skip to main content


Title: Compensatory Thermal Adaptation of Soil Microbial Respiration Rates in Global Croplands
Abstract

Understanding whether soil microbial respiration adapts to the ambient thermal climate with an enhanced or compensatory response, hence potentially stimulating or slowing down soil carbon losses with warming, is key to accurately forecast and model climate change impacts on the global carbon cycle. Despite the interest in this topic and the plethora of recent studies in natural ecosystems, it has been seldom explored in croplands. Using two recently published independent datasets of soil microbial metabolic quotient (MMQ; microbial respiration rate per unit biomass) and carbon use efficiency (CUE; partitioning of C to microbial growth vs. respiration), we find a compensatory thermal adaptive response for MMQ in global croplands. That is, mean annual temperature (MAT) has a negative effect on MMQ. However, this compensatory thermal adaptation is only half or less of that found in previous studies for noncultivated ecosystems. In contrast to the negative MMQ‐MAT pattern, microbial CUE increases with MAT across global croplands. By incorporating this positive CUE‐MAT relationship (greater C partitioning into microbial growth rather than respiration with increasing temperature) into a microbial‐explicit soil organic carbon model, we successfully predict the thermal compensation of MMQ observed in croplands. Our model‐data integration and database cross‐validation suggest that a warmer climate may select for microbial communities with higher CUE, providing a plausible mechanism for their compensatory metabolic response. By helping to identify appropriate representations of microbial physiological processes in soil biogeochemical models, our work will help build confidence in model projections of cropland C dynamics under a changing climate.

 
more » « less
NSF-PAR ID:
10455334
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
DOI PREFIX: 10.1029
Date Published:
Journal Name:
Global Biogeochemical Cycles
Volume:
34
Issue:
6
ISSN:
0886-6236
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Giovannoni, Stephen J. (Ed.)
    ABSTRACT 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. 
    more » « less
  2. Summary

    Autotrophic respiration is a major driver of the global C cycle and may contribute a positive climate warming feedback through increased atmospheric concentrations ofCO2. The extent of this feedback depends on plants' ability to acclimate respiration to maintain a constant carbon use efficiency (CUE).

    We quantified respiratory partitioning of gross primary production (GPP) andCUEof field‐grown trees in a long‐term warming experiment (+3°C). We delivered a13C–CO2pulse to whole tree crowns and chased that pulse in the respiration of leaves, whole crowns, roots, and soil. We also measured the isotopic composition of soil microbial biomass and the respiration rates of leaves and whole crowns.

    We documented homeostatic respiratory acclimation of foliar and whole‐crown respiration rates; the trees adjusted to experimental warming such that leaf‐level respiration rates were not increased. Experimental warming had no detectable impact on respiratory partitioning or mean residence times. Of the13C label acquired by the trees, aboveground respiration consumed 10%, belowground respiration consumed 40%, and the remaining 50% was retained.

    Experimental warming of +3°C did not alter respiratory partitioning at the scale of entire trees, suggesting that complete acclimation of respiration to warming is likely to dampen a positive climate warming feedback.

     
    more » « less
  3. Abstract

    Soil moisture is a major driver of microbial activity and thus, of the release of carbon (C) into the Earth's atmosphere. Yet, there is no consensus on the relationship between soil moisture and microbial respiration, and as a result, moisture response functions are a poorly constrained aspect of C models. In addition, models assume that the response of microbial respiration to moisture is the same for all ecosystems, regardless of climate history, an assumption that many empirical studies have challenged. These gaps in understanding of the microbial respiration response to moisture contribute to uncertainty in model predictions.

    We review our understanding of what drives microbial moisture response, highlighting evidence that historical precipitation can influence both responses to moisture and sensitivity to drought. We present two hypotheses, the ‘climate history hypothesis’, where we predict that baseline moisture response functions change as a function of precipitation history, and the ‘drought legacy hypothesis’, in which we suggest that the intensity and frequency of historical drought have shaped microbial communities in ways that will control moisture responses to contemporary drought. Underlying mechanisms include biological selection and filtering of the microbial community by rainfall regimes, which result in microbial traits and trade‐offs that shape function.

