28Soil microbial biomass can reach its annual maximum pool size beneath the winter 29 snowpack and is known to decline abruptly following snowmelt in seasonally snow-covered 30 ecosystems. Observed differences in winter versus summer microbial taxonomic composition 31 also suggests that phylogenetically conserved traits may permit winter-versus summer-adapted 32 microorganisms to occupy distinct niches. In this study, we sought to identify archaea, bacteria, 33 and fungi that are associated with the soil microbial bloom overwinter and the subsequent 34 biomass collapse following snowmelt at a high-altitude watershed in central Colorado, USA. 35 Archaea, bacteria, and fungi were categorized into three life strategies (Winter-Adapted, 36 Snowmelt-Specialist, Spring-Adapted) based on changes in abundance during winter, the 37 snowmelt period, and after snowmelt in spring. We calculated indices of phylogenetic 38 relatedness (archaea and bacteria) or assigned functional attributes (fungi) to organisms within 39 life strategies to infer whether phylogenetically conserved traits differentiate Winter-Adapted, 40 Snowmelt-Specialist, and Spring-Adapted groups. We observed that the soil microbial bloom 41 was correlated in time with a pulse of snowmelt infiltration, which commenced 65 days prior to 42 soils becoming snow-free. A pulse of nitrogen (N, as nitrate) occurred after snowmelt, along 43 with a collapse in the microbial biomass pool size, and an increased abundance of nitrifying 44 archaea and bacteria (e.g., Thaumarchaeota, Nitrospirae). Winter-and Spring-Adapted archaea 45 and bacteria were phylogenetically clustered, suggesting that phylogenetically conserved traits 46 allow Winter-and Spring-Adapted archaea and bacteria to occupy distinct niches. In contrast, 47Snowmelt-Specialist archaea and bacteria were phylogenetically overdispersed, suggesting that 48 the key mechanism(s) of the microbial biomass crash are likely to be density-dependent (e.g.,
49trophic interactions, competitive exclusion) and affect organisms across a broad phylogenetic 50 3 spectrum. Saprotrophic fungi were the dominant functional group across fungal life strategies, 51 however, ectomycorrhizal fungi experienced a large increase in abundance in spring. If well-52 coupled plant-mycorrhizal phenology currently buffers ecosystem N losses in spring, then 53 changes in snowmelt timing may alter ecosystem N retention potential. Overall, we observed that 54 the snowmelt separates three distinct soil niches that are occupied by ecologically distinct groups 55 of microorganisms. This ecological differentiation is of biogeochemical importance, particularly 56 with respect to the mobilization of nitrogen during winter, before and after snowmelt. 57 58 59