Temperature and pH mediate stoichiometric constraints of organically derived soil nutrients.

It remains unclear how warming will affect resource flows during soil organic matter (SOM) decomposition, in part due to uncertainty in how exoenzymes produced by microbes and roots will function. Rising temperatures can enhance the activity of most exoenzymes, but soil pH can impose limitations on their catalytic efficiency. The effects of temperature and pH on enzyme activity are often examined in environmental samples, but purified enzyme kinetics reveal fundamental attributes of enzymes' intrinsic temperature responses and how relative release of decay-liberated resources (their flow ratios) can change with environmental conditions. In this paper, we illuminate the principle that fundamental, biochemical limitations on SOM release of C, N, and P during decay, and differential exoenzymes' responses to the environment, can exert biosphere-scale significance on the stoichiometry of bioavailable soil resources. To that end, we combined previously published intrinsic temperature sensitivities of two hydrolytic enzymes that release C and N during decay with a novel data set characterizing the kinetics of a P-releasing enzyme (acid phosphatase) across an ecologically relevant pH gradient. We use these data to estimate potential change in the flow ratios derived from these three enzymes' activities (C:N, C:P, and N:P) at the global scale by the end of the century, based on temperature projections and soil pH distribution. Our results highlight how the temperature sensitivity of these hydrolytic enzymes and the influence of pH on that sensitivity can govern the relative availability of bioavailable resources derived from these enzymes. The work illuminates the utility of weaving well-defined kinetic constraints of microbes' exoenzymes into models that incorporate changing SOM inputs and composition, nutrient availability, and microbial functioning into their efforts to project terrestrial ecosystem functioning in a changing climate.

Microbial inputs at the litter layer translate climate into altered organic matter properties.

Plant litter chemistry is altered during decomposition but it remains unknown if these alterations, and thus the composition of residual litter, will change in response to climate. Selective microbial mineralization of litter components and the accumulation of microbial necromass can drive litter compositional change, but the extent to which these mechanisms respond to climate remains poorly understood. We addressed this knowledge gap by studying needle litter decomposition along a boreal forest climate transect. Specifically, we investigated how the composition and/or metabolism of the decomposer community varies with climate, and if that variation is associated with distinct modifications of litter chemistry during decomposition. We analyzed the composition of microbial phospholipid fatty acids (PLFAs) in the litter layer and measured natural abundance δ13 CPLFA values as an integrated measure of microbial metabolisms. Changes in litter chemistry and δ13 C values were measured in litterbag experiments conducted at each transect site. A warmer climate was associated with higher litter nitrogen concentrations as well as altered microbial community structure (lower fungi:bacteria ratios) and microbial metabolism (higher δ13 CPLFA ). Litter in warmer transect regions accumulated less aliphatic-C (lipids, waxes) and retained more O-alkyl-C (carbohydrates), consistent with enhanced 13 C-enrichment in residual litter, than in colder regions. These results suggest that chemical changes during litter decomposition will change with climate, driven primarily by indirect climate effects (e.g., greater nitrogen availability and decreased fungi:bacteria ratios) rather than direct temperature effects. A positive correlation between microbial biomass δ13 C values and 13 C-enrichment during decomposition suggests that change in litter chemistry is driven more by distinct microbial necromass inputs than differences in the selective removal of litter components. Our study highlights the role that microbial inputs during early litter decomposition can play in shaping surface litter contribution to soil organic matter as it responds to climate warming effects such as greater nitrogen availability.

Ecological and Genomic Attributes of Novel Bacterial Taxa That Thrive in Subsurface Soil Horizons.

While most bacterial and archaeal taxa living in surface soils remain undescribed, this problem is exacerbated in deeper soils, owing to the unique oligotrophic conditions found in the subsurface. Additionally, previous studies of soil microbiomes have focused almost exclusively on surface soils, even though the microbes living in deeper soils also play critical roles in a wide range of biogeochemical processes. We examined soils collected from 20 distinct profiles across the United States to characterize the bacterial and archaeal communities that live in subsurface soils and to determine whether there are consistent changes in soil microbial communities with depth across a wide range of soil and environmental conditions. We found that bacterial and archaeal diversity generally decreased with depth, as did the degree of similarity of microbial communities to those found in surface horizons. We observed five phyla that consistently increased in relative abundance with depth across our soil profiles: Chloroflexi, Nitrospirae, Euryarchaeota, and candidate phyla GAL15 and Dormibacteraeota (formerly AD3). Leveraging the unusually high abundance of Dormibacteraeota at depth, we assembled genomes representative of this candidate phylum and identified traits that are likely to be beneficial in low-nutrient environments, including the synthesis and storage of carbohydrates, the potential to use carbon monoxide (CO) as a supplemental energy source, and the ability to form spores. Together these attributes likely allow members of the candidate phylum Dormibacteraeota to flourish in deeper soils and provide insight into the survival and growth strategies employed by the microbes that thrive in oligotrophic soil environments.IMPORTANCE Soil profiles are rarely homogeneous. Resource availability and microbial abundances typically decrease with soil depth, but microbes found in deeper horizons are still important components of terrestrial ecosystems. By studying 20 soil profiles across the United States, we documented consistent changes in soil bacterial and archaeal communities with depth. Deeper soils harbored communities distinct from those of the more commonly studied surface horizons. Most notably, we found that the candidate phylum Dormibacteraeota (formerly AD3) was often dominant in subsurface soils, and we used genomes from uncultivated members of this group to identify why these taxa are able to thrive in such resource-limited environments. Simply digging deeper into soil can reveal a surprising number of novel microbes with unique adaptations to oligotrophic subsurface conditions.

