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Although the vast majority of ice that formed on the Antarctic continent over the past 34 million years has been lost to the oceans, pockets of ancient ice persist in the Dry Valleys of the Transantarctic Mountains. Here we report on the potential metabolic activity of microbes and the state of community DNA in ice derived from Mullins and upper Beacon Valleys. The minimum age of the former is 100 ka, whereas that of the latter is ≈8 Ma, making it the oldest known ice on Earth. In both samples, radiolabeled substrates were incorporated into macromolecules, and microbes grew in nutrient-enriched meltwaters, but metabolic activity and cell viability were critically compromised with age. Although a 165 rDNA-based community reconstruction suggested relatively low bacterial sequence diversity in both ice samples, metagenomic analyses of community DNA revealed many diverse orthologs to extant metabolic genes. Analyses of five ice samples, spanning the last 8 million years in this region, demonstrated an exponential decline in the average community DNA size with a half-life of ≈1.1 million years, thereby constraining the geological preservation of microbes in icy environments and the possible exchange of genetic material to the oceans. [ABSTRACT FROM AUTHOR]