National Academies Press: OpenBook

Frontiers in Polar Biology in the Genomic Era (2003)

Chapter: 1. Introduction

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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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Suggested Citation:"1. Introduction." National Research Council. 2003. Frontiers in Polar Biology in the Genomic Era. Washington, DC: The National Academies Press. doi: 10.17226/10623.
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1 Introduction WHAT IS GENOMICS? Genomics, or genome science, is "the study of the structure, content, and evolution of genomes," including the "analysis of the expression and function of both gene and proteins" (Gibson and Muse, 2002~. In this context, genomics encompasses functional genomics (gene and protein expression and function), structural genomics (analysis of the three- dimensional structures of proteins), metabolomics (analysis of the metabolites produced and consumed by a population of cells), and many other "-omics" (e.g., ecogenomics, metagenomics, pharmacogenomics, toxicogenomics). Genome sciences make use of, and are integrated by, the related disciplines of bioinformatics and computational biology. These genomic approaches offer global or near-global overviews of gene lists, and gene and protein expression. Furthermore, genomic profiles enable the exploration of the genetic content of organisms that cannot be studied by classical genetic methods. The definitions of these and other special- ized terms will be introduced at first use and are summarized in Box 1-1. The major goal of this report is to suggest how these new genomic tech- nologies can foster increased understanding of polar biology by allowing novel types of studies that heretofore were not possible to conduct in polar settings. 15

16 INS ~ FO[~R BlO[OGy ~ ~ GENERIC Egg CEOLOCIC AND CLIMATIC TRENDS THAT INELOENCED EVOLOTION IN THE POLAR REGIONS Me distinct geologic and climatic histories of He Arctic and Antarctic have created To unique polar ecosystems that share some atb~utes ~h11e differing greatly in others. The Antarctic is a glaciated continent

INTRODUCTION 17 surrounded by a cold, often ice-covered ocean, while the Arctic is a cold, ice-dominated ocean surrounded by large, continental landmasses. The geologic and climatic histories that led to these different environments set the stage for the evolution of their respective biotas and disparate eco- systems (Figure 1-1~.

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INTRODUCTION 19 Antarctica and the Southern Ocean A globe of the Earth some 250 million years ago would show the continent we know as Antarctica today in the center of the vast super- continent Pangaea. Over time, major rifting events fragmented the super- continent until Antarctica developed its present shape. The rifting opened seaways between major oceans and changed the ocean circulation around the Antarctic continent. Throughout this time, Antarctica has remained in the low southern latitudes and has been in a near-polar position for roughly 100 million years (Lawyer et al., 1992~. Despite this polar posi- tion, the climate was initially quite warm. Seas around the continent had bottom-water temperatures ranging from 12 to 16°C (Kennett, 1977, 1982) and supported a complex fish fauna typical of contemporary temperate oceans (Eastman, 1991, 1993), while temperate vegetation flourished on land (Francis, 1999~. These temperate climatic conditions ended dramati- cally when rifting opened crucial oceanic passages, including the Tas- manian Seaway (~35 Ma) and the Drake Passage (~25 Ma), and declining atmospheric carbon dioxide levels combined to trigger profound Antarctic cooling and the onset of rapid glaciation (DeConto and Pollard, 2003~. The East Antarctic continent was likely glaciated for the first time about 34 million years ago (Zachos et al., 2001), but ice extent initially was probably quite variable (Barrett et al., 1987; DeConto and Pollard, 2003~. Further cooling shifted East Antarctica into a persistently cold mode (Demon and Hall, 2000) and allowed growth of the more dynamic West Antarctic ice sheet (Alley and Bindschadler, 2001~. The general cooling trend over tens of millions of years has been interrupted by important reversals (e.g., Scherer, 2002~. Still, overall, the present polar ocean sur- rounding Antarctica is the most severely and consistently cold marine environment on Earth (Dewitt, 1971; Littlepage, 1965~. Today, the footprint of global change is variable across Antarctica. The Dry Valleys of McMurdo Sound have cooled by 0.7 degree per de- cade between 1986 and 2000 (Doran et al., 2002~. The peninsula also is experiencing significant warming, and several ice shelves on the Antarc- tic Peninsula have retreated, some reduced to fragments of their original size (Turner et al., 2002~. Some of these changes have been dramatic: ice shelves breaking off ice bergs the size of small states or simply disinte- grating over the course of weeks, as was the case for the Larsen B ice shelf, where 3,250 km2 of shelf area disintegrated over a 35-day period begin- ning in lanuary 2002 <http: / /nsidc.org/iceshelves/larsenb2002/>. The temperature trend for much of the continent remains unresolved due to the paucity of data (Turner et al., 2001~.

