Frey Serita D.

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Frey

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Serita D.

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0000-0002-9221-5919

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Long-term warming alters carbohydrate degradation potential in temperate forest soils

(American Society for Microbiology, 2016-09-02) Pold, Grace ; Billings, Andrew F. ; Blanchard, Jeffrey L. ; Burkhardt, Daniel B. ; Frey, Serita D. ; Melillo, Jerry M. ; Schnabel, Julia ; van Diepen, Linda T. A. ; DeAngelis, Kristen M.

As Earth's climate warms, soil carbon pools and the microbial communities that process them may change, altering the way in which carbon is recycled in soil. In this study, we used a combination of metagenomics and bacterial cultivation to evaluate the hypothesis that experimentally raising soil temperatures by 5°C for 5, 8, or 20 years increased the potential for temperate forest soil microbial communities to degrade carbohydrates. Warming decreased the proportion of carbohydrate-degrading genes in the organic horizon derived from eukaryotes and increased the fraction of genes in the mineral soil associated with Actinobacteria in all studies. Genes associated with carbohydrate degradation increased in the organic horizon after 5 years of warming but had decreased in the organic horizon after warming the soil continuously for 20 years. However, a greater proportion of the 295 bacteria from 6 phyla (10 classes, 14 orders, and 34 families) isolated from heated plots in the 20-year experiment were able to depolymerize cellulose and xylan than bacterial isolates from control soils. Together, these findings indicate that the enrichment of bacteria capable of degrading carbohydrates could be important for accelerated carbon cycling in a warmer world.
Long-term forest soil warming alters microbial communities in temperate forest soils

(Frontiers Media, 2015-02-13) DeAngelis, Kristen M. ; Pold, Grace ; Topcuoglu, Begum D. ; van Diepen, Linda T. A. ; Varney, Rebecca M. ; Blanchard, Jeffrey L. ; Melillo, Jerry M. ; Frey, Serita D.

Soil microbes are major drivers of soil carbon cycling, yet we lack an understanding of how climate warming will affect microbial communities. Three ongoing field studies at the Harvard Forest Long-term Ecological Research (LTER) site (Petersham, MA) have warmed soils 5°C above ambient temperatures for 5, 8, and 20 years. We used this chronosequence to test the hypothesis that soil microbial communities have changed in response to chronic warming. Bacterial community composition was studied using Illumina sequencing of the 16S ribosomal RNA gene, and bacterial and fungal abundance were assessed using quantitative PCR. Only the 20-year warmed site exhibited significant change in bacterial community structure in the organic soil horizon, with no significant changes in the mineral soil. The dominant taxa, abundant at 0.1% or greater, represented 0.3% of the richness but nearly 50% of the observations (sequences). Individual members of the Actinobacteria, Alphaproteobacteria and Acidobacteria showed strong warming responses, with one Actinomycete decreasing from 4.5 to 1% relative abundance with warming. Ribosomal RNA copy number can obfuscate community profiles, but is also correlated with maximum growth rate or trophic strategy among bacteria. Ribosomal RNA copy number correction did not affect community profiles, but rRNA copy number was significantly decreased in warming plots compared to controls. Increased bacterial evenness, shifting beta diversity, decreased fungal abundance and increased abundance of bacteria with low rRNA operon copy number, including Alphaproteobacteria and Acidobacteria, together suggest that more or alternative niche space is being created over the course of long-term warming.
Adjustment of forest ecosystem root respiration as temperature warms

( 2008-06) Burton, Andrew J. ; Melillo, Jerry M. ; Frey, Serita D.

Adjustment of ecosystem root respiration to warmer climatic conditions can alter the autotrophic portion of soil respiration and influence the amount of carbon available for biomass production. We examined 44 published values of annual forest root respiration and found an increase in ecosystem root respiration with increasing mean annual temperature (MAT), but the rate of this cross-ecosystem increase (Q10 = 1.6) is less than published values for short-term responses of root respiration to temperature within ecosystems (Q10 = 2 to 3). When specific root respiration rates and root biomass values were examined, there was a clear trend for decreasing root metabolic capacity (respiration rate at a standard temperature) with increasing MAT. There also were tradeoffs between root metabolic capacity and root system biomass, such that there were no instances of high growing season respiration rates and high root biomass occurring together. We also examined specific root respiration rates at three soil warming experiments at Harvard Forest, USA, and found decreases in metabolic capacity for roots from the heated plots. This decline could be due to either physiological acclimation or to the effects of co-occurring drier soils on the measurement date. Regardless of the cause, these findings clearly suggest that modeling efforts that allow root respiration to increase exponentially with temperature, with Q10 values of 2 or more, may over-predict root contributions to ecosystem CO2 efflux for future climates and underestimate the amount of C available for other uses, including NPP.
Decreased mass specific respiration under experimental warming is robust to the microbial biomass method employed

