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Although microbial communities from many glacial environments have been analyzed, microbes living in the debris atop debris-covered glaciers represent an understudied frontier in the cryosphere. The few previous molecular studies of microbes in supraglacial debris have either had limited phylogenetic resolution, limited spatial resolution (e.g. only one sample site on the glacier) or both. Here, we present the microbiome of a debris-covered glacier across all three domains of life, using a spatially-explicit sampling scheme to characterize the Middle Fork Toklat Glacier's microbiome from its terminus to sites high on the glacier. Our results show that microbial communities differ across the supraglacial transect, but surprisingly these communities are strongly spatially autocorrelated, suggesting the presence of a supraglacial chronosequence. This pattern is dominated by phototrophic microbes (both bacteria and eukaryotes) which are less abundant near the terminus and more abundant higher on the glacier. We use these data to refute the hypothesis that the inhabitants of the glacier are randomly deposited atmospheric microbes, and to provide evidence that succession from a predominantly photosynthetic to a more heterotrophic community is occurring on the glacier.