Active communities and growth of soil microorganisms are framed by mean annual precipitation in three California annual grasslands

Abstract

Earth system models project altered precipitation regimes across much of the globe; in California, the winter wet season is predicted to extend into spring, and the summer dry period to lengthen. How these precipitation trends will affect microbial traits and soil carbon (C) cycling is a key knowledge gap. Specifically, we do not have a mechanistic understanding of the linkages between soil moisture legacy effects, microbial population dynamics and soil C persistence. Using quantitative stable isotope probing (qSIP), we compared total and growing soil microbial communities across three California annual grasslands that span a rainfall gradient yet developed on similar parent material. We also assessed multiple edaphic variables, including the radiocarbon (14C) age of soil C, and found soil C turnover time increased with annual precipitation, but that soil microbes respired recently-fixed C regardless of site rainfall history. Samples were assayed in the wet season, when we expected environmental conditions would be most similar across sites. We hypothesized that growing communities would be more compositionally similar across the gradient than the total background microbiome. We also predicted that the long-term legacy effect of soil water limitation would be reflected in a lower community growth capacity at the driest site. We found that the proportion of the total community that was detected as growing was 28%, 48% and 58% at the wet, intermediate and dry sites, respectively. The composition of growing communities strongly resembled that of total communities, and growing communities were no more similar across the gradient than total communities, indicating a strong effect of climate of the structure of growing microbial communities. Members of three phyla, Acidobacteria, Actinobacteria, and Proteobacteria, were responsible for [~]79% of the cumulative 18O assimilation and 80% of all taxa that we defined as growers. Bacterial growth rates were low at the driest site relative to the intermediate and wettest sites. Reduced growth at the driest site was observed across major phyla, including the Actinobacteria, Acidobacteria, Bacteroidetes, Gemmatimonadetes and Proteobacteria. Microbial communities at the driest site displayed phylogenetic clustering, suggesting that climate history impacts microbial growth through environmental filtering for slow growing taxa. Taxonomic identity was a strong predictor of growth, such that the growth rates of a taxon at one site predicted its growth rates at the others. This cross-site coherence in growth is likely a consequence of genetically determined physiological traits, and is consistent with the idea that evolutionary history influences growth rate.