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.
Highlights
Heterotrophic microorganisms break down organic carbon (OC) into assimilable molecules, which are subsequently incorporated into biomass or returned to the environment as exudates or respired CO2
Lehmeier et al (2016) used a coupled chemostat and C isotope analyzer to improve our understanding of C flows from substrate through microbial biomass and into respired CO2, which is of great interest at multiple scales and levels of organization, from microbes to ecosystems (Blair et al, 1985; Hagström et al, 1988; Henn and Chapela, 2000; Šantrucková et al, 2000; Henn et al, 2002; Werth and Kuzyakov, 2010; Brüggemann et al, 2011; Dijkstra et al, 2011a,b; Penger et al, 2014)
Because our estimates of biomass-C specific uptake were computed by summing biomass-C specific rates of growth and respiration, and biomass-C specific growth rate was relatively constant across all chemostat runs (Figure 1A), temperature responses of biomass-C specific uptake rates were similar to those of biomass-C specific respiration at each C availability (Figure 1C)
Summary
Heterotrophic microorganisms break down organic carbon (OC) into assimilable molecules, which are subsequently incorporated into biomass or returned to the environment as exudates or respired CO2. Because of the important role they play in regulating OC in terrestrial and aquatic systems and atmospheric CO2, ecosystem scientists have explicitly incorporated microbial dynamics into Earth system models (Allison et al, 2010; Wieder et al, 2013; Hagerty et al, 2014; Tang and Riley, 2015). It remains unclear what values should be used for microbial parameters [e.g., C use efficiency (CUE), biomass-C specific respiration] and how these parameters change with environmental conditions (Luo et al, 2016). Quantifying the effects of temperature on biomass-C specific respiration rate, CUE, and microbial 13C discrimination for a ubiquitous microbe (Lehmeier et al, 2016) provides a mechanistic basis and justification for the often assumed temperature dependence of CUE in Earth-system models
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