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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. 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. 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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4. 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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5. Maximum summer temperatures predict the temperature adaptation of Arctic soil bacterial communities

   https://doi.org/10.5194/bg-20-767-2023  

   Rijkers, Ruud; Dekker, Mark; Aerts, Rien; Weedon, James T. (January 2023, Biogeosciences)

   Abstract. Rapid warming of the Arctic terrestrial region has the potential to increase soil decomposition rates and form a carbon-driven feedback to future climate change. For an accurate prediction of the role of soil microbes in these processes, it will be important to understand the temperature responses of soil bacterial communities and implement them into biogeochemical models. The temperature adaptation of soil bacterial communities for a large part of the Arctic region is unknown. We evaluated the current temperature adaption of soil bacterial communities from 12 sampling sites in the sub- to High Arctic region. Temperature adaptation differed substantially between the soil bacterial communities of these sites, with estimates of optimal growth temperature (Topt) ranging between 23.4 ± 0.5 and 34.1 ± 3.7 ∘C. We evaluated possible statistical models for the prediction of the temperature adaption of soil bacterial communities based on different climate indices derived from soil temperature records or on bacterial community composition data. We found that highest daily average soil temperature was the best predictor for the Topt of the soil bacterial communities, increasing by 0.63 ∘C ∘C−1. We found no support for the prediction of temperature adaptation by regression tree analysis based on the relative abundance data of the most common bacterial species. Increasing summer temperatures will likely increase Topt of soil bacterial communities in the Arctic. Incorporating this mechanism into soil biogeochemical models and combining it with projections of soil temperature will help to reduce uncertainty in assessments of the vulnerability of soil carbon stocks in the Arctic. 

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