and bioinformatics; and in education and outreach. To exploit synergies of perspective, the work- shop was also balanced among biologists who conduct research in the Arctic, in the Antarctic, and in nonpolar environments. The breadth of expertise helped the committee identify key science questions and assess the opportunities and challenges associated with exploiting new genomic (and complementary nongenomic) technologies in polar biological research. WHY POLAR BIOLOGY? Clearly, biology in polar regions shares its traditions with all of biol- ogy it explores the same fundamental questions about organisms and ecosystems, from essentially the same diversity of disciplinary perspec- tives and using similar methods. Like the rest of biology, polar biology

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SUMMARY 3 has changed over time, because of both the increasing sophistication of our knowledge base and the advances in technology and computing power. But different regions of Earth have always offered their own compelling scientific opportunities and scientists often specialize so that they can explore these opportunities in depth. For the polar regions, great distances, physical isolation, long periods of darkness, and extreme climates have always posed special challenges- the challenges associated with getting to and operating in these environ- ments and of gaining a full perspective on a species when observations were limited to the "good" months when it is light and warm enough to conduct work. Thus, improvements in technology have always tied closely with advances in our ability to conduct science in polar regions and to expand the range of questions that could be addressed. Although some of the key research questions identified in this report indeed apply to other regions, there are reasons for the special polar emphasis. First, in general, polar regions remain one of the least studied and least under- stood ecosystems on the planet, and improving this understanding becomes more and more critical as we come to see the relationship of the polar regions with global processes. Second, and more specifi- cally, genome research applied to polar biology would serve as a useful "test bed" for temperate and tropical regions (e.g., there are tens of thou- sands of tropical fishes but only about 250 in Antarctica so our ability to develop a comprehensive view is enhanced). Finally, in the end we need thorough understanding of all ecosystems so that we can conduct com- parative studies across latitudinal clines, and these studies can then help elucidate physiological and biochemical mechanisms for adaptation in a way that no single perspective would allow. Polar ecosystems provide study systems that can yield major insights into a wide range of basic and applied issues in biological science. The distinct geological, oceanographic, and climatic histories of the Arctic and Antarctic have created two polar ecosystems that differ in some attributes while sharing similarities in others. The Arctic, in essence, is an ice- dominated ocean surrounded by large, continental landmasses with wide, shallow continental shelves; the Antarctic, on the other hand, is a glaciated continent featuring narrow, deep coastal margins and surrounded by an ice-covered ocean. Both polar ecosystems are predominantly cold, isolated, and subject to pronounced seasonal cycles of temperature and photo- period. Organisms not only survive, but thrive, under these extreme conditions, thus providing a unique perspective on the fundamental charac- teristics of life processes and the mechanisms of evolutionary adaptation. Many of the potential discoveries to be made in the study of adaptations of polar organisms stand not only to make important contributions to basic biological science but also to offer opportunities for advancing bio-

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4 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA technology and biomedicine for instance in the development of proto- cols for cryopreservation of cells, tissues, and other biological materials. Although remarkably well adapted to extreme physical conditions, polar organisms are highly sensitive to anthropogenic perturbation, such as the production of greenhouse gases and ozone-destroying chemicals. Human activities are already affecting polar ecosystems dramatically, and these effects are likely to increase in the future. If we are to predict the impact of environmental change on global ecosystems, it is critical that we evaluate closely and understand polar ecosystems, which in many ways may serve as "canaries in the coal mine" in terms of providing warnings about the effects of climate change worldwide. IMPORTANT QUESTIONS IN POLAR BIOLOGY The committee identified four major focal areas of polar biological research that could benefit significantly from the application of genome- enabled technologies. This categorization reflects the important contribu- tions that new technologies can make at all levels of biological organiza- tion, ranging from fundamental molecular-scale phenomena at the level of the genome to processes involving entire ecosystems and the human communities that depend on them. 1. Evolution and biodiversity of polar organisms. A major shaping force in the evolution of polar organisms and polar ecosystems was the devel- opment of the extreme physical conditions of the two polar regions, nota- bly their very low temperatures. Polar species thus provide exceptional models for analyzing adaptive evolutionary change in extreme environ- ments. Because the Arctic and Antarctic regions underwent glaciation during different geological epochs (Pleistocene and Miocene, respec- tively), comparison of adaptations in ecotypically equivalent boreal and austral taxa will provide important insights into convergent and diver- gent evolutionary adaptation. Permafrost, subglacial lakes, and other frozen environments may preserve a repository of ancient organisms and DNA that could be used (1) for analyses of biodiversity during different geological time periods and (2) to elucidate the evolutionary relationships between ancient and present-day organisms. What new types of genetic information have been gained to enable polar organisms to function well under the stressful physical conditions of the polar regions, especially extremes of cold? What "raw material" was used to fabricate the new types of genes found in cold-adapted polar organisms? Have Arctic and Antarctic species exploited similar or differ- ent genetic "raw material" to fabricate adaptations?

