Up Against The Wall: The Effects of Climate Warming on Soil Microbial Diversity and The Potential for Feedbacks to The Carbon Cycle

Earth’s climate is warming, and there is evidence that increased temperature alters soil C cycling, which may result in a self-reinforcing (positive), microbial mediated feedback to the climate system. Though soil microbes are major drivers of soil C cycling, we lack an understanding of how temperature affects SOM decomposition. Numerous studies have explored, to differing degrees, the extent to which climate change may affect biodiversity. While there is ample evidence that community diversity begets ecosystem stability and resilience, we know of keystone species that perform functions whose effects far outweigh their relative abundance. In this paper, we first review the meaning of microbial diversity and how it relates to ecosystem function, then conduct a literature review of field-based climate warming studies that have made some measure of microbial diversity. Finally, we explore how measures of diversity may yield a larger, more complete picture of climate warming effects on microbial communities, and how this may translate to altered carbon cycling and greenhouse gas emissions. While warming effects seem to be ecosystem-specific, the lack of observable consistency between measures is due in some part to the diversity in measures of microbial diversity

Genome Sequences of \u3cem\u3eFrankineae\u3c/em\u3e sp. Strain MT45 and \u3cem\u3eJatrophihabitans\u3c/em\u3e sp. Strain GAS493, Two Actinobacteria Isolated from Forest Soil

Frankiaceae are bacterial endosymbionts that are also found free-living in soil. Here, we present the genome sequences of two novel bacterial members of the order Frankiales, class Actinobacteria, isolated from temperate terrestrial forest soils. The genomes for MT45 and GAS493 indicate a genetic capacity for carbohydrate degradation but not nitrogen fixation

DRIVERS and CONSEQUENCES of CARBON USE EFFICIENCY - and ITS MEASUREMENT in SOIL

Soils serve as massive carbon sinks, but their ability to continue this ecological service is contingent on how the resident soil microbial community will respond to the ongoing climate crisis. One key dimension of the microbial response to warming is its carbon use efficiency (CUE), or the fraction of carbon taken up by an organism which is allocated to growth rather than respiration. However, the scientific community is still in the early stages of understanding the drivers, consequences - and even accurate measurements of - CUE. In this dissertation, I first quantified the variability of CUE and its responsiveness to temperature and substrate for soil bacteria grown in the lab. I subsequently implemented this knowledge into a plant litter decomposition model to determine how including organism-level variation in CUE alters projected soil carbon stocks in a warmer world. Finally, I completed a series of numerical simulations to evaluate how robust a commonly-used method of measuring CUE in the field is to changes in the microbial community present. I found that CUE was highly variable and depended on both substrate and temperature in a bacteria-specific manner. No robust genetic or genomic markers of CUE or its temperature dependence emerged, indicative of the wide diversity of bacteria characterized in this study. Nonetheless, efficiency tended to decrease with warming more-so in taxa which were already characterized by high efficiency, causing a degree of homogenization in CUE at higher temperatures. Introducing variation in CUE temperature sensitivity to the litter decomposition model DEMENT caused additional litter carbon loss under warming, which indicates the possible importance of accounting for CUE as a niche dimension for species sorting to act upon in decomposition models. Finally, I found the 18O-H2O method of measuring CUE in mixed soil communities is particularly susceptible to misleading results when the assumption of extracellular water being the sole source of oxygen to DNA is violated. Overall, my results indicate that understanding microbial physiology is essential to both the accurate measurement and projection of CUE under the global climate crisis, but that explaining the genomic underpinning of this physiological variation remains a challenge

Draft Genome Sequence of a Terrestrial Planctomycete, \u3cem\u3eSingulisphaera\u3c/em\u3e sp. Strain GP 187, Isolated from Forest Soil

Here we present the draft genome sequence of a novel species of the genus Singulisphaera (phylum Planctomycetes, family Isosphaeraceae), isolated from soil. Singulisphaera sp. strain GP 187 has a relatively large mobilome and numerous novel genes that may contriubte to the production of bioactive molecules

Lowland tundra plant stoichiometry is somewhat resilient decades following fire despite substantial and sustained shifts in community structure

