Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter

Microbial carbon use efficiency (CUE) is a critical regulator of soil organic matter dynamics and terrestrial carbon fluxes, with strong implications for soil biogeochemistry models. While ecologists increasingly appreciate the importance of CUE, its core concepts remain ambiguous: terminology is inconsistent and confusing, methods capture variable temporal and spatial scales, and the significance of many fundamental drivers remains inconclusive. Here we outline the processes underlying microbial efficiency and propose a conceptual framework that structures the definition of CUE according to increasingly broad temporal and spatial drivers where (1) CUEP reflects population-scale carbon use efficiency of microbes governed by species-specific metabolic and thermodynamic constraints, (2) CUEC defines community-scale microbial efficiency as gross biomass production per unit substrate taken up over short time scales, largely excluding recycling of microbial necromass and exudates, and (3) CUEE reflects the ecosystem-scale efficiency of net microbial biomass production (growth) per unit substrate taken up as iterative breakdown and recycling of microbial products occurs. CUEE integrates all internal and extracellular constraints on CUE and hence embodies an ecosystem perspective that fully captures all drivers of microbial biomass synthesis and decay. These three definitions are distinct yet complementary, capturing the capacity for carbon storage in microbial biomass across different ecological scales. By unifying the existing concepts and terminology underlying microbial efficiency, our framework enhances data interpretation and theoretical advances

The temperature response of soil microbial efficiency and its feedback to climate

Soils are the largest repository of organic carbon (C) in the terrestrial biosphere and represent an important source of carbon dioxide (CO2) to the atmosphere, releasing 60–75 Pg C annually through microbial decomposition of organic materials1,2. A primary control on soil CO2 flux is the efficiency with which the microbial community uses C. Despite its critical importance to soil–atmosphere CO2 exchange, relatively few studies have examined the factors controlling soil microbial efficiency. Here, we measured the temperature response of microbial efficiency in soils amended with substrates varying in lability. We also examined the temperature sensitivity of microbial efficiency in response to chronic soil warming in situ. We find that the efficiency with which soil microorganisms use organic matter is dependent on both temperature and substrate quality, with efficiency declining with increasing temperatures for more recalcitrant substrates. However, the utilization efficiency of a more recalcitrant substrate increased at higher temperatures in soils exposed to almost two decades of warming 5 °C above ambient. Our work suggests that climate warming could alter the decay dynamics of more stable organic matter compounds, thereby having a positive feedback to climate that is attenuated by a shift towards a more efficient microbial community in the longer term

Estimating Annual Soil Carbon Loss in Agricultural Peatland Soils Using a Nitrogen Budget Approach

Around the world, peatland degradation and soil subsidence is occurring where these soils have been converted to agriculture. Since initial drainage in the mid-1800s, continuous farming of such soils in the California Sacramento-San Joaquin Delta (the Delta) has led to subsidence of up to 8 meters in places, primarily due to soil organic matter (SOM) oxidation and physical compaction. Rice (Oryza sativa) production has been proposed as an alternative cropping system to limit SOM oxidation. Preliminary research on these soils revealed high N uptake by rice in N fertilizer omission plots, which we hypothesized was the result of SOM oxidation releasing N. Testing this hypothesis, we developed a novel N budgeting approach to assess annual soil C and N loss based on plant N uptake and fallow season N mineralization. Through field experiments examining N dynamics during growing season and winter fallow periods, a complete annual N budget was developed. Soil C loss was calculated from SOM-N mineralization using the soil C:N ratio. Surface water and crop residue were negligible in the total N uptake budget (3 - 4 % combined). Shallow groundwater contributed 24 - 33 %, likely representing subsurface SOM-N mineralization. Assuming 6 and 25 kg N ha-1 from atmospheric deposition and biological N2 fixation, respectively, our results suggest 77 - 81 % of plant N uptake (129 - 149 kg N ha-1) was supplied by SOM mineralization. Considering a range of N uptake efficiency from 50 - 70 %, estimated net C loss ranged from 1149 - 2473 kg C ha-1. These findings suggest that rice systems, as currently managed, reduce the rate of C loss from organic delta soils relative to other agricultural practices