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SUMMARY 5 What types of genetic information have been lost during evolution under extremely stable thermal conditions, such as those found in major regions of the polar seas? Are some polar organisms especially suscep- tible to global warming as a result of having lost genetic information needed to allow adaptation to higher and more variable temperatures? Do polar species contain the genetic information needed to cope with anthropogenic stresses such as ozone depletion? How rapidly do the genomes of polar organisms evolve and what are the mechanisms of genomic change? How do the processes of gene transcription and protein translation compare in polar and nonpolar species? Do polar species manifest reduced capacities to alter gene expression in the face of environmental change? What is the evolutionary origin of the organisms present in the polar ice caps, glaciers, and subglacial lakes? Are they metabolically active; and if so, do they possess novel metabolic pathways? Are polar environments reservoirs of paleogenes that can facilitate the evolution of present-day species through lateral gene transfer? What are the determinants of microbial diversity in the marine and terrestrial ecosystems of the polar regions? 2. Polar physiology and biochemistry. The abilities of polar organisms to carry out the physiological and biochemical processes required for metabolism, growth, and reproduction under extreme climatic conditions are based on widespread adaptive change. Proteins, membranes, and other key biochemical components of polar species exhibit a broad suite of adaptations that may at once "fit" their biochemistry to polar condi- tions and at the same time limit their functional range to the extreme environments of the poles. Among the important questions related to physiological and biochemical systems are the following: How have many "cold-blooded" polar fishes and invertebrates succeeded in reducing their metabolic rates? Can these mechanisms be used in biotechnological and biomedical procedures? What evolutionary mechanisms are available to adapt/preserve enzymatic activity at low temperatures? Can insights from study of these cold-adapted proteins guide bio- technological development of commercially useful molecules; for example, enzymes with novel activities that work efficiently at low and moderate temperatures? What are the types of molecules that serve as "antifreeze" agents and ice-nucleators? How do these molecules work? What biotechnologi- cal and biomedical potential is represented by these molecules?

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6 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA What types of physiological and biochemical adaptations enable the cells and organs of some small Arctic mammals to survive at sub-zero temperatures during hibernation? Can these same mechanisms be ex- ploited in biomedical procedures including cryosurgery and cryostorage of tissues and organs? What sensing and regulatory pathways have polar organisms evolved to cope with abiotic stresses? 3. Polar microbial communities. A broad suite of questions can be addressed to advance our understanding of the functioning of polar microbial ecosystems. To these ends, appropriate genomic methodolo- gies must be linked to a variety of new methods for field investigation, including new drilling technologies and unmanned observatories. The potential rewards of these new lines of study are vast and include contri- butions to aquatic, terrestrial, and potentially, extraterrestrial biology. For example, the cryptoendolithic organisms and those dwelling in the peren- nially ice-covered lakes of the McMurdo Dry Valleys (which were once thought to be abiotic) have long been recognized as potential analogues of life (if any) on Mars. Similarly, the long-isolated microbial communities of Lake Vostok might serve as a model for evaluating the potential for life on Europa. Genome analysis of these organisms will provide us with an understanding of their origins and of genetic traits that might be expected in extraterrestrial life. Some key questions on polar ecosystem biology that can be addressed by creative use of genomics and other new tech- nologies are the following: What types of microorganisms are present in polar aquatic and terrestrial ecosystems and what roles do these microorganisms play in ecosystem processes? What is the relationship between the composition and bio- geochemical function of polar microbial communities? What factors control the composition, interaction, and productivity of the organisms in polar microbial aggregates? What is the lower temperature limit for evolving microbial life? Can we exploit an understanding of microbial life in Earth's polar regions to design probes and experiments to detect potential life in extra- terrestrial environments? 4. Assessment and remediation of human impact on polar ecosystems. The impacts of human activities on polar ecosystems range from the direct impacts of activities such as fishing to less direct effects due to atmo- spheric modifications (greenhouse gases and ozone-destroying chemi- cals). The use of genomic technologies and other new approaches will