The Arctic is experiencing the greatest increase in average surface temperature globally, which is projected to amplify wildfire frequency and severity. Wildfire alters the biogeochemical characteristics of arctic ecosystems. However, the extent of these changes over time-particularly with regard to plant stoichiometries relative to community structure-is not well documented. Four years after the Yukon-Kuskokwim Delta, Alaska, experienced its largest fire season, aboveground plant and lichen biomass was harvested across a gradient of burn history: unburned ("reference"), 2015 burn ("recent burn"), and 1972 burn ("historic burn") to assess the resilience of tundra plant communities to fire disturbance. Fire reduced aboveground biomass in the recent burn; early recovery was characterized by evergreen shrub and graminoid dominance. In the historic burn, aboveground biomass approached reference conditions despite a sustained reduction of lichen biomass. Although total plant and lichen carbon (C) and nitrogen (N) were reduced immediately following fire, N stocks recovered to a greater degree-reducing community-level C:N. Notably, at the species level, N enrichment was observed only in the recent burn. Yet, community restructuring persisted for decades following fire, reflecting a sustained reduction in N-poor lichens relative to more N-rich vascular plant species

Changes in substrate availability drive carbon cycle response to chronic warming

As earth\u27s climate continues to warm, it is important to understand how the capacity of terrestrial ecosystems to retain carbon (C) will be affected. We combined measurements of microbial activity with the concentration, quality, and physical accessibility of soil carbon to microorganisms to evaluate the mechanisms by which more than two decades of experimental warming has altered the carbon cycle in a Northeast US temperate deciduous forest. We found that concentrations of soil organic matter were reduced in both the organic and mineral soil horizons. The molecular composition of the carbon was altered in the mineral soil with significant reductions in the relative abundance of polysaccharides and lignin, and an increase in lipids. Mineral-associated organic matter was preferentially depleted by warming in the top 3 cm of mineral soil. We found that potential extracellularenzyme activity per gram of soil at a common temperature was generally unaffected by warming treatment. However, by measuring potential extracellular enzyme activities between 4 and 30 °C, we found that activity per unit microbial biomass at in-situ temperatures was increased by warming. This was associated with a tendency for microbial biomass to decrease with warming. These results indicate that chronic warming has reduced soil organic matter concentrations, selecting for a smaller but more active microbial community increasingly dependent on mineral-associated organic matter

Sporadic P limitation constrains microbial growth and facilitates SOM accumulation in the stoichiometrically coupled, acclimating microbe-plant-soil model

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Pold, G., Kwiatkowski, B. L., Rastetter, E. B., & Sistla, S. A. Sporadic P limitation constrains microbial growth and facilitates SOM accumulation in the stoichiometrically coupled, acclimating microbe-plant-soil model. Soil Biology & Biochemistry, 165, (2022): 108489, https://doi.org/10.1016/j.soilbio.2021.108489.Requirements for biomass carbon (C), nitrogen (N), and phosphorus (P) constrain organism growth and are important agents for structuring ecosystems. Arctic tundra habitats are strongly nutrient limited as decomposition and recycling of nutrients are slowed by low temperature. Modeling interactions among these elemental cycles affords an opportunity to explore how disturbances such as climate change might differentially affect these nutrient cycles. Here we introduce a C–N–P-coupled version of the Stoichiometrically Coupled Acclimating Microbe-Plant-Soil (SCAMPS) model, “SCAMPS-CNP”, and a corresponding modified CN-only model, “SCAMPS-CN”. We compared how SCAMPS-CNP and the modified SCAMPS-CN models project a moderate (RCP 6.0) air warming scenario will impact tussock tundra nutrient availability and ecosystem C stocks. SCAMPS-CNP was characterized by larger SOM and smaller organism C stocks compared to SCAMPS-CN, and a greater reduction in ecosystem C stocks under warming. This difference can largely be attributed to a smaller microbial biomass in the CNP model, which, instead of being driven by direct costs of P acquisition, was driven by variable resource limitation due to asynchronous C, N, and P availability and demand. Warming facilitated a greater relative increase in plant and microbial biomass in SCAMPS-CNP, however, facilitated by increased extracellular enzyme pools and activity, which more than offset the metabolic costs associated with their production. Although the microbial community was able to flexibly adapt its stoichiometry and become more bacteria-like (N-rich) in both models, its stoichiometry deviated further from its target value in the CNP model because of the need to balance cellular NP ratio. Our results indicate that seasonality and asynchrony in resources affect predicted changes in ecosystem C storage under warming in these models, and therefore build on a growing body of literature indicating stoichiometry should be considered in carbon cycling projections.This work was funded by the National Science Foundation Signals in the Soil grant number 1841610 to SAS and EBR

