Carbon Availability Modifies Temperature Responses of Heterotrophic Microbial Respiration, Carbon Uptake Affinity, and Stable Carbon Isotope Discrimination

Abstract

Microbial transformations of organic carbon (OC) generate a large flux of CO2 into the atmosphere and influence the C balance of terrestrial and aquatic ecosystems. Yet, inherent heterogeneity in natural environments precludes direct quantification of multiple microbial C fluxes that underlie CO2 production. Here we used a continuous flow bioreactor coupled with a stable C isotope analyzer to determine the effects of temperature and C availability (cellobiose concentration) on C fluxes and 13C discrimination of a microbial population growing at steady-state in a homogeneous, well-mixed environment. We estimated C uptake affinity and C use efficiency (CUE) to characterize the physiological responses of microbes to changing environmental conditions. Temperature increased biomass-C specific respiration rate and C uptake affinity at lower C availability, but did not influence those parameters at higher C availability. CUE decreased non-linearly with increasing temperature. The non-linear, negative relationship between CUE and temperature was more pronounced under lower C availability than under relatively high C availability. We observed stable isotope fractionation between C substrate and microbial biomass C (7~12‰ depletion), and between microbial biomass and respired CO2 (4~10‰ depletion). Microbial discrimination against 13C-containing cellobiose during C uptake was influenced by temperature and C availability, while discrimination during respiration was only influenced by C availability. Shifts in C uptake affinity with temperature and C availability may have modified uptake-induced 13C fractionation. By stressing the importance of C availability on temperature responses of microbial C fluxes, C uptake affinity, CUE, and isotopic fractionation, this study contributes to a fundamental understanding of C flow through microbes. This will help guide parameterization of microbial responses to varying temperature and C availability within Earth-system models.

Temperature sensitivity of biomass‐specific microbial exo‐enzyme activities and CO2 efflux is resistant to change across short‐ and long‐term timescales

“…In this study, changes in incubation temperature from 5 to 25°C enhanced exo-enzyme activities and respiration rates by ~300% and ~176%, respectively, while biomass decreased only by ~35%. These results suggest field-relevant congruency with controlled, single population laboratory studies demonstrating that respiratory costs of a common soil bacterium increase more so than growth with warming Min et al, 2016). Future studies investigating the physiological mechanisms driving changes in microbial biomass and exo-enzyme production as temperature varies seem necessary for developing a predictive understanding of microbial C cycling in varying environmental conditions.…”

“…Fully addressing the mechanisms governing microbial community dynamics is beyond the scope of this work, but microbial growth strategies (e.g., carbon use efficiency (CUE) and growth rate) may provide useful insight for envisioning microbial community shifts (Roller & Schmidt, 2015). Microbial CUE often is defined as the ratio of growth to the sum of growth and respiration, and often decreases with increasing temperature Min et al, 2016;Schindlbacher et al, 2015).…”

Can Antarctic lichens acclimatize to changes in temperature?

“…Reich, Tjoelker, Machado, & Oleksyn, 2006), their mycorrhizal symbionts (Heinemeyer, Ineson, Ostle, & Fitter, 2006) and free-living ectomycorrhizal fungi grown in agar (Malcolm, L opez-Guti errez, Koide, & Eissenstat, 2008). For heterotrophic soil microbes, the topic is controversial (Carey et al, 2016;Crowther & Bradford, 2013;Min, Lehmeier, Ballantyne, & Billings, 2016).…”

Model formulation of microbial CO2 production and efficiency can significantly influence short and long term soil C projections

“…In contrast, the MSR formulation portrays microbial efficiency as a function of both MSR and substrate availability, i.e., a dynamic aggregate resulting from the interaction between microbial physiology and environmental conditions. Consequently, variation and covariation in MSR and in substrate availability, which has been recently demonstrated in controlled experimental conditions [15], can independently influence efficiency in the MSR formulation. The two formulations of respiratory losses can be seen as opposite ends of a continuum, with all respiratory losses proportional to uptake for a pure CUE formulation and proportional to microbial biomass C for a pure MSR formulation.…”

“…Such differences will be independent of substrate particulars such as quality or recalcitrance because our focus is on the fate of C fate after it is taken up. For the comparison of interest here, we do not need to address varying propensities of acquisition for [15,17] different substrates. Differences in SOC composition will certainly influences rates of acquisition and microbial growth rate, but because our focus is on how C that is already liberated is lost as CO 2 , SOC chemistry will not influence the dynamical consequences of different mathematical formulations of microbial respiration.…”