    We present an integrated modelling and empirical approach for understanding microbial moisture responses and improving models. Standardized measures of moisture response (respiration rate across a range of moistures) and accompanying microbial properties are needed across sites. These data can be incorporated into trait‐based models to produce generalized moisture response functions, which can then be validated and incorporated into conventional and microbially explicit ecosystem models of soil C cycling. Future studies should strive to analyse realistic moisture conditions and consider the role of environmental factors and soil structure in microbial response.

    Microbes are the engines that drive C storage and are sensitive to changes in rainfall. A greater understanding of the factors that govern this sensitivity could be a key part of improving predictions of soil C dynamics, climate change and C‐climate feedbacks.

    Read the freePlain Language Summaryfor this article on the Journal blog.

     
    more » « less
  4. Abstract

    Global soil carbon (C) stocks are expected to decline with warming, and changes in microbial processes are key to this projection. However, warming responses of critical microbial parameters such as carbon use efficiency (CUE) and biomass turnover (rB) are not well understood. Here, we determine these parameters using a probabilistic inversion approach that integrates a microbial‐enzyme model with 22 years of carbon cycling measurements at Harvard Forest. We find that increasing temperature reduces CUE but increases rB, and that two decades of soil warming increases the temperature sensitivities of CUE and rB. These temperature sensitivities, which are derived from decades‐long field observations, contrast with values obtained from short‐term laboratory experiments. We also show that long‐term soil C flux and pool changes in response to warming are more dependent on the temperature sensitivity of CUE than that of rB. Using the inversion‐derived parameters, we project that chronic soil warming at Harvard Forest over six decades will result in soil C gain of <1.0% on average (1st and 3rd quartiles: 3.0% loss and 10.5% gain) in the surface mineral horizon. Our results demonstrate that estimates of temperature sensitivity of microbial CUE and rB can be obtained and evaluated rigorously by integrating multidecadal datasets. This approach can potentially be applied in broader spatiotemporal scales to improve long‐term projections of soil C feedbacks to climate warming.

     
    more » « less
  5. Abstract

    Almost half of the global terrestrial soil carbon (C) is stored in the northern circumpolar permafrost region, where air temperatures are increasing two times faster than the global average. As climate warms, permafrost thaws and soil organic matter becomes vulnerable to greater microbial decomposition. Long‐term soil warming of ice‐rich permafrost can result in thermokarst formation that creates variability in environmental conditions. Consequently, plant and microbial proportional contributions to ecosystem respiration may change in response to long‐term soil warming. Natural abundance δ13C and Δ14C of aboveground and belowground plant material, and of young and old soil respiration were used to inform a mixing model to partition the contribution of each source to ecosystem respiration fluxes. We employed a hierarchical Bayesian approach that incorporated gross primary productivity and environmental drivers to constrain source contributions. We found that long‐term experimental permafrost warming introduced a soil hydrology component that interacted with temperature to affect old soil C respiration. Old soil C loss was suppressed in plots with warmer deep soil temperatures because they tended to be wetter. When soil volumetric water content significantly decreased in 2018 relative to 2016 and 2017, the dominant respiration sources shifted from plant aboveground and young soil respiration to old soil respiration. The proportion of ecosystem respiration from old soil C accounted for up to 39% of ecosystem respiration and represented a 30‐fold increase compared to the wet‐year average. Our findings show that thermokarst formation may act to moderate microbial decomposition of old soil C when soil is highly saturated. However, when soil moisture decreases, a higher proportion of old soil C is vulnerable to decomposition and can become a large flux to the atmosphere. As permafrost systems continue to change with climate, we must understand the thresholds that may propel these systems from a C sink to a source.

     
    more » « less