Distribution and Environmental Drivers of Fungal Denitrifiers in Global Soils

The microbial process of denitrification is the primary source of the greenhouse gas nitrous oxide (N2O) from terrestrial ecosystems. Fungal denitrifiers, unlike many bacteria, lack the N2O reductase, and thereby are sources of N2O. Still, their diversity, global distribution, and environmental determinants, as well as their relative importance, compared to bacterial and archaeal denitrifiers, remain unresolved. Employing a phylogenetically informed approach to analyze 1,980 global soil and rhizosphere metagenomes for the denitrification marker gene nirK, which codes for the copper dependent nitrite reductase in denitrification, we show that fungal denitrifiers are sparse, yet cosmopolitan and that they are dominated by saprotrophs and pathogens. Few showed biome-specific distribution patterns, although members of the Fusarium oxysporum species complex, which are known to produce substantial amounts of N2O, were proportionally more abundant and diverse in the rhizosphere than in other biomes. Fungal denitrifiers were most frequently detected in croplands, but they were most abundant in forest soils when normalized to metagenome size. Nevertheless, the overwhelming dominance of bacterial and archaeal denitrifiers suggests a much lower fungal contribution to N2O emissions than was previously estimated. In relative terms, they could play a role in soils that are characterized by a high carbon to nitrogen ratio and a low pH, especially in the tundra as well as in boreal and temperate coniferous forests. Because global warming predicts the proliferation of fungal pathogens, the prevalence of potential plant pathogens among fungal denitrifiers and the cosmopolitan distribution of these organisms suggest that fungal denitrifier abundance may increase in terrestrial ecosystems.IMPORTANCE Fungal denitrifiers, in contrast to their bacterial counterparts, are a poorly studied functional group within the nitrogen cycle, even though they produce the greenhouse gas N2O. To curb soil N2O emissions, a better understanding of their ecology and distribution in soils from different ecosystems is needed. Here, we probed a massive amount of DNA sequences and corresponding soil data from a large number of samples that represented the major soil environments for a broad understanding of fungal denitrifier diversity at the global scale. We show that fungal denitrifiers are predominantly cosmopolitan saprotrophs and opportunistic pathogens. Fungal denitrifiers constituted, on average, 1% of the total denitrifier community. This suggests that earlier estimations of fungal denitrifier abundance, and, thereby, it is also likely that the contributions of fungal denitrifiers to N2O emissions have been overestimated. Nevertheless, with many fungal denitrifiers being plant pathogens, they could become increasingly relevant, as soilborne pathogenic fungi are predicted to increase with ongoing climate change.Fungal denitrifiers, in contrast to their bacterial counterparts, are a poorly studied functional group within the nitrogen cycle, even though they produce the greenhouse gas N2O. To curb soil N2O emissions, a better understanding of their ecology and distribution in soils from different ecosystems is needed

Two decades of warming increases diversity of a potentially lignolytic bacterial community

As Earth\u27s climate warms, the massive stores of carbon found in soil are predicted to become depleted, and leave behind a smaller carbon pool that is less accessible to microbes. At a long-term forest soil-warming experiment in central Massachusetts, soil respiration and bacterial diversity have increased, while fungal biomass and microbially-accessible soil carbon have decreased. Here, we evaluate how warming has affected the microbial community\u27s capability to degrade chemically-complex soil carbon using lignin-amended BioSep beads. We profiled the bacterial and fungal communities using PCR-based methods and completed extracellular enzyme assays as a proxy for potential community function. We found that lignin-amended beads selected for a distinct community containing bacterial taxa closely related to known lignin degraders, as well as members of many genera not previously noted as capable of degrading lignin. Warming tended to drive bacterial community structure more strongly in the lignin beads, while the effect on the fungal community was limited to unamended beads. Of those bacterial operational taxonomic units (OTUs) enriched by the warming treatment, many were enriched uniquely on lignin-amended beads. These taxa may be contributing to enhanced soil respiration under warming despite reduced readily available C availability. In aggregate, these results suggest that there is genetic potential for chemically complex soil carbon degradation that may lead to extended elevated soil respiration with long-term warming

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