skip to main content


Title: The Transcriptional Response of Soil Bacteria to Long-Term Warming and Short-Term Seasonal Fluctuations in a Terrestrial Forest
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
Award ID(s):
1832210
NSF-PAR ID:
10315254
Author(s) / Creator(s):
; ; ; ; ; ; ;
Date Published:
Journal Name:
Frontiers in Microbiology
Volume:
12
ISSN:
1664-302X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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.

    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.

     
    more » « less
  2. Abstract

    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.

     
    more » « less
  3. Abstract

    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.

     
    more » « less
  4. Abstract

    How climate warming interacts with atmospheric nitrogen (N) deposition to affect carbon (C) release from soils remains largely elusive, posing a major challenge in projecting climate change‒terrestrial C feedback.

    As part of a 5‐year (2006–2010) field manipulative experiment, this study was designed to examine the effects of 24‐hr continuous warming and N addition on soil respiration and explore the underlying mechanisms in a semi‐arid grassland on the Mongolian Plateau, China.

    Across the 5 years and all plots, soil respiration was not changed under the continuous warming, but was decreased by 3.7% under the N addition. The suppression of soil respiration by N addition in the third year and later could be mainly due to the reductions in the forb‐to‐grass biomass ratios. Moreover, there were interactive effects between continuous warming and N addition on soil respiration. Continuous warming increased soil respiration by 5.8% in the ambient N plots, but reduced it by 6.3% in the enriched N plots. Soil respiration was unaffected by N addition in the ambient temperature plots yet decreased by 9.4% in the elevated temperature plots. Changes of soil moisture and the proportion of legume biomass in the community might be primarily responsible for the non‐additive effects of continuous warming and N addition on soil respiration.

    This study provides empirical evidence for the positive climate warming‒soil C feedback in the ambient N condition. However, N deposition reverses the positive warming‒soil C feedback into a negative feedback, leading to decreased C loss from soils under a warming climate. Incorporating our findings into C‐cycling models could reduce the uncertainties of model projections for land C sink and global C cycling under multifactorial global change scenarios.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  5. The permafrost region has accumulated organic carbon in cold and waterlogged soils over thousands of years and now contains three times as much carbon as the atmosphere. Global warming is degrading permafrost with the potential to accelerate climate change as increased microbial decomposition releases soil carbon as greenhouse gases. A 19-year time series of soil and ecosystem respiration radiocarbon from Alaska provides long-term insight into changing permafrost soil carbon dynamics in a warmer world. Nine per cent of ecosystem respiration and 23% of soil respiration observations had radiocarbon values more than 50‰ lower than the atmospheric value. Furthermore, the overall trend of ecosystem and soil respiration radiocarbon values through time decreased more than atmospheric radiocarbon values did, indicating that old carbon degradation was enhanced. Boosted regression tree analyses showed that temperature and moisture environmental variables had the largest relative influence on lower radiocarbon values. This suggested that old carbon degradation was controlled by warming/permafrost thaw and soil drying together, as waterlogged soil conditions could protect soil carbon from microbial decomposition even when thawed. Overall, changing conditions increasingly favoured the release of old carbon, which is a definitive fingerprint of an accelerating feedback to climate change as a consequence of warming and permafrost destabilization.

    This article is part of the Theo Murphy meeting issue ‘Radiocarbon in the Anthropocene’.

     
    more » « less