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1. Thermal adaptation of soil microbial growth traits in response to chronic warming

   https://doi.org/10.1128/aem.00825-23  

   Eng, Ashley Y. ; Narayanan, Achala ; Alster, Charlotte J. ; DeAngelis, Kristen M. ( November 2023 , Applied and Environmental Microbiology)

   Spear, John R. (Ed.)

   Adaptation of soil microbes due to warming from climate change has been observed, but it remains unknown what microbial growth traits are adaptive to warming. We studied bacterial isolates from the Harvard Forest Long-Term Ecological Research site, where field soils have been experimentally heated to 5°C above ambient temperature with unheated controls for 30 years. We hypothesized that Alphaproteobacteria from warmed plots have (i) less temperature-sensitive growth rates; (ii) higher optimum growth temperatures; and (iii) higher maximum growth temperatures compared to isolates from control plots. We made high-throughput measurements of bacterial growth in liquid cultures over time and across temperatures from 22°C to 37°C in 2–3°C increments. We estimated growth rates by fitting Gompertz models to the growth data. Temperature sensitivity of growth rate, optimum growth temperature, and maximum growth temperature were estimated by the Ratkowsky 1983 model and a modified Macromolecular Rate Theory (MMRT) model. To determine evidence of adaptation, we ran phylogenetic generalized least squares tests on isolates from warmed and control soils. Our results showed evidence of adaptation of higher optimum growth temperature of bacterial isolates from heated soils. However, we observed no evidence of adaptation of temperature sensitivity of growth and maximum growth temperature. Our project begins to capture the shape of the temperature response curves, but illustrates that the relationship between growth and temperature is complex and cannot be limited to a single point in the biokinetic range.

   Soils are the largest terrestrial carbon sink and the foundation of our food, fiber, and fuel systems. Healthy soils are carbon sinks, storing more carbon than they release. This reduces the amount of carbon dioxide released into the atmosphere and buffers against climate change. Soil microbes drive biogeochemical cycling and contribute to soil health through organic matter breakdown, plant growth promotion, and nutrient distribution. In this study, we determined how soil microbial growth traits respond to long-term soil warming. We found that bacterial isolates from warmed plots showed evidence of adaptation of optimum growth temperature. This suggests that increased microbial biomass and growth in a warming world could result in greater carbon storage. As temperatures increase, greater microbial activity may help reduce the soil carbon feedback loop. Our results provide insight on how atmospheric carbon cycling and soil health may respond in a warming world.

    

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2. The Transcriptional Response of Soil Bacteria to Long-Term Warming and Short-Term Seasonal Fluctuations in a Terrestrial Forest

   https://doi.org/10.3389/fmicb.2021.666558  

   Roy Chowdhury, Priyanka ; Golas, Stefan M. ; Alteio, Lauren V. ; Stevens, Joshua T. ; Billings, Andrew F. ; Blanchard, Jeffrey L. ; Melillo, Jerry M. ; DeAngelis, Kristen M. ( August 2021 , Frontiers in Microbiology)

   Terrestrial ecosystems are an important carbon store, and this carbon is vulnerable to microbial degradation with climate warming. After 30 years of experimental warming, carbon stocks in a temperate mixed deciduous forest were observed to be reduced by 30% in the heated plots relative to the controls. In addition, soil respiration was seasonal, as was the warming treatment effect. We therefore hypothesized that long-term warming will have higher expressions of genes related to carbohydrate and lipid metabolism due to increased utilization of recalcitrant carbon pools compared to controls. Because of the seasonal effect of soil respiration and the warming treatment, we further hypothesized that these patterns will be seasonal. We used RNA sequencing to show how the microbial community responds to long-term warming (~30 years) in Harvard Forest, MA. Total RNA was extracted from mineral and organic soil types from two treatment plots (+5°C heated and ambient control), at two time points (June and October) and sequenced using Illumina NextSeq technology. Treatment had a larger effect size on KEGG annotated transcripts than on CAZymes, while soil types more strongly affected CAZymes than KEGG annotated transcripts, though effect sizes overall were small. Although, warming showed a small effect on overall CAZymes expression, several carbohydrate-associated enzymes showed increased expression in heated soils (~68% of all differentially expressed transcripts). Further, exploratory analysis using an unconstrained method showed increased abundances of enzymes related to polysaccharide and lipid metabolism and decomposition in heated soils. Compared to long-term warming, we detected a relatively small effect of seasonal variation on community gene expression. Together, these results indicate that the higher carbohydrate degrading potential of bacteria in heated plots can possibly accelerate a self-reinforcing carbon cycle-temperature feedback in a warming climate. 