( 2009-05) Bradford, Mark A. ; Wallenstein, Matthew D. ; Allison, Steven D. ; Treseder, Kathleen K. ; Frey, Serita D. ; Watts, Brian W. ; Davies, Christian A. ; Maddox, Thomas R. ; Melillo, Jerry M. ; Mohan, Jacqueline E. ; Reynolds, James F.

Hartley et al. question whether reduction in Rmass, under experimental warming, arises because of the biomass method. We show the method they treat as independent yields the same result. We describe why the substrate-depletion hypothesis cannot alone explain observed responses, and urge caution in the interpretation of the seasonal data.
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world

( 2017-03) Melillo, Jerry M. ; Frey, Serita D. ; DeAngelis, Kristen M. ; Werner, William J. ; Bernard, Michael J. ; Bowles, F. P. ; Pold, Grace ; Grandy, A. Stuart

In a 26-year soil warming experiment in a mid-latitude hardwood forest, we documented changes in soil carbon cycling to investigate the potential consequences for the climate system. We found that soil warming results in a four-phase pattern of soil organic matter decay and carbon dioxide fluxes to the atmosphere, with phases of substantial soil carbon loss alternating with phases of no detectable loss. Several factors combine to affect the timing, magnitude, and thermal acclimation of soil carbon loss. These include depletion of microbially accessible carbon pools, reductions in microbial biomass, a shift in microbial carbon use efficiency, and changes in microbial community composition. Our results support projections of a long-term, self-reinforcing carbon feedback from mid-latitude forests to the climate system as the world warms.
Fungal community response to long-term soil warming with potential implications for soil carbon dynamics

(Ecological Society of America, 2021-05-11) Pec, Gregory J. ; van Diepen, Linda T. A. ; Knorr, Melissa ; Grandy, A. Stuart ; Melillo, Jerry M. ; DeAngelis, Kristen M. ; Blanchard, Jeffrey L. ; Frey, Serita D.

The direction and magnitude of climate warming effects on ecosystem processes such as carbon cycling remain uncertain. Soil fungi are central to these processes due to their roles as decomposers of soil organic matter, as mycorrhizal symbionts, and as determinants of plant diversity. Yet despite their importance to ecosystem functioning, we lack a clear understanding of the long-term response of soil fungal communities to warming. Toward this goal, we characterized soil fungal communities in two replicated soil warming experiments at the Harvard Forest (Petersham, Massachusetts, USA) which had experienced 5°C above ambient soil temperatures for 5 and 20 yr at the time of sampling. We assessed fungal diversity and community composition by sequencing the ITS2 region of rDNA using Illumina technology, along with soil C concentrations and chemistry. Three main findings emerged: (1) long-, but not short-term warming resulted in compositional shifts in the soil fungal community, particularly in the saprotrophic and unknown components of the community; (2) soil C concentrations and the total C stored in the organic horizon declined in response to both short- (5 yr) and long-term (20 yr) warming; and (3) following long-term warming, shifts in fungal guild relative abundances were associated with substantial changes in soil organic matter chemistry, particularly the relative abundance of lignin. Taken together, our results suggest that shifts with warming in the relative abundance of fungal functional groups and dominant fungal taxa are related to observed losses in total soil C.
Thermal adaptation of soil microbial respiration to elevated temperature

( 2008-07-22) Bradford, Mark A. ; Davies, Christian A. ; Frey, Serita D. ; Maddox, Thomas R. ; Melillo, Jerry M. ; Mohan, Jacqueline E. ; Reynolds, James F. ; Treseder, Kathleen K. ; Wallenstein, Matthew D.

