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1. Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

   https://doi.org/10.1128/mBio.02293-19  

   Pold, Grace ; Domeignoz-Horta, Luiz A. ; Morrison, Eric W. ; Frey, Serita D. ; Sistla, Seeta A. ; DeAngelis, Kristen M. ( February 2020 , mBio)

   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. 

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2. Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long‐term warming

   https://doi.org/10.1111/gcb.16544  

   Domeignoz‐Horta, Luiz A. ; Pold, Grace ; Erb, Hailey ; Sebag, David ; Verrecchia, Eric ; Northen, Trent ; Louie, Katherine ; Eloe‐Fadrosh, Emiley ; Pennacchio, Christa ; Knorr, Melissa A. ; et al ( March 2023 , Global Change Biology)

   Microbes are responsible for cycling carbon (C) through soils, and predicted changes in soil C stocks under climate change are highly sensitive to shifts in the mechanisms assumed to control the microbial physiological response to warming. Two mechanisms have been suggested to explain the long-­ term warming impact on microbial physiology: microbial thermal acclimation and changes in the quantity and quality of substrates available for microbial metabolism. Yet studies disentangling these two mechanisms are lacking. To resolve the drivers of changes in microbial physiology in response to long-­ term warming, we sampled soils from 13-­ and 28-­ year-­ old soil warming experiments in different seasons. We performed short-­ term laboratory incubations across a range of temperatures to measure the relationships between temperature sensitivity of physiology (growth, respiration, carbon use efficiency, and extracellular enzyme activity) and the chemical composition of soil organic matter. We observed apparent thermal acclimation of microbial respiration, but only in summer, when warming had exacerbated the seasonally-­ induced, already small dissolved organic matter pools. Irrespective of warming, greater quantity and quality of soil carbon increased the extracellular enzymatic pool and its temperature sensitivity. We propose that fresh litter input into the system seasonally cancels apparent thermal acclimation of C-­ cycling processes to decadal warming. Our findings reveal that long-term warming has indirectly affected microbial physiology via reduced C availability in this system, implying that earth system models including these negative feedbacks may be best suited to describe long-­ term warming effects on these soils. 

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3. Reduced carbon use efficiency and increased microbial turnover with soil warming

   https://doi.org/10.1111/gcb.14517  

   Li, Jianwei ; Wang, Gangsheng ; Mayes, Melanie A. ; Allison, Steven D. ; Frey, Serita D. ; Shi, Zheng ; Hu, Xiao‐Ming ; Luo, Yiqi ; Melillo, Jerry M. ( December 2018 , Global Change Biology)

   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.

    

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4. Climate warming and tree carbon use efficiency in a whole‐tree 13 CO 2 tracer study

   https://doi.org/10.1111/nph.15721  

   Drake, John E. ; Furze, Morgan E. ; Tjoelker, Mark G. ; Carrillo, Yolima ; Barton, Craig V. M. ; Pendall, Elise ( March 2019 , New Phytologist)

   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.

    

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5. Limiting Resources Define the Global Pattern of Soil Microbial Carbon Use Efficiency

   https://doi.org/10.1002/advs.202308176  

   Cui, Yongxing ; Hu, Junxi ; Peng, Shushi ; Delgado‐Baquerizo, Manuel ; Moorhead, Daryl L ; Sinsabaugh, Robert L ; Xu, Xiaofeng ; Geyer, Kevin M ; Fang, Linchuan ; Smith, Pete ; et al ( July 2024 , Advanced Science)

   Microbial carbon (C) use efficiency (CUE) delineates the proportion of organic C used by microorganisms for anabolism and ultimately influences the amount of C sequestered in soils. However, the key factors controlling CUE remain enigmatic, leading to considerable uncertainty in understanding soil C retention and predicting its responses to global change factors. Here, we investigate the global patterns of CUE estimate by stoichiometric modeling in surface soils of natural ecosystems, and examine its associations with temperature, precipitation, plant‐derived C and soil nutrient availability. We found that CUE is determined by the most limiting resource among these four basic environmental resources within specific climate zones (i.e., tropical, temperate, arid, and cold zones). Higher CUE is common in arid and cold zones and corresponds to limitations in temperature, water, and plant‐derived C input, while lower CUE is observed in tropical and temperate zones with widespread limitation of nutrients (e.g., nitrogen or phosphorus) in soil. The contrasting resource limitations among climate zones led to an apparent increase in CUE with increasing latitude. The resource‐specific dependence of CUE implies that soils in high latitudes with arid and cold environments may retain less organic C in the future, as warming and increased precipitation can reduce CUE. In contrast, oligotrophic soils in low latitudes may increase organic C retention, as CUE could be increased with concurrent anthropogenic nutrient inputs. The findings underscore the importance of resource limitations for CUE and suggest asymmetric responses of organic C retention in soils across latitudes to global change factors.

    

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