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SUMMARY yield important insights into all spatial and temporal scales of human effects and may provide strategies for the remediation of human pertur- bation of polar environments. Among the questions that could be ad- dressed through application of these new technologies are the following: How will the thinning and shrinking of ice cover in Arctic marine habitats affect ecosystem structure? How will global warming influence the distributions of marine animal and plant species, for example, in the case of Arctic fishes that may have to remain in cold waters to find adequate nutrition? How will the loss of key species in polar communities affect eco- system functioning (e.g., net primary productivity, decomposition rates, carbon and nitrogen cycles) and community composition at temporal and spatial (local to landscape) scales? Will climate change increase the frequency and success of biologi- cal invasions? What ecosystem-wide changes will be caused by these . ~ Invasions ~ What is the potential of using genetic technologies as forensic tools? The utility of DNA methods in "environmental forensics" has been proven, for example, in the case of identifying species of whale meat sold commercially. Can these technologies be used for improved manage- ment of polar resources? What roles do soil microorganisms play in bioremediation in polar regions for instance, in soils contaminated by petroleum spills? Can new varieties of microorganisms be obtained from contaminated soils for use in bioremediation processes? To tap the full potential of genomics in addressing these and other key science questions, focused effort will be needed. The establishment of a Polar Genome Science Initiative would help address these research ques- tions effectively. The Polar Genome Science Initiative would need to include the following aims: generation of genetic and physical maps of genomes of selected polar species; high-throughput sequencing of genomic DNA and expressed genes; gene identification and annotation; population analysis via single-nucleotide polymorphisms; and transcriptome, proteome, metabolome, and envirogenome analyses. Because genome projects produce a high volume of sequence data and annotated information, a comprehensive Polar Genome Science Initia- tive must make provision for creation, curation, validation, and manage-

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8 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA ment of these databases and for bioinformatics tools necessary for insight- ful genome analyses. Selecting polar organisms for genome analysis needs careful thought to ensure that resources are targeted effectively. Choices should be based on evidence that: interest. analysis of its genome will address broad and significant scientific questions; it is a good model for evolution in an isolated polar environment; it provides opportunities for comparisons to organisms of compa- rable ecotype from polar habitats and along polar-to-temperate latitudinal clines; and/or its cellular processes possess characteristics of biotechnological Monitoring physiological and biochemical processes of polar organ- isms and monitoring polar ecosystems are keys to linking data generated from a Polar Genome Science Initiative to understanding and predicting organismal and ecosystem responses to environmental changes. Examples of novel approaches and advanced technologies for measuring biological processes include: multiple-element and compound-specific stable isotope analyses for studying photosynthetic and biogeochemical processes, respectively; stable isotope probing, an advanced culture-independent tech- nique for isolation of DNA from microorganisms at a species level; instrument packages and "tags" for measuring geoposition, water depth, heart rate, and blood chemistry of animals that are subsequently released back in the field; and "biosensors" to detect particular DNA molecules or antigens for characterizing the compositions of aquatic microbial communities or for tracking plankton blooms. COMPLEMENTS TO GENOMIC SCIENCE: ENABLING TECHNOLOGIES, FACILITIES, AND INFRASTRUCTURE The success of future polar genomic research depends not only on the new technologies available and the expertise of individual researchers but also on the equipment, infrastructure, and facilities that will enable researchers to sample, analyze, and experiment with organisms in polar ecosystems. The committee identified key technologies, infrastructure,

