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Global warming, in combination with altered precipitation patterns, is accelerating global soil respiration, which could in turn accelerate climate change. The biological mechanisms through which soil carbon (C) responds to climate are not well understood, limiting our ability to predict future global soil respiration rates. As part of a climate manipulation experiment, we tested whether differences in soil heterotrophic respiration (R-H) driven by season or climate treatment are linked to (1) relative abundances of microbes in active and dormant metabolic states, (2) net changes in microbial biomass and/or (3) changes in the relative abundances of microbial groups with different C-use strategies. We used a flow-cytometric single-cell metabolic assay to quantify the abundance of active and dormant microbes, and the phospholipid fatty acid method to determine microbial biomass and ratios of fungi:bacteria and Gram-positive:Gram-negative bacteria. R-H did not respond to climate treatments but was greater in the warm and dry summer than in the cool and less-dry fall. These dynamics were better explained when microbial data were taken into account compared to when only physical data (temperature and moisture) were used. Overall, our results suggest that R-H responses to temperature are stronger when soil contains more active microbes, and that seasonal patterns of R-H can be better explained by shifts in microbial activity than by shifts in the relative abundances of fungi and Gram-positive and Gram-negative bacteria. These findings contribute to our understanding of how and under which conditions microbes influence soil C responses to climate.