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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. Responses of tundra soil microbial communities to half a decade of experimental warming at two critical depths

   https://doi.org/10.1073/pnas.1901307116  

   Johnston, Eric R. ; Hatt, Janet K. ; He, Zhili ; Wu, Liyou ; Guo, Xue ; Luo, Yiqi ; Schuur, Edward A. ; Tiedje, James M. ; Zhou, Jizhong ; Konstantinidis, Konstantinos T. ( July 2019 , Proceedings of the National Academy of Sciences)

   Northern-latitude tundra soils harbor substantial carbon (C) stocks that are highly susceptible to microbial degradation with rising global temperatures. Understanding the magnitude and direction (e.g., C release or sequestration) of the microbial responses to warming is necessary to accurately model climate change. In this study, Alaskan tundra soils were subjected to experimental in situ warming by ∼1.1 °C above ambient temperature, and the microbial communities were evaluated using metagenomics after 4.5 years, at 2 depths: 15 to 25 cm (active layer at outset of the experiment) and 45 to 55 cm (transition zone at the permafrost/active layer boundary at the outset of the experiment). In contrast to small or insignificant shifts after 1.5 years of warming, 4.5 years of warming resulted in significant changes to the abundances of functional traits and the corresponding taxa relative to control plots (no warming), and microbial shifts differed qualitatively between the two soil depths. At 15 to 25 cm, increased abundances of carbohydrate utilization genes were observed that correlated with (increased) measured ecosystem carbon respiration. At the 45- to 55-cm layer, increased methanogenesis potential was observed, which corresponded with a 3-fold increase in abundance of a single archaeal clade of the Methanosarcinales order, increased annual thaw duration (45.3 vs. 79.3 days), and increased CH 4 emissions. Collectively, these data demonstrate that the microbial responses to warming in tundra soil are rapid and markedly different between the 2 critical soil layers evaluated, and identify potential biomarkers for the corresponding microbial processes that could be important in modeling. 

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3. Infrared heater system for warming tropical forest understory plants and soils

   https://doi.org/10.1002/ece3.3780  

   Kimball, Bruce A. ; Alonso‐Rodríguez, Aura M. ; Cavaleri, Molly A. ; Reed, Sasha C. ; González, Grizelle ; Wood, Tana E. ( January 2018 , Ecology and Evolution)

   The response of tropical forests to global warming is one of the largest uncertainties in predicting the future carbon balance of Earth. To determine the likely effects of elevated temperatures on tropical forest understory plants and soils, as well as other ecosystems, an infrared (IR) heater system was developed to provide in situ warming for the Tropical Responses to Altered Climate Experiment (TRACE) in the Luquillo Experimental Forest in Puerto Rico. Three replicate heated 4‐m‐diameter plots were warmed to maintain a 4°C increase in understory vegetation compared to three unheated control plots, as sensed by IR thermometers. The equipment was larger than any used previously and was subjected to challenges different from those of many temperate ecosystem warming systems, including frequent power surges and outages, high humidity, heavy rains, hurricanes, saturated clayey soils, and steep slopes. The system was able to maintain the target 4.0°C increase in hourly average vegetation temperatures to within ± 0.1°C. The vegetation was heterogeneous and on a 21° slope, which decreased uniformity of the warming treatment on the plots; yet, the green leaves were fairly uniformly warmed, and there was little difference among 0–10 cm depth soil temperatures at the plot centers, edges, and midway between. Soil temperatures at the 40–50 cm depth increased about 3°C compared to the controls after a month of warming. As expected, the soil in the heated plots dried faster than that of the control plots, but the average soil moisture remained adequate for the plants. TheTRACEheating system produced an adequately uniform warming precisely controlled down to at least 50‐cm soil depth, thereby creating a treatment that allows for assessing mechanistic responses of tropical plants and soil to warming, with applicability to other ecosystems. No physical obstacles to scaling the approach to taller vegetation (i.e., trees) and larger plots were observed.