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SUMMARY 9 and facilities that have to be developed or improved to facilitate the advancement of polar genomic research. Sampling. Subglacial lakes that have been isolated from direct gas exchange with the atmosphere for perhaps 20 million years offer an in- credible research opportunity. Clean technology must be developed to avoid contaminating the lakes with contemporary microbiota. Sampling procedure can also be improved by the development of new fast-access drilling methods and of ice-traverse technology to enable efficient field operations. For marine research, improved technologies for collection and shipment of sensitive specimens must be developed. Notably, the ability to reliably preserve and ship sensitive samples to be used in molecular biological and chemical analyses to home laboratories is essen- tial to many research programs. Facilities. To facilitate genomic research in the Arctic, improved facili- ties for collection, analysis, and shipment of materials are needed. The Toolik and Barrow facilities of Alaska are operating at, or near, full capacity, so some expansion of these U.S.-based laboratories is desirable. In the eastern Arctic, U.S. biological research has traditionally been sup- ported through an international agreement with Denmark due to the lack of U.S.-based facilities in Greenland. Establishment of a U.S. Arctic labora- tory at Thule or negotiation of an agreement to allow U.S. polar biologists access to Svalbard would provide new opportunities to study northern polar ecosystems. Due to the difficulties in conducting work during the dark, extremely harsh, polar winter, a substantial fraction of research activity in polar regions is restricted to the warmer parts of the year when the sun is above the horizon. Thus, large gaps in our understanding of organism and ecosystem function exist because processes affecting life in the polar envi- ronment occur year-round. Year-round access to terrestrial and marine facilities will not only yield new scientific insights into natural systems but also allow greater flexibility for a broad range of scientists to partici- pate directly in field research. The opportunities provided by winter access could also encourage new participants to enter polar research. Given the scientific impetus for year-round sample collection and analysis, a base-funded and staffed repository for frozen samples of polar organisms is needed. A sample repository would ensure the proper archiving and curation of samples, ensure the provenance of samples submitted for deposition, and provide accessibility to samples from polar organisms to the broader community of biologists. Integration of research activities. Integration and synthesis of knowl- edge on the genomes, physiologies, and biochemistries of polar organisms, and the biogeochemical and physical characteristics of polar ecosystems,

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10 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA is an important challenge that must be addressed if polar biology is to realize its full potential. Integration requires creating possibilities for teams of scientists that work within a particular habitat to gather and share information and techniques. Likewise, researchers doing similar research in Arctic and Antarctic ecosystems must be encouraged to share information and insights. Programs such as the Arctic System Science Program serve to help unite the Arctic scientific community both within the United States and internationally. Conferences and workshops can be used to facilitate communication among scientists willing to cross biologi- cal disciplines and scales and to develop systemic understanding of the organism, habitat, or region under study. This kind of integration of knowledge will accelerate the infusion of genomics and other techniques into polar biology. Field courses and postdoctoral fellowships should be designed to encourage nonpolar scientists with relevant expertise to pursue studies in the Arctic and Antarctic and to collaborate with polar scientists. Increasing the flow of information to nonspecialists. In addition to increasing interactions between polar biologists and the broader commu- nity of biological scientists, continued efforts should be made to enhance the flow of information about polar biology to a wider audience because polar ecosystems play an important role in global-scale phenomena. Thus, what happens to organisms in polar ecosystems may have implications for biological processes in other terrestrial and aquatic ecosystems. Some potential strategies and venues for increasing awareness of polar biology and disseminating new discoveries to a wider audience include the following: Coverage of polar topics in textbooks and curricula should be expanded. Modern educational technology, such as real-time distance learning, should be used to bring students into close contact with polar biology. Additional strategies should be developed for bringing teachers and students into the field. Web sites should be developed that provide attractive, informa- tive, and up-to-date information to new audiences. Polar scientists should be encouraged to be proactive communi cators of discoveries to the media. Educational and outreach activities in the Arctic should also include the indigenous communities that are part of the ecosystem. The effort should be two-way, with scientists respecting and learning from the expe- riences of local residents. Encouraging local communities to contribute to research activities seems a wise approach for communicating what science

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SUMMARY 11 is being conducted and why and for identifying research questions and facilitating the research itself. FINDINGS AND RECOMMENDATIONS A New Unifying Approach to Polar Biological Research Finding 1: Genome science is an addition to, not a replacement for, other approaches to the study of polar biology. The applica- tion of new genomic technologies has the potential to be a unify- ing paradigm for polar biological sciences. Key opportunities include the following: Polar organisms and communities offer unique opportunities to study evolution using genome sciences. The use of genomic methods will give insights into the effects of global change on polar biota and biogeochemistry. Genome .~cience.s have vast potential for elucidating function in microbial communities. Polar genome sciences could make broad contributions to bio- medicine and biotechnology (for example, cryopreservation, cryosurgery, and cold-functioning enzymes). A polar genome research initiative will provide important new information on the evolution, physiology, and biochemistry of polar or- ganisms. Such information not only enhances our understanding of how polar ecosystems function but also helps our search for life in icy worlds. Recommendation 1-1: The National Science Foundation (NSF) should develop a major new initiative in polar genome sciences that emphasizes collaborative multidisciplinary research and co- ordinates research efforts. The Polar Genome Science Initiative could facilitate genome analyses of polar organisms and support the relevant research on their physiology, biochemistry, ecosys- tem function, and biotechnological applications. Recommendation 1-2: A new polar genome initiative should capitalize on data from existing Long-Term Ecological Research and Microbial Observatory sites to take advantage of the long- term datasets and the geographical distribution of these sites. Additional approaches may be taken so that research can be con- ducted at sites with comparable conditions at both poles. For example, there is currently no marine site in the Arctic.

