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. IMPORTANCE 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. 

Thermal adaptation of soil microbial growth traits in response to chronic warming

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 thirty years. We hypothesized that Alphaproteobacteria from warmed plots have (1) less temperature sensitive growth rates; (2) higher optimum growth temperatures; and (3) 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 22-37°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. Importance 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 to 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 increased optimum growth temperature. This suggests that increased microbial biomass and growth relative to respiration in a warming world should 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.

https://www.biorxiv.org/content/biorxiv/early/2023/05/20/2023.05.19.541531.full.pdf

Below-ground carbon transformations represent a natural climate change mitigation solution, but newly-acquired traits adaptive to climate stress may alter microbial climate feedback mechanisms. To better define microbial evolutionary responses to long-term climate warming, we study microorganisms from an ongoing in situ soil warming experiment at the Harvard Forest Long-term Ecological Research (LTER) site where, for over three decades, soils are continuously heated 5 °C above ambient temperatures. We hypothesize that across generations of chronic warming, genomic signatures within diverse bacterial lineages reflect trait-based adaptations related to growth and carbon utilization. From our culture collection of soil bacteria isolated from experimental heated and control plots, we sequenced genomes representing taxa dominant in soil communities and sensitive to warming, including independent lineages of Alphaproteobacteria, Actinobacteria, and Betaproteobacteria. We investigated differences in genomic attributes and patterns of functional gene content to identify genetic signatures of adaptation. Comparative pangenomics revealed differently abundant gene clusters with functional annotations related to carbon and nitrogen metabolism. We also observed differences in global codon usage bias between heated and control genomes, suggesting potential adaptive traits related to growth or growth efficiency. This effect was more varied for organisms with fewer 16S rrn operons, suggesting that these organisms experience different selective pressures on growth efficiency. Together, these data illustrate the emergence of lineage-specific traits as well as common ecological-evolutionary microbial responses to climate change.

/pdf/pangenomes-reveal-genomic-signatures-of-microbial-adaptation-2boqtc4v.pdf

Pangenomes reveal genomic signatures of microbial adaptation to experimental soil warming

Pangenomes suggest ecological-evolutionary responses to experimental soil warming.

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Pangenomes reveal genomic signatures of microbial adaptation to experimental soil warming

Pangenomes suggest ecological-evolutionary responses to experimental soil warming.