20 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA The Arctic Ocean and its Surrounding Landmasses While the geologic framework has had a clear influence on the Ant- arctic environmental conditions, the tectonic control and the interconnec- tions of major ocean basins in the Arctic are less well defined. When growth of terrestrial ice sheets drew down sea level during the Quaternary, and perhaps earlier, the shallows of the Bering Straits became exposed as a land bridge connecting Asia and North America (Kennett, 1982), block- ing direct circulation between the Pacific and Arctic Oceans. Continental motions across the Atlantic Ocean shifted Eurasia and North America apart, contributing to improved communication between the Arctic Ocean and the Atlantic Ocean, while squeezing the Bering Straits and restricting Arctic Ocean communication with the Pacific. Although profound effects on oceanic circulation have resulted, the exact history is still unresolved (Kennett, 1982; NRC, 1991; Aagard et al., 1999~. Extensive glaciation of the Northern Hemisphere post-dated the Antarctic glaciation by over 30 million years. The first major glaciation probably occurred in the late Pliocene (Kennett, 1982) and was certainly occurring by the Pliocene-Pleistocene boundary, about 2.5 million years ago (Shackleton et al., 1984~. Since then, multiple cycles of ice sheet accu- mulation and melting have occurred, on 40,000 year and then 100,000 year cycles, each dramatically altering the biogeography of both terres- trial and marine organisms. These ice-sheet cycles appear to be driven by cycles in Earth's orbit that control the seasonal distribution of the sun's radiation (Clark et al., 1999~. The accompanying dramatic shifts included climatic zones displaced as many as 20-30 degrees of latitude and large fluctuations in ocean circulation patterns, sometimes over timescales of just hundreds of years. Dramatic changes in global atmospheric tempera- ture (5-8°C), called Dansgaard-Oeschger cycles, occurred at intervals of 1,000-3,000 years at least within the most recent glacial cycle (Iohnsen et al., 1992; GRIP Members; 1993; Grootes et al., 1993; Taylor et al., 1993; Raymo et al., 1998~. Moreover, transitions between climatic regimes have been very abrupt; for example, approximately 50 percent of the tempera- ture change associated with the last glacial period occurred in less than a decade (Severinghaus et al., 1998; NRC, 2002~. Today, the sea ice cover of the Arctic Ocean is in transition, losing 3 percent of the area of total ice cover and 7 percent of the area of multiyear ice per decade during recent decades (Johannessen et al., 1999; Kerr, l999~. The decline in sea ice extent is much greater than can be accounted for by natural climate variation (Vinnikov et al., 1999~. Recent surface warming and ice thinning in the Arctic may be caused by changes in the state of the Arctic Oscillation mode of atmospheric circulation (Moritz et al., 2002~. Global warming due to accumulation of anthropogenic greenhouse gases

INTRODUCTION 21 may also be driving the shrinkage, directly or by influencing the Arctic Oscillation. Observations by people indigenous to the Arctic confirm that changes to both the marine and terrestrial ecosystems are occurring more rapidly now than in the past (Krupnik and Jolly, 2002~. PHYSICAL PARAMETERS THAT SHAPE BIOLOGICAL PROCESSES The Antarctic and the Arctic present physical parameters that shape their biotic communities and processes, but as a result of their distinct histories some of these parameters are similar and some are quite different. S· ·1 · ~ 1mllarlhes · Both regions are cold, isolated, and subject to pronounced seasonal cycles of temperature and daylength. · Glaciers, icebergs, and sea ice profoundly influence the biogeo- graphic distribution of organisms in both regions and provide novel eco- logical niches for colonization. · Thermal conditions in both polar regions have served as an effec- tive barrier to colonization by temperate species, although global warm- ing is reducing this barrier. · Both regions are highly sensitive to anthropogenic impacts, such as chlorofluorocarbon (CFC)-induced ozone holes. Differences · The Southern Ocean has been remarkably cold and stable for at least 8 million years, whereas the Arctic Ocean cooled much more recently (~2.5 Ma). This difference in thermal history may have led to differences in breadth of thermal tolerance by Arctic and Antarctic organisms. · Arctic surface air temperatures are more variable than those of the Antarctic in annual, seasonal and daily timeframes and often may change by 40-50°C over a few days or on the same date between years. Tolerance of such rapid temperature variability may have driven the adaptive evo- lution of Arctic organisms in ways that are not experienced by Antarctic species. · Riverine freshwater and sediment discharge to the Arctic Ocean are substantial, whereas they are virtually nonexistent in the Antarctic. · Delivery of glacial icebergs, melt water, and till is of greater import to the Southern Ocean. · The continental shelves of the Arctic Ocean are broad and rela- tively shallow, whereas those of the Southern Ocean are narrow and deep.

