Marschmann, G. L. | Search bioRxiv

bioRxiv2022

Life history strategies and niches of soil bacteria emerge from interacting thermodynamic, biophysical, and metabolic traits

Efficient biochemical transformation of belowground carbon by microorganisms plays a critical role in determining the long-term fate of soil carbon. As plants assimilate carbon from the atmosphere, up to 50% is exuded into the area surrounding growing roots, where it may be transformed into microbial biomass and subsequently stabilized through mineral associations. However, due to a hierarchy of interacting microbial traits, it remains elusive how emergent life-history strategies of microorganisms influence the processing of root exudate carbon. Here, by combining theory-based predictions of substrate uptake kinetics for soil bacteria and a new genome-informed trait-based dynamic energy budget model, we predicted life history traits and trade-offs of a broad range of soil bacteria growing on 82 root exudate metabolites. The model captured resource-dependent trade-offs between growth rate (power) and growth efficiency (yield) that are fundamental to microbial fitness in communities. During early phases of plant development, growth rates of bacteria were largely constrained by maximum growth potential, highlighting the predictive power of genomic traits during nutrient-replete soil conditions. In contrast, selection for efficiency was important later in the plant growing season, where the model successfully predicted microbial substrate preferences for aromatic organic acids and plant hormones. The predicted carbon-use efficiencies for growth on organics acids were much higher than typical values observed in soil. These predictions provide mechanistic underpinning for the apparent efficiency of the microbial route to mineral stabilization in the rhizosphere and add an additional layer of complexity to rhizosphere microbial community assembly.

ecology↗

bioRxiv2021

Kinetic Properties of Microbial Exoenzymes Vary with Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile

Current knowledge of the mechanisms and responses of soil organic matter (SOM) turnover to warming is mainly limited to surface soils, although over 50% of global soil carbon is contained in subsoils. Deep soils have different physicochemical properties, nutrient inputs and microbiomes, which may harbor distinct functional traits and lead to different SOM dynamics and temperature responses. We hypothesized that kinetic and thermal properties of microbial exoenzymes, which mediate SOM depolymerization, vary with soil depth, reflecting microbial adaptation to distinct substrate and temperature regimes. We determined the Michaelis-Menten (MM) kinetics of three ubiquitous enzymes involved in carbon (C), nitrogen (N) and phosphorus (P) acquisition at six soil depths down to 90 cm at a temperate coniferous forest, and their temperature sensitivity based on Arrhenius and Macromolecular Rate Theory (MMRT) models over six temperatures between 4-50{degrees}C. Maximal enzyme velocity (Vmax) decreased strongly with depth for all enzymes, both on a dry soil mass and a microbial biomass C basis, whereas their affinities increased, indicating adaptation to lower substrate availability. Surprisingly, microbial biomass-specific catalytic efficiencies also decreased with depth, except for the P-acquiring enzyme, indicating distinct nutrient demands at depth relative to microbial abundance. These results indicated that deep soil microbiomes encode enzymes with intrinsically lower turnover and/or produce less enzymes per cell, likely reflecting distinct life strategies. The relative kinetics between different enzymes also varied with depth, suggesting an increase in relative P demand with depth, or that phosphatases may be involved in C acquisition. Warming consistently led to increased Vmax and catalytic efficiency of all enzymes, and thus to overall higher SOM-decomposition potential, but enzyme temperature sensitivity was similar through the soil profile based on both Arrhenius/Q10 and MMRT models. Nevertheless, temperature directly affected the kinetic properties of different enzyme types in a depth-dependent manner, and thus the relative depolymerization potential of different compounds. Our results indicate that kinetic and thermal properties of exoenzymes are intrinsic traits of soil microbiomes adapted to distinct physicochemical conditions associated with different soil depths, and improve our conceptual understanding of critical mechanisms underlying SOM dynamics and responses to warming through the soil profile.

microbiology↗