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1. Pangenomes suggest ecological-evolutionary responses to experimental soil warming

   https://doi.org/10.1128/msphere.00059-25  

   Choudoir, Mallory J; Narayanan, Achala; Rodriguez-Ramos, Damayanti; Simoes, Rachel; Efroni, Alon; Sondrini, Abigail; DeAngelis, Kristen M (April 2025, mSphere)

   Tringe, Susannah Green (Ed.)

   ABSTRACT Below-ground carbon transformations that contribute to healthy soils represent a natural climate change mitigation, but newly acquired traits adaptive to climate stress may alter microbial feedback mechanisms. To better define microbial evolutionary responses to long-term climate warming, we study microorganisms from an ongoingin situsoil warming experiment where, for over three decades, temperate forest soils are continuously heated at 5°C above ambient. We hypothesize that across generations of chronic warming, genomic signatures within diverse bacterial lineages reflect adaptations related to growth and carbon utilization. From our bacterial culture collection isolated from experimental heated and control plots, we sequenced genomes representing dominant taxa sensitive to warming, including lineages of Actinobacteria, Alphaproteobacteria, and Betaproteobacteria. We investigated genomic attributes and functional gene content to identify signatures of adaptation. Comparative pangenomics revealed accessory gene clusters related to central metabolism, competition, and carbon substrate degradation, with few functional annotations explicitly associated with long-term warming. Trends in functional gene patterns suggest genomes from heated plots were relatively enriched in central carbohydrate and nitrogen metabolism pathways, while genomes from control plots were relatively enriched in amino acid and fatty acid metabolism pathways. We observed that genomes from heated plots had less codon bias, suggesting potential adaptive traits related to growth or growth efficiency. Codon usage bias varied for organisms with similar 16Srrnoperon copy number, suggesting that these organisms experience different selective pressures on growth efficiency. Our work suggests the emergence of lineage-specific trends as well as common ecological-evolutionary microbial responses to climate change.IMPORTANCEAnthropogenic climate change threatens soil ecosystem health in part by altering below-ground carbon cycling carried out by microbes. Microbial evolutionary responses are often overshadowed by community-level ecological responses, but adaptive responses represent potential changes in traits and functional potential that may alter ecosystem function. We predict that microbes are adapting to climate change stressors like soil warming. To test this, we analyzed the genomes of bacteria from a soil warming experiment where soil plots have been experimentally heated 5°C above ambient for over 30 years. While genomic attributes were unchanged by long-term warming, we observed trends in functional gene content related to carbon and nitrogen usage and genomic indicators of growth efficiency. These responses may represent new parameters in how soil ecosystems feedback to the climate system. 

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2. 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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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. Response of Root Respiration to Warming and Nitrogen Addition Depends on Tree Species

   https://doi.org/10.1111/gcb.17530  

   Muratore, T. J.; Knorr, M. A.; Simpson, M. J.; Stephens, R. B.; Phillips, R. P.; Frey, S. D. (October 2024, Global Change Biology)

   ABSTRACT Roots contribute a large fraction of CO₂efflux from soils, yet the extent to which global change factors affect root‐derived fluxes is poorly understood. We investigated how red maple (Acer rubrum) and red oak (Quercus rubra) root biomass and respiration respond to long‐term (15 years) soil warming, nitrogen addition, or their combination in a temperate forest. We found that ecosystem root respiration was decreased by 40% under both single‐factor treatments (nitrogen addition or warming) but not under their combination (heated × nitrogen). This response was driven by the reduction of mass‐specific root respiration under warming and a reduction in maple root biomass in both single‐factor treatments. Mass‐specific root respiration rates for both species acclimated to soil warming, resulting in a 43% reduction, but were not affected by N addition or the combined heated × N treatment. Notably, the addition of nitrogen to warmed soils alleviated thermal acclimation and returned mass‐specific respiration rates to control levels. Oak roots contributed disproportionately to ecosystem root respiration despite the decrease in respiration rates as their biomass was maintained or enhanced under warming and nitrogen addition. In contrast, maple root respiration rates were consistently higher than oak, and this difference became critical in the heated × nitrogen treatment, where maple root biomass increased, contributing significantly more CO₂relative to single‐factor treatments. Our findings highlight the importance of accounting for the root component of respiration when assessing soil carbon loss in response to global change and demonstrate that combining warming and N addition produces effects that cannot be predicted by studying these factors in isolation. 

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5. 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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