The effect of temperature and substrate quality on the carbon use efficiency of saprotrophic decomposition

Öquist, Mats; Erhagen, Björn; Haei, Mahsa; Sparrman, Tobias; Ilstedt, Ulrik; Schleucher, Jürgen; Nilsson, Mats

doi:10.1007/s11104-016-3104-x

Cited by 47 publications

(24 citation statements)

References 47 publications

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“…In ecosystem and Earth System models, CUE is typically parameterized either to be unaffected by warming or to exhibit a homogeneous community-level decrease (1)(2)(3). In response to short-term increases in temperature, community-level CUE can increase (4,5), decrease (4,6), or remain unaffected (4,(6)(7)(8), with no clear explanation as to why these temperature responses differ (9). Organism-level CUE decreases in response to increasing temperature when respiration increases more than growth; this accelerated respiration can be caused by increased protein turnover (10), changes in membrane fluidity (11), or the loss of energy-conserving sites in the electron transport chain (12).…”

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confidence: 99%

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Pold

Domeignoz‐Horta

Morrison

et al. 2020

mBio

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The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought. IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.

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confidence: 99%

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Pold

Domeignoz‐Horta

Morrison

et al. 2020

mBio

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“…Vance and Chapin 2001;Ekblad and Nordgren 2002). Changes in soil temperature and moisture may exacerbate this C limitation, further modifying the metabolic conditions of saprotrophs (Ågren and Wetterstedt 2007;Öquist et al 2016). The pattern of microbial SOM utilization observed in this study mirrors that of microbial basal respiration and suggests that access to SOM changes with temperature, becoming more thermodynamically constrained at lower temperatures.…”

Section: Discussionmentioning

confidence: 52%

“…3) is intriguing. This indicates that some organic chemical compounds only decompose at higher incubation temperatures, presumably because the temperature affects substrate availability and thus the metabolic conditions of saprotrophs (Ågren and Wetterstedt 2007;Öquist et al 2016).…”

Section: Discussionmentioning

confidence: 99%

“…However, in practice it is difficult to determine exactly how the decomposition of SOM depends on the temperature. This is largely due to the multitude of processes involved and the fact that the overall response depends on a wide range of environmental factors aside from the temperature, as well as substrate availability (Davidson and Janssens 2006;Ågren and Wetterstedt 2007;Öquist et al 2009, 2016. It has been suggested that the organochemical composition of the SOM controls microbial access to the substrate and must therefore be accounted for when attempting to understand the temperature response of SOM decomposition (Conant et al 2011;Erhagen et al 2015).…”

Section: Introductionmentioning

confidence: 99%

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Boreal tree species affect soil organic matter composition and saprotrophic mineralization rates

et al. 2019

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Aims To investigate how different tree species affect the composition of SOM and its mineralization in boreal forest ecosystems. Methods We used pyrolysis GC-MS for molecularlevel characterization of the SOM formed under five common boreal tree species at a replicated field exper-iment~50years after plantation. We incubated soil samples at 4, 9, 14 and 19°C and measured inherent CO 2 production and substrate-induced respiration. We then evaluated if the saprotrophic microbial activity and its temperature sensitivity was controlled by the SOM composition.Results The molecular composition of the SOM emerged as key factor influencing SOM properties in plots with different tree species. Most of the variance in the SOM content was explained by the organo-chemical composition of the SOM. More importantly, the fraction of the microbial community able to utilize the native SOM was largely controlled by the SOM organochemical composition. Temperature sensitivity of CO 2 production (Q 10 ) was not explained by SOM composition. However, the microbial access to different SOM pools varied with temperature. Conclusions These results bridge the gap between the paradigms of short-term litter and long-term SOM decomposition showing that, on an intermediate timescale (~50 years), boreal tree species affect SOM molecular composition and saprotrophic mineralization rates.

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“…The reduced quantity of available SOC in our experiment likely also reduced CUE because under low substrate levels, a greater fraction of the available SOC is needed for cellular maintenance (Öquist et al. ). Although CUE may be unresponsive to the concentration of an added substrate (Roberts et al.…”

Section: Discussionmentioning

confidence: 84%

Carbon control on terrestrial ecosystem function across contrasting site productivities: the carbon connection revisited

Dove

Stark

Newman

et al. 2019

Ecology

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Understanding how altered soil organic carbon (SOC) availability affects microbial communities and their function is imperative in predicting impacts of global change on soil carbon (C) storage and ecosystem function. However, the response of soil microbial communities and their function to depleted C availability in situ is unclear. We evaluated the role of soil C inputs in controlling microbial biomass, community composition, physiology, and function by (1) experimentally excluding plant C inputs in situ for 9 yr in four temperate forest ecosystems along a productivity gradient in Oregon, USA; and (2) integrating these findings with published data from similar C‐exclusion studies into a global meta‐analysis. Excluding plant C inputs for 9 yr resulted in a 13% decrease in SOC across the four Oregon sites and an overall shift in the microbial community composition, with a 45% decrease in the fungal : bacterial ratio and a 13% increase in Gram‐positive : Gram‐negative bacterial ratio. Although gross N mineralization decreased under C exclusion, decreases in gross N immobilization were greater, resulting in increased net N mineralization rates in all but the lowest‐productivity site. Microbial biomass showed a variable response to C exclusion that was method dependent; however, we detected a 29% decrease in C‐use efficiency across the sites, with greater declines occurring in less‐productive sites. Although extracellular enzyme activity increased with C exclusion, C exclusion resulted in a 31% decrease in microbial respiration across all sites. Our meta‐analyses of published data with similar C‐exclusion treatments were largely consistent with our experimental results, showing decreased SOC, fungal : bacterial ratios, and microbial respiration, and increased Gram‐positive : Gram‐negative bacterial ratio following exclusion of C inputs to soil. Effect sizes of SOC and respiration correlated negatively with the duration of C exclusion; however, there were immediate effects of C exclusion on microbial community composition and biomass that were unaltered by duration of treatment. Our field‐based experimental results and analyses demonstrate unequivocally the dominant control of C availability on soil microbial biomass, community composition, and function, and provide additional insight into the mechanisms for these effects in forest ecosystems.

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The effect of temperature and substrate quality on the carbon use efficiency of saprotrophic decomposition

Cited by 47 publications

References 47 publications

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Boreal tree species affect soil organic matter composition and saprotrophic mineralization rates

Carbon control on terrestrial ecosystem function across contrasting site productivities: the carbon connection revisited

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