In the short-term heterotrophic soil respiration is strongly and positively related to temperature. In the long-term its response to temperature is uncertain. One reason for this is because in field experiments increases in respiration due to warming are relatively short-lived. The explanations proposed for this ephemeral response include depletion of fast-cycling, soil carbon pools and thermal adaptation of microbial respiration. Using a >15 year soil warming experiment in a mid-latitude forest, we show that the apparent ‘acclimation’ of soil respiration at the ecosystem scale results from combined effects of reductions in soil carbon pools and microbial biomass, and thermal adaptation of microbial respiration. Mass specific respiration rates were lower when seasonal temperatures were higher, suggesting that rate reductions under experimental warming likely occurred through temperature-induced changes in the microbial community. Our results imply that stimulatory effects of global temperature rise on soil respiration rates may be lower than currently predicted.
Slowed biogeochemical cycling in sub-arctic birch forest linked to reduced mycorrhizal growth and community change after a defoliation event

(Springer, 2016-08-25) Parker, Thomas C. ; Sadowsky, Jesse ; Dunleavy, Haley ; Subke, Jens-Arne ; Frey, Serita D. ; Wookey, Philip A.

Sub-arctic birch forests (Betula pubescens Ehrh. ssp. czerepanovii) periodically suffer large-scale defoliation events caused by the caterpillars of the geometrid moths Epirrita autumnata and Operophtera brumata. Despite their obvious influence on ecosystem primary productivity, little is known about how the associated reduction in belowground C allocation affects soil processes. We quantified the soil response following a natural defoliation event in sub-arctic Sweden by measuring soil respiration, nitrogen availability and ectomycorrhizal fungi (EMF) hyphal production and root tip community composition. There was a reduction in soil respiration and an accumulation of soil inorganic N in defoliated plots, symptomatic of a slowdown of soil processes. This coincided with a reduction of EMF hyphal production and a shift in the EMF community to lower autotrophic C-demanding lineages (for example, /russula-lactarius). We show that microbial and nutrient cycling processes shift to a slower, less C-demanding state in response to canopy defoliation. We speculate that, amongst other factors, a reduction in the potential of EMF biomass to immobilise excess mineral nitrogen resulted in its build-up in the soil. These defoliation events are becoming more geographically widespread with climate warming, and could result in a fundamental shift in sub-arctic ecosystem processes and properties. EMF fungi may be important in mediating the response of soil cycles to defoliation and their role merits further investigation.
Microbial diversity drives carbon use efficiency in a model soil

(Nature Research, 2020-07-23) Domeignoz-Horta, Luiz A. ; Pold, Grace ; Liu, Xiao-Jun Allen ; Frey, Serita D. ; Melillo, Jerry M. ; DeAngelis, Kristen M.

Empirical evidence for the response of soil carbon cycling to the combined effects of warming, drought and diversity loss is scarce. Microbial carbon use efficiency (CUE) plays a central role in regulating the flow of carbon through soil, yet how biotic and abiotic factors interact to drive it remains unclear. Here, we combine distinct community inocula (a biotic factor) with different temperature and moisture conditions (abiotic factors) to manipulate microbial diversity and community structure within a model soil. While community composition and diversity are the strongest predictors of CUE, abiotic factors modulated the relationship between diversity and CUE, with CUE being positively correlated with bacterial diversity only under high moisture. Altogether these results indicate that the diversity × ecosystem-function relationship can be impaired under non-favorable conditions in soils, and that to understand changes in soil C cycling we need to account for the multiple facets of global changes.
Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long‐term warming

(Wiley, 2022-11-30) Domeignoz‐Horta, Luiz A. ; Pold, Grace ; Erb, Hailey ; Sebag, David ; Verrecchia, Eric ; Northen, Trent ; Louie, Katherine ; Eloe‐Fadrosh, Emiley ; Pennacchio, Christa ; Knorr, Melissa A. ; Frey, Serita D. ; Melillo, Jerry M. ; DeAngelis, Kristen M.

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.Warming can accelerate or decelerate soil microbial response to warmer temperatures. Here we provide support for the hypothesis that microbial temperature sensitivity is contingent upon substrate availability, which itself is reduced by warming. Thus we show the complex interplay between microbial activity and changes in soil carbon stocks.
Microbial responses to long-term warming differ across soil microenvironments

(Oxford University Press, 2024-04-06) Liu, Xiao-Jun Allen ; Han, Shun ; Frey, Serita D. ; Melillo, Jerry M. ; Zhou, Jizhong ; DeAngelis, Kristen M.

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.

Frey Serita D.

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