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2 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA Coordination is Essential Finding 2: To facilitate the advancement of polar genome sci- ences, coordination of research efforts will be required to ensure efficient transfer of technologies, provide guidance to researchers on choosing organisms for genome analyses, and help in the development of new scientific initiatives. Coordination of research efforts should begin with syntheses of the available information, thereby avoiding duplication of research efforts. It should facili- tate increased communication among the polar scientists and also with nonpolar scientists who have expertise in genomics and other technological advances applicable to polar studies. Recommendation 2: NSF should form a scientific standing com- mittee to establish priorities and coordinate large-scale efforts for genome-enabled polar science (for example, genome sequencing, transcriptome analysis, and coordinated bioinformatics databases). Virtual Genome Science Centers Finding 3: Genomic technologies, both those currently available and those anticipated in the future, are applicable to some of the key questions in polar biology. However, the technical demands of genome science often transcend the resources of any individual researcher. Recommendation 3: NSF should support some mechanism to facilitate gene sequencing and related genomic activities beyond the budget of any individual principal investigator, such as vir- tual genome science centers. The purpose of the virtual centers would be to provide infrastructure for individual researchers and to facilitate technology transfer among researchers. New infra- structure is not needed, rather some type of coordinating body (e.g., University National Oceanographic Laboratory System, Ocean Drilling Program). Enabling Technologies Finding 4: Enabling technologies are critical to the successful application of genomic technologies to polar studies. Recommendation 4: Ancillary technologies such as observato- ries, ice drilling, remote sensing, mooring and autonomous

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SUMMARY sensors, and isotope approaches should be developed to support application of genomic technologies to polar studies. Increasing Awareness and Education Finding 5: Polar systems play important roles in global-scale phe- nomena and there is a need for enhanced flow of information about polar biology to a wide audience of scientists, policymakers, and the general public. Recommendation 5: NSF should continue its efforts to make information about polar regions available to teachers, schools, and the public. Short- and long-term plans should be developed for increasing public awareness of polar biology. In the near future, postdoctoral fellowships in polar biology could be set up to encourage young scientists to enter the field. Long-term plans should include continued efforts to incorporate polar biology in college and K-12 curricula. Impediments to Integrated Polar Science Finding 6: Impediments to conducting multidisciplinary inte- grated polar science exist, including administrative, fiscal, and infrastructure issues: 13 Coordination among directorates within NSF and coordination among agencies are both essential for advancing polar biology. International collaborations are vital for all polar research. Cur- rent procedures make the involvement of international scientists in U.S. polar biological projects difficult. Attempts to conduct comparative research at both poles can be difficult. Although NSF's Office of Polar Programs support research at both poles, grant applications for Arctic and Antarctic research have to be made to two separate NSF research programs. Research proposals often undergo two reviews and scientists must prepare separate budgets for each proposal. Infrastructure for Arctic and Antarctic biology needs improvement. The conduct of molecular research in the polar regions requires specific infrastructure, and there is no high-technology equipment for such work in the Arctic. Development of ice-drilling and clean-sampling technolo- gies in the Antarctic will facilitate research in deep ice and subglacial lakes.

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4 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA Recommendation 6-1: To reach the goal of getting excellent science done as efficiently as possible, NSF should remove im- pediments to cross-directorate funding. Because integrated polar science often requires interagency cooperation, NSF should lead by example and form partnerships with the National Aeronautics and Space Administration and others as relevant. Memoranda of understanding among directorates within NSF and among fund- ing agencies are one mechanism to facilitate transfer of informa- tion and coordination of research. Recommendation 6-2: Establishment of international research partnerships or memoranda of understanding will facilitate and enhance these collaborative efforts. Issues such as stipends, travel, visas, education, ship time, aircraft use, and other logisti- cal issues should be addressed in these memoranda to ensure successful operation of international collaborative polar research. Recommendation 6-3: More information is needed to develop solutions to problems related to conducting bipolar research. NSF should conduct a brief survey of researchers and research groups who would potentially work in both poles to identify impedi- ments and then take steps to address them. Recommendation 6-4: To facilitate integrated, multidisciplinary biological research at both poles, NSF will have to improve bio- logical laboratories and research vessels, and develop ice-drilling resources in the polar regions. Opportunities to allow year-round access to, and operation of, field sites should be pursued.