Abstract
Annually, half of all plant-derived carbon is added to soil where it is microbially respired to CO2. However, understanding of the microbiology of this process is limited because most culture-independent methods cannot link metabolic processes to the organisms present, and this link to causative agents is necessary to predict the results of perturbations on the system. We collected soil samples at two sub-root depths (10–20 cm and 30–40 cm) before and after a rainfall-driven nutrient perturbation event in a Northern California grassland that experiences a Mediterranean climate. From ten samples, we reconstructed 198 metagenome-assembled genomes that represent all major phylotypes. We also quantified 6,835 proteins and 175 metabolites and showed that after the rain event the concentrations of many sugars and amino acids approach zero at the base of the soil profile. Unexpectedly, the genomes of novel members of the Gemmatimonadetes and Candidate Phylum Rokubacteria phyla encode pathways for methylotrophy. We infer that these abundant organisms contribute substantially to carbon turnover in the soil, given that methylotrophy proteins were among the most abundant proteins in the proteome. Previously undescribed Bathyarchaeota and Thermoplasmatales archaea are abundant in deeper soil horizons and are inferred to contribute appreciably to aromatic amino acid degradation. Many of the other bacteria appear to breakdown other components of plant biomass, as evidenced by the prevalence of various sugar and amino acid transporters and corresponding hydrolyzing machinery in the proteome. Overall, our work provides organism-resolved insight into the spatial distribution of bacteria and archaea whose activities combine to degrade plant-derived organics, limiting the transport of methanol, amino acids and sugars into underlying weathered rock. The new insights into the soil carbon cycle during an intense period of carbon turnover, including biogeochemical roles to previously little known soil microbes, were made possible via the combination of metagenomics, proteomics, and metabolomics.
Highlights
The terrestrial carbon reservoir is primarily distributed among grasslands (∼34%), forests (∼39%), and cultivated farms (∼17%) (White, Murray & Rohweder, 2000)
Carbon exported from the shallow soils provides nutrients for microorganisms in lower soil horizons and the deeper subsurface
We investigated the distribution of metabolites in triplicate extracted soil water samples using a robust Liquid Chromatography-based Mass Spectroscopy (LC-MS) metabolomics workflow based on a previous study on samples from the meadow soils (Swenson et al, 2015)
Summary
The terrestrial carbon reservoir is primarily distributed among grasslands (∼34%), forests (∼39%), and cultivated farms (∼17%) (White, Murray & Rohweder, 2000). While in forests the majority of fixed carbon is stored vegetation, most fixed carbon in grasslands is stored in soil. Grassland soils are one of the most important reservoirs of terrestrial carbon on the planet. This observation has motivated many studies of processes that impact the fate of carbon compounds in grassland soil systems (Blazewicz, Schwartz & Firestone, 2014; Kandeler et al, 2006; Mau et al, 2015; Reinsch et al, 2014; Schimel & Schaeffer, 2012; Verastegui et al, 2014). Carbon exported from the shallow soils provides nutrients for microorganisms in lower soil horizons and the deeper subsurface
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