skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


This content will become publicly available on April 29, 2026

Title: Pangenomes suggest ecological-evolutionary responses to experimental soil warming
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.  more » « less
Award ID(s):
1949882
PAR ID:
10620782
Author(s) / Creator(s):
; ; ; ; ; ;
Editor(s):
Tringe, Susannah Green
Publisher / Repository:
American Society for Microbiology
Date Published:
Journal Name:
mSphere
Volume:
10
Issue:
4
ISSN:
2379-5042
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; (, 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. 
    more » « less
  2. ; ; ; ; ; ; ; (, 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. 
    more » « less
  3. ; (, 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. 
    more » « less
  4. ; ; ; ; ; ; (, 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. 
    more » « less
  5. ; ; ; ; ; (, ISME Communications)
    Soil carbon loss is likely to increase due to climate warming, but microbiomes and microenvironments may dampen this effect. In a 30-year warming experiment, physical protection within soil aggregates affected the thermal responses of soil microbiomes and carbon dynamics. In this study, we combined metagenomic analysis with physical characterization of soil aggregates to explore mechanisms by which microbial communities respond to climate warming across different soil microenvironments. Long-term warming decreased the relative abundances of genes involved in degrading labile compounds (e.g., cellulose), but increased those genes involved in degrading recalcitrant compounds (e.g., lignin) across aggregate sizes. These changes were observed in most phyla of bacteria, especially for Acidobacteria, Actinobacteria, Bacteroidetes, Chloroflexi, and Planctomycetes. Microbial community composition was considerably altered by warming, leading to declined diversity for bacteria and fungi but not for archaea. Microbial functional genes, diversity, and community composition differed between macroaggregates and microaggregates, indicating the essential role of physical protection in controlling microbial community dynamics. Our findings suggest that microbes have the capacity to employ various strategies to acclimate or adapt to climate change (e.g., warming, heat stress) by shifting functional gene abundances and community structures in varying microenvironments, as regulated by soil physical protection. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email