Temperature sensitivity of biomass-specific microbial exo-enzyme activities and CO2 efflux is resistant to change across short- and long-term timescales.

Accurate representation of temperature sensitivity (Q10 ) of soil microbial activity across time is critical for projecting soil CO2 efflux. As microorganisms mediate soil carbon (C) loss via exo-enzyme activity and respiration, we explore temperature sensitivities of microbial exo-enzyme activity and respiratory CO2 loss across time and assess mechanisms associated with these potential changes in microbial temperature responses. We collected soils along a latitudinal boreal forest transect with different temperature regimes (long-term timescale) and exposed these soils to laboratory temperature manipulations at 5, 15, and 25°C for 84 days (short-term timescale). We quantified temperature sensitivity of microbial activity per g soil and per g microbial biomass at days 9, 34, 55, and 84, and determined bacterial and fungal community structure before the incubation and at days 9 and 84. All biomass-specific rates exhibited temperature sensitivities resistant to change across short- and long-term timescales (mean Q10  = 2.77 ± 0.25, 2.63 ± 0.26, 1.78 ± 0.26, 2.27 ± 0.25, 3.28 ± 0.44, 2.89 ± 0.55 for ß-glucosidase, N-acetyl-ß-d-glucosaminidase, leucine amino peptidase, acid phosphatase, cellobiohydrolase, and CO2 efflux, respectively). In contrast, temperature sensitivity of soil mass-specific rates exhibited either resilience (the Q10 value changed and returned to the original value over time) or resistance to change. Regardless of the microbial flux responses, bacterial and fungal community structure was susceptible to change with temperature, significantly differing with short- and long-term exposure to different temperature regimes. Our results highlight that temperature responses of microbial resource allocation to exo-enzyme production and associated respiratory CO2 loss per unit biomass can remain invariant across time, and thus, that vulnerability of soil organic C stocks to rising temperatures may persist in the long term. Furthermore, resistant temperature sensitivities of biomass-specific rates in spite of different community structures imply decoupling of community constituents and the temperature responses of soil microbial activities.

Carbon Availability Modifies Temperature Responses of Heterotrophic Microbial Respiration, Carbon Uptake Affinity, and Stable Carbon Isotope Discrimination.

Microbial transformations of organic carbon (OC) generate a large flux of CO2 into the atmosphere and influence the C balance of terrestrial and aquatic ecosystems. Yet, inherent heterogeneity in natural environments precludes direct quantification of multiple microbial C fluxes that underlie CO2 production. Here we used a continuous flow bioreactor coupled with a stable C isotope analyzer to determine the effects of temperature and C availability (cellobiose concentration) on C fluxes and 13C discrimination of a microbial population growing at steady-state in a homogeneous, well-mixed environment. We estimated C uptake affinity and C use efficiency (CUE) to characterize the physiological responses of microbes to changing environmental conditions. Temperature increased biomass-C specific respiration rate and C uptake affinity at lower C availability, but did not influence those parameters at higher C availability. CUE decreased non-linearly with increasing temperature. The non-linear, negative relationship between CUE and temperature was more pronounced under lower C availability than under relatively high C availability. We observed stable isotope fractionation between C substrate and microbial biomass C (7~12‰ depletion), and between microbial biomass and respired CO2 (4~10‰ depletion). Microbial discrimination against 13C-containing cellobiose during C uptake was influenced by temperature and C availability, while discrimination during respiration was only influenced by C availability. Shifts in C uptake affinity with temperature and C availability may have modified uptake-induced 13C fractionation. By stressing the importance of C availability on temperature responses of microbial C fluxes, C uptake affinity, CUE, and isotopic fractionation, this study contributes to a fundamental understanding of C flow through microbes. This will help guide parameterization of microbial responses to varying temperature and C availability within Earth-system models.

'One physical system': Tansley's ecosystem as Earth's critical zone.

Integrative concepts of the biosphere, ecosystem, biogeocenosis and, recently, Earth's critical zone embrace scientific disciplines that link matter, energy and organisms in a systems-level understanding of our remarkable planet. Here, we assert the congruence of Tansley's (1935) venerable ecosystem concept of 'one physical system' with Earth science's critical zone. Ecosystems and critical zones are congruent across spatial-temporal scales from vegetation-clad weathering profiles and hillslopes, small catchments, landscapes, river basins, continents, to Earth's whole terrestrial surface. What may be less obvious is congruence in the vertical dimension. We use ecosystem metabolism to argue that full accounting of photosynthetically fixed carbon includes respiratory CO2 and carbonic acid that propagate to the base of the critical zone itself. Although a small fraction of respiration, the downward diffusion of CO2 helps determine rates of soil formation and, ultimately, ecosystem evolution and resilience. Because life in the upper portions of terrestrial ecosystems significantly affects biogeochemistry throughout weathering profiles, the lower boundaries of most terrestrial ecosystems have been demarcated at depths too shallow to permit a complete understanding of ecosystem structure and function. Opportunities abound to explore connections between upper and lower components of critical-zone ecosystems, between soils and streams in watersheds, and between plant-derived CO2 and deep microbial communities and mineral weathering.

How interactions between microbial resource demands, soil organic matter stoichiometry, and substrate reactivity determine the direction and magnitude of soil respiratory responses