    

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4. Decreased Soil Organic Matter in a Long‐Term Soil Warming Experiment Lowers Soil Water Holding Capacity and Affects Soil Thermal and Hydrological Buffering

   https://doi.org/10.1029/2019JG005158  

   Werner, W. J. ; Sanderman, J. ; Melillo, J. M. ( April 2020 , Journal of Geophysical Research: Biogeosciences)

   Long‐term soil warming can decrease soil organic matter (SOM), resulting in self‐reinforcing feedback to the global climate system. We investigated additional consequences of SOM reduction for soil water holding capacity (WHC) and soil thermal and hydrological buffering. At a long‐term soil warming experiment in a temperate forest in the northeastern United States, we suspended the warming treatment for 104 days during the summer of 2017. The formerly heated plot remained warmer (+0.39 °C) and drier (−0.024 cm³H₂O cm⁻³soil) than the control plot throughout the suspension. We measured decreased SOM content (−0.184 g SOM g⁻¹for O horizon soil, −0.010 g SOM g⁻¹for A horizon soil) and WHC (−0.82 g H₂O g⁻¹for O horizon soil, −0.18 g H₂O g⁻¹for A horizon soil) in the formerly heated plot relative to the control plot. Reduced SOM content accounted for 62% of the WHC reduction in the O horizon and 22% in the A horizon. We investigated differences in SOM composition as a possible explanation for the remaining reductions with Fourier transform infrared (FTIR) spectra. We found FTIR spectra that correlated more strongly with WHC than SOM, but those particular spectra did not differ between the heated and control plots, suggesting that SOM composition affects WHC but does not explain treatment differences in this study. We conclude that SOM reductions due to soil warming can reduce WHC and hydrological and thermal buffering, further warming soil and decreasing SOM. This feedback may operate in parallel, and perhaps synergistically, with carbon cycle feedbacks to climate change.

    

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5. Ethylene-mediated metabolic priming increases photosynthesis and metabolism to enhance plant growth and stress tolerance

   https://doi.org/10.1093/pnasnexus/pgad216  

   Brenya, Eric ; Dutta, Esha ; Herron, Brittani ; Walden, Lauren H. ; Roberts, Daniel M. ; Binder, Brad M. ; Bayer, ed., Edward ( July 2023 , PNAS Nexus)

   Enhancing crop yields is a major challenge because of an increasing human population, climate change, and reduction in arable land. Here, we demonstrate that long-lasting growth enhancement and increased stress tolerance occur by pretreatment of dark grown Arabidopsis seedlings with ethylene before transitioning into light. Plants treated this way had longer primary roots, more and longer lateral roots, and larger aerial tissue and were more tolerant to high temperature, salt, and recovery from hypoxia stress. We attributed the increase in plant growth and stress tolerance to ethylene-induced photosynthetic-derived sugars because ethylene pretreatment caused a 23% increase in carbon assimilation and increased the levels of glucose (266%), sucrose/trehalose (446%), and starch (87%). Metabolomic and transcriptomic analyses several days posttreatment showed a significant increase in metabolic processes and gene transcripts implicated in cell division, photosynthesis, and carbohydrate metabolism. Because of this large effect on metabolism, we term this “ethylene-mediated metabolic priming.” Reducing photosynthesis with inhibitors or mutants prevented the growth enhancement, but this was partially rescued by exogenous sucrose, implicating sugars in this growth phenomenon. Additionally, ethylene pretreatment increased the levels of CINV1 and CINV2 encoding invertases that hydrolyze sucrose, and cinv1;cinv2 mutants did not respond to ethylene pretreatment with increased growth indicating increased sucrose breakdown is critical for this trait. A model is proposed where ethylene-mediated metabolic priming causes long-term increases in photosynthesis and carbohydrate utilization to increase growth. These responses may be part of the natural development of seedlings as they navigate through the soil to emerge into light.

    

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