22 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA Thus different types of benthic habitats are available in the two polar oceans. · Surface lakes and permafrost are prominent features of Arctic land- masses, whereas the Antarctic continent is covered by a massive ice sheet that has isolated subterranean lakes. · Given the predominance of ice in the Antarctic environment, the terrestrial flora and fauna of the Arctic are more diverse. · The Arctic is home to indigenous human populations. These people have a long and close relationship to the environment and associated biological resources and are affected when these resources change, whether because of natural variability or anthropogenic influences. EVOLUTION IN POLAR REGIONS The genetic structures of northern populations, communities, and species whether terrestrial or marine are the "genetic legacy" of rapid Quaternary climate changes (Hewitt, 2000), and the genomes of boreal species are expected to bear the signature of these changes. In the Antarc- tic, by contrast, the evolution of marine species has been driven by a long period of stable, low temperatures; and the relatively limited terrestrial ecosystems have been shaped by temperatures considerably more severe, but less variable, than those of the north. Indeed, the McMurdo Dry Valleys have been studied as an analogue for potential life on Mars, and subglacial Lake Vostok has been studied as model for possible life on Europa. The key to understanding the mechanisms of biotic evolution in the distinct polar regimes of the north and south lies in analysis of the genomes of organisms from major taxa at the individual, species, popula- tion, and community levels of biological organization. EXAMPLES OF RESEARCH AREAS THAT COULD BE ADDRESSED WITH GENOMIC TOOLS The development of sophisticated technologies for genome analysis, as well as other enabling technologies (such as remote sensing, and nanoscale biosensors), promises to revolutionize our understanding of polar organisms, communities, and ecosystems. Areas of research (explored in depth in Chapter 2) that offer potentially valuable opportu- nities include: · Polar ecosystems and global warming. Climate modeling and direct experimental measurement indicate that environmental change, includ- ing warming, will be most extreme in the polar regions. New genetic and genomic technologies, such as transcriptional profiling using microarrays

INTRODUCTION 23 and protein turnover studies via two-dimensional electrophoresis and mass spectrometry, can be leveraged to understand the impact of such change on individual species and on community structure. · Ecological impact of ultraviolet radiation. Due to the anthropogenic ozone hole that forms over Antarctica each austral spring, terrestrial and marine organisms of the photosphere experience levels of ultraviolet radiation that are much higher than those that were present during the evolution of these species. What are the impacts of this exposure on organismal fitness and community structure? Microarrays, proteomics, and metabolomics can be brought to bear to yield quantitative indicators of ecological impact. · Evolutionary mechanisms of adaptation to extreme environmental condi- tions. What molecular, biochemical, and physiological mechanisms enable polar organisms to survive, grow, reproduce, and indeed thrive, under extreme cold conditions? Because the Arctic and Antarctic regions under- went glaciation during different geological epochs (Pleistocene and Miocene, respectively), comparison of adaptations in ecotypically equiva- lent boreal and austral taxa will provide important insights into conver- gent and divergent evolutionary adaptation. Other major environmental variables that have influenced evolution in polar regions include the extreme variability of annual light cycles and the dry conditions of the Antarctic continent. · Systematics of polar organisms. In many instances, the phylogenetic relationships of polar organisms are poorly understood. Total-evidence phylogenetics, which incorporates molecular, cytological, and morpho- logical character sets, can be applied to resolve evolutionary ambiguities and enhance our understanding of the origin and radiation of key taxo- nomic groups. Analysis of whole genomes will greatly facilitate system- atic studies of polar organisms. · Gene flow. Measurement of gene flow between populations is criti- cal to understanding evolutionary speciation. Allele-specific microarray technology can be employed to determine the effect of gene flow between populations on the rates and patterns of speciation in polar regions. · Polar regions as extraterrestrial analogues. The cryptoendolithic and lake-dwelling organisms of the McMurdo Dry Valleys have long been recognized as potential analogues of life (if any) on Mars, just as perma- frost formations in the Arctic provide useful frozen habitat analogues. Similarly, the long-isolated (~20 million years), microbial communities of Lake Vostok in Antarctica and the severely chilled microorganisms in winter Arctic sea ice might serve as models for evaluating the potential for life on Europa. Genome analyses of these organisms will provide us with an understanding of their origins and of genetic traits that might be expected in extraterrestrial life.

24 FRONTIERS IN POLAR BIOLOGY IN THE GENOMIC ERA · Polar biotechnology. The uniquely cold-adapted enzymes of polar organisms provide numerous opportunities for biotechnological devel- opment. Proteases that function at temperatures near 0°C are already important for food processing and for cold-water detergent formulations. One can envision that enzymes from polar organisms will have numerous commercial applications where maintenance of low temperature is required. Molecules that protect polar organisms against damage from freezing also have important biotechnological applications.

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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 on polar organisms to the potential for life in subglacial Lake Vostok, the opportunities to advance our understanding of polar ecosystems are unprecedented. The era of “genome-enabled” biology is upon us, and new technologies will allow us to examine polar biological questions of unprecedented scope and to do so with extraordinary depth and precision.

Frontiers in Polar Biology in the Genomic Revolution highlights research areas in polar biology that can benefit from genomic technologies and assesses the impediments to the conduct of polar genomic research. It also emphasizes the importance of ancillary technologies to the successful application of genomic technologies to polar studies. It recommends the development of a new initiative in polar genome sciences that emphasizes collaborative multidisciplinary research to facilitate genome analyses of polar organisms and coordinate research efforts.

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