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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.)

   ABSTRACT 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. IMPORTANCESoils 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. Climate legacies determine grassland responses to future rainfall regimes

   https://doi.org/10.1111/gcb.16084  

   Broderick, Caitlin M.; Wilkins, Kate; Smith, Melinda D.; Blair, John M. (January 2022, Global Change Biology)

   Abstract Climate variability and periodic droughts have complex effects on carbon (C) fluxes, with uncertain implications for ecosystem C balance under a changing climate. Responses to climate change can be modulated by persistent effects of climate history on plant communities, soil microbial activity, and nutrient cycling (i.e., legacies). To assess how legacies of past precipitation regimes influence tallgrass prairie C cycling under new precipitation regimes, we modified a long‐term irrigation experiment that simulated a wetter climate for >25 years. We reversed irrigated and control (ambient precipitation) treatments in some plots and imposed an experimental drought in plots with a history of irrigation or ambient precipitation to assess how climate legacies affect aboveground net primary productivity (ANPP), soil respiration, and selected soil C pools. Legacy effects of elevated precipitation (irrigation) included higher C fluxes and altered labile soil C pools, and in some cases altered sensitivity to new climate treatments. Indeed, decades of irrigation reduced the sensitivity of both ANPP and soil respiration to drought compared with controls. Positive legacy effects of irrigation on ANPP persisted for at least 3 years following treatment reversal, were apparent in both wet and dry years, and were associated with altered plant functional composition. In contrast, legacy effects on soil respiration were comparatively short‐lived and did not manifest under natural or experimentally‐imposed “wet years,” suggesting that legacy effects on CO₂efflux are contingent on current conditions. Although total soil C remained similar across treatments, long‐term irrigation increased labile soil C and the sensitivity of microbial biomass C to drought. Importantly, the magnitude of legacy effects for all response variables varied with topography, suggesting that landscape can modulate the strength and direction of climate legacies. Our results demonstrate the role of climate history as an important determinant of terrestrial C cycling responses to future climate changes. 

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3. Long-term warming in a temperate forest accelerates soil organic matter decomposition despite increased plant-derived inputs

   https://doi.org/10.1007/s10533-024-01165-9  

   San_Román, Atzín X; Srikanthan, Nivetha; Hamid, Andreia A; Muratore, Thomas J; Knorr, Melissa A; Frey, Serita D; Simpson, Myrna J (September 2024, Biogeochemistry)

   Abstract Climate change may alter soil microbial communities and soil organic matter (SOM) composition. Soil carbon (C) cycling takes place over multiple time scales; therefore, long-term studies are essential to better understand the factors influencing C storage and help predict responses to climate change. To investigate this further, soils that were heated by 5 °C above ambient soil temperatures for 18 years were collected from the Barre Woods Soil Warming Study at the Harvard Forest Long-term Ecological Research site. This site consists of large 30 × 30 m plots (control or heated) where entire root systems are exposed to sustained warming conditions. Measurements included soil C and nitrogen concentrations, microbial biomass, and SOM chemistry using gas chromatography–mass spectrometry and solid-state¹³C nuclear magnetic resonance spectroscopy. These complementary techniques provide a holistic overview of all SOM components and a comprehensive understanding of SOM composition at the molecular-level. Our results showed that soil C concentrations were not significantly altered with warming; however, various molecular-level alterations to SOM chemistry were observed. We found evidence for both enhanced SOM decomposition and increased above-ground plant inputs with long-term warming. We also noted shifts in microbial community composition while microbial biomass remained largely unchanged. These findings suggest that prolonged warming induced increased availability of preferred substrates, leading to shifts in the microbial community and SOM biogeochemistry. The observed increase in gram-positive bacteria indicated changes in substrate availability as gram-positive bacteria are often associated with the decomposition of complex organic matter, while gram-negative bacteria preferentially break down simpler organic compounds altering SOM composition over time. Our results also highlight that additional plant inputs do not effectively offset chronic warming-induced SOM decomposition in temperate forests. 

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4. Long-term warming inverts the relationship between ecosystem function and microbial resource acquisition

   https://doi.org/10.1101/2024.10.23.619826  

   Shinfuku, Melissa S; DeAngelis, Kristen M (October 2024, bioRxiv)

   Abstract Soil microbial traits drive ecosystem functions, which can explain the positive correlation between microbial functional diversity and ecosystem function. However, microbial adaptation to climate change related warming stress can shift microbial traits with direct implications for soil carbon cycling. Here, we investigated how long-term warming affects the relationship between microbial trait diversity and ecosystem function. Soils were sampled after 24 years of +5°C warming alongside unheated control soils from the Harvard Forest Long-Term Ecological Research site. Ecosystem function was estimated from six different enzyme activities and microbial biomass. Functional diversity was calculated from metatranscriptomics sequencing, where reads were assigned to yield, acquisition, or stress trait categories. We found that in organic horizon soils, warming decreased the richness of acquisition-related traits. In the mineral soils, we observed that heated soils exhibited a negative relationship with the richness of acquisition-related traits. These results suggest that microbial communities exposed to long-term warming are shifting away from a resource acquisition life history strategy. 

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5. Saltwater and phosphorus drive unique soil biogeochemical processes in freshwater and brackish wetland mesocosms

   https://doi.org/10.1002/ecs2.3704  

   Servais, Shelby; Kominoski, John S.; Fernandez, Marco; Morales, Kristina (August 2021, Ecosphere)

   Abstract Coastal ecosystems are exposed to saltwater intrusion but differential effects on biogeochemical cycling are uncertain. We tested how elevated salinity and phosphorus (P) individually and interactively affect microbial activities and biogeochemical cycling in freshwater and brackish wetland soils. In experimental mesocosms, we added crossed gradients of elevated concentrations of soluble reactive P (SRP) (0, 20, 40, 60, 80 μg/L) and salinity (0, 4, 7, 12, 16 ppt) to freshwater and brackish peat soils (10, 14, 17, 22, 26 ppt) for 35 d. We quantified changes in water chemistry [dissolved organic carbon (DOC), ammonium (), nitrate + nitrite (N + N), SRP concentrations], soil microbial extracellular enzyme activities, respiration rates, microbial biomass C, and soil chemistry (%C, %N, %P, C:N, C:P, N:P). DOC, , and SRP increased in freshwater but decreased in brackish mesocosms with elevated salinity. DOC similarly decreased in brackish mesocosms with added P, and N + N decreased with elevated salinity in both freshwater and brackish mesocosms. In freshwater soils, water column P uptake occurred only in the absence of elevated salinity and when P was above 40 µg/L. Freshwater microbial EEAs, respiration rates, and microbial biomass C were consistently higher compared to those from brackish soils, and soil phosphatase activities and microbial respiration rates in freshwater soils decreased with elevated salinity. Elevated salinity increased arylsulfatase activities and microbial biomass C in brackish soils, and elevated P increased microbial respiration rates in brackish soils. Freshwater soil %C, %N, %P decreased and C:P and N:P increased with elevated salinity. Elevated P increased %C and C:N in freshwater soils and increased %P but decreased C:P and N:P in brackish soils. Freshwater soils released more C and nutrients than brackish soils when exposed to elevated salinity, and both soils were less responsive to elevated P than expected. Freshwater soils became more nutrient‐depleted with elevated salinity, whereas brackish soils were unaffected by salinity but increased P uptake. Microbial activities in freshwater soils were inhibited by elevated salinity and unaffected by added P, but brackish soil microbial activities slightly increased with elevated salinity and P. 

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