Microbial diversity drives carbon use efficiency in a model soil

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Domeignoz-Horta, L. A., Pold, G., Liu, X. A., Frey, S. D., Melillo, J. M., & DeAngelis, K. M. Microbial diversity drives carbon use efficiency in a model soil. Nature Communications, 11(1), (2020): 3684, doi:10.1038/s41467-020-17502-z.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.Funding for this project was provided by the Department of Energy grant DE-SC0016590 to K.M.D. and S.D.F., and an American Association of University Women Dissertation fellowship to G.P. We would also like to thank Stuart Grandy and Kevin Geyer for the fruitful discussions and Mary Waters, Courtney Bly and Ana Horta for their help with samples processing

Long-term forest soil warming alters microbial communities in temperate forest soils

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

Reduced carbon use efficiency and increased microbial turnover with soil warming

Global soil carbon (C) stocks are expected to decline with warming, and changes in microbial processes are key to this projection. However, warming responses of critical microbial parameters such as carbon use efficiency (CUE) and biomass turnover (rB) are not well understood. Here, we determine these parameters using a probabilistic inversion approach that integrates a microbial-enzyme model with 22 years of carbon cycling measurements at Harvard Forest. We find that increasing temperature reduces CUE but increases rB, and that two decades of soil warming increases the temperature sensitivities of CUE and rB. These temperature sensitivities, which are derived from decades-long field observations, contrast with values obtained from short-term laboratory experiments. We also show that long-term soil C flux and pool changes in response to warming are more dependent on the temperature sensitivity of CUE than that of rB. Using the inversion-derived parameters, we project that chronic soil warming at Harvard Forest over six decades will result in soil C gain of \u3c1.0% on average (1st and 3rd quartiles: 3.0% loss and 10.5% gain) in the surface mineral horizon. Our results demonstrate that estimates of temperature sensitivity of microbial CUE and rB can be obtained and evaluated rigorously by integrating multidecadal datasets. This approach can potentially be applied in broader spatiotemporal scales to improve long-term projections of soil C feedbacks to climate warming

Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world

Author Posting. © The Author(s), 2017. This is the author's version of the work. It is posted here for personal use, not for redistribution. The definitive version was published in Science 358 (2017): 101-105, doi:10.1126/science.aan2874.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.This research has been supported by grants from the Department of Energy - DE-SC0010740; DOE DE-SC0016590: and the National Science Foundation - DEB 1237491 (LTER) ; DEB 1456528 (LTREB)

Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils

As Earth\u27s 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

Fungal Community Response to Long-Term Soil Warming With Potential Implications for Soil Carbon Dynamics

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 degrees 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

Decreased mass specific respiration under experimental warming is robust to the microbial biomass method employed

Author Posting. © The Author(s), 2009. This is the author's version of the work. It is posted here by permission of Blackwell for personal use, not for redistribution. The definitive version was published in Ecology Letters 12 (2009): E15-E18, doi:10.1111/j.1461-0248.2009.01332.x.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.This research was supported by the Office of Science (BER), U.S. Department of Energy, the Andrew W. Mellon Foundation and U.S. National Science Foundation grants to the Coweeta LTER program

Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long‐term warming

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

Carbon budget of the Harvard Forest Long- Term Ecological Research site: pattern, process, and response to global change

How, where, and why carbon (C) moves into and out of an ecosystem through time are long- standing questions in biogeochemistry. Here, we bring together hundreds of thousands of C- cycle observations at the Harvard Forest in central Massachusetts, USA, a mid- latitude landscape dominated by 80- 120- yr- old closed- canopy forests. These data answered four questions: (1) where and how much C is presently stored in dominant forest types; (2) what are current rates of C accrual and loss; (3) what biotic and abiotic factors contribute to variability in these rates; and (4) how has climate change affected the forest- s C cycle? Harvard Forest is an active C sink resulting from forest regrowth following land abandonment. Soil and tree biomass comprise nearly equal portions of existing C stocks. Net primary production (NPP) averaged 680- 750 g C·m- 2·yr- 1; belowground NPP contributed 38- 47% of the total, but with large uncertainty. Mineral soil C measured in the same inventory plots in 1992 and 2013 was too heterogeneous to detect change in soil- C pools; however, radiocarbon data suggest a small but persistent sink of 10- 30 g C·m- 2·yr- 1. Net ecosystem production (NEP) in hardwood stands averaged ~300 g C·m- 2·yr- 1. NEP in hemlock- dominated forests averaged ~450 g C·m- 2·yr- 1 until infestation by the hemlock woolly adelgid turned these stands into a net C source. Since 2000, NPP has increased by 26%. For the period 1992- 2015, NEP increased 93%. The increase in mean annual temperature and growing season length alone accounted for ~30% of the increase in productivity. Interannual variations in GPP and NEP were also correlated with increases in red oak biomass, forest leaf area, and canopy- scale light- use efficiency. Compared to long- term global change experiments at the Harvard Forest, the C sink in regrowing biomass equaled or exceeded C cycle modifications imposed by soil warming, N saturation, and hemlock removal. Results of this synthesis and comparison to simulation models suggest that forests across the region are likely to accrue C for decades to come but may be disrupted if the frequency or severity of biotic and abiotic disturbances increases.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/163495/3/ecm1423_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/163495/2/ecm1423-sup-0001-AppendixS1.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/163495/1/ecm1423.pd

The state of the Martian climate

60°N was +2.0°C, relative to the 1981–2010 average value (Fig. 5.1). This marks a new high for the record. The average annual surface air temperature (SAT) anomaly for 2016 for land stations north of starting in 1900, and is a significant increase over the previous highest value of +1.2°C, which was observed in 2007, 2011, and 2015. Average global annual temperatures also showed record values in 2015 and 2016. Currently, the Arctic is warming at more than twice the rate of lower latitudes