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3. Temperature sensitivity of biomass‐specific microbial exo‐enzyme activities and CO 2 efflux is resistant to change across short‐ and long‐term timescales

   https://doi.org/10.1111/gcb.14605  

   Min, Kyungjin ; Buckeridge, Kate ; Ziegler, Susan E. ; Edwards, Kate A. ; Bagchi, Samik ; Billings, Sharon A. ( March 2019 , Global Change Biology)

   Accurate representation of temperature sensitivity (Q₁₀) of soil microbial activity across time is critical for projecting soil CO₂efflux. As microorganisms mediate soil carbon (C) loss via exo‐enzyme activity and respiration, we explore temperature sensitivities of microbial exo‐enzyme activity and respiratory CO₂loss across time and assess mechanisms associated with these potential changes in microbial temperature responses. We collected soils along a latitudinal boreal forest transect with different temperature regimes (long‐term timescale) and exposed these soils to laboratory temperature manipulations at 5, 15, and 25°C for 84 days (short‐term timescale). We quantified temperature sensitivity of microbial activity per g soil and per g microbial biomass at days 9, 34, 55, and 84, and determined bacterial and fungal community structure before the incubation and at days 9 and 84. All biomass‐specific rates exhibited temperature sensitivities resistant to change across short‐ and long‐term timescales (meanQ₁₀ = 2.77 ± 0.25, 2.63 ± 0.26, 1.78 ± 0.26, 2.27 ± 0.25, 3.28 ± 0.44, 2.89 ± 0.55 for β‐glucosidase,N‐acetyl‐β‐d‐glucosaminidase, leucine amino peptidase, acid phosphatase, cellobiohydrolase, and CO₂efflux, respectively). In contrast, temperature sensitivity of soil mass‐specific rates exhibited either resilience (theQ₁₀value changed and returned to the original value over time) or resistance to change. Regardless of the microbial flux responses, bacterial and fungal community structure was susceptible to change with temperature, significantly differing with short‐ and long‐term exposure to different temperature regimes. Our results highlight that temperature responses of microbial resource allocation to exo‐enzyme production and associated respiratory CO₂loss per unit biomass can remain invariant across time, and thus, that vulnerability of soil organic C stocks to rising temperatures may persist in the long term. Furthermore, resistant temperature sensitivities of biomass‐specific rates in spite of different community structures imply decoupling of community constituents and the temperature responses of soil microbial activities.

    

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4. Temperature sensitivities of extracellular enzyme V max and K m across thermal environments

   https://doi.org/10.1111/gcb.14045  

   Allison, Steven D. ; Romero‐Olivares, Adriana L. ; Lu, Ying ; Taylor, John W. ; Treseder, Kathleen K. ( February 2018 , Global Change Biology)

   The magnitude and direction of carbon cycle feedbacks under climate warming remain uncertain due to insufficient knowledge about the temperature sensitivities of soil microbial processes. Enzymatic rates could increase at higher temperatures, but this response could change over time if soil microbes adapt to warming. We used the Arrhenius relationship, biochemical transition state theory, and thermal physiology theory to predict the responses of extracellular enzymeV_maxandK_mto temperature. Based on these concepts, we hypothesized thatV_maxandK_mwould correlate positively with each other and show positive temperature sensitivities. For enzymes from warmer environments, we expected to find lowerV_max,K_m, andK_mtemperature sensitivity but higherV_maxtemperature sensitivity. We tested these hypotheses with isolates of the filamentous fungusNeurospora discretacollected from around the globe and with decomposing leaf litter from a warming experiment in Alaskan boreal forest. ForNeurosporaextracellular enzymes,V_maxQ₁₀ranged from 1.48 to 2.25, andK_mQ₁₀ranged from 0.71 to 2.80. In agreement with theory,V_maxandK_mwere positively correlated for some enzymes, andV_maxdeclined under experimental warming in Alaskan litter. However, the temperature sensitivities ofV_maxandK_mdid not vary as expected with warming. We also found no relationship between temperature sensitivity ofV_maxorK_mand mean annual temperature of the isolation site forNeurosporastrains. DecliningV_maxin the Alaskan warming treatment implies a short‐term negative feedback to climate change, but theNeurosporaresults suggest that climate‐driven changes in plant inputs and soil properties are important controls on enzyme kinetics in the long term. Our empirical data on enzymeV_max,K_m, and temperature sensitivities should be useful for parameterizing existing biogeochemical models, but they reveal a need to develop new theory on thermal adaptation mechanisms.

    

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5. Multi-year incubation experiments boost confidence in model projections of long-term soil carbon dynamics

   https://doi.org/10.1038/s41467-020-19428-y  

   Jian, Siyang ; Li, Jianwei ; Wang, Gangsheng ; Kluber, Laurel A. ; Schadt, Christopher W. ; Liang, Junyi ; Mayes, Melanie A. ( November 2020 , Nature Communications)

   Global soil organic carbon (SOC) stocks may decline with a warmer climate. However, model projections of changes in SOC due to climate warming depend on microbially-driven processes that are usually parameterized based on laboratory incubations. To assess how lab-scale incubation datasets inform model projections over decades, we optimized five microbially-relevant parameters in the Microbial-ENzyme Decomposition (MEND) model using 16 short-term glucose (6-day), 16 short-term cellulose (30-day) and 16 long-term cellulose (729-day) incubation datasets with soils from forests and grasslands across contrasting soil types. Our analysis identified consistently higher parameter estimates given the short-term versus long-term datasets. Implementing the short-term and long-term parameters, respectively, resulted in SOC loss (–8.2 ± 5.1% or –3.9 ± 2.8%), and minor SOC gain (1.8 ± 1.0%) in response to 5 °C warming, while only the latter is consistent with a meta-analysis of 149 field warming observations (1.6 ± 4.0%). Comparing multiple subsets of cellulose incubations (i.e., 6, 30, 90, 180, 360, 480 and 729-day) revealed comparable projections to the observed long-term SOC changes under warming only on 480- and 729-day. Integrating multi-year datasets of soil incubations (e.g., > 1.5 years) with microbial models can thus achieve more reasonable parameterization of key microbial processes and subsequently boost the accuracy and confidence of long-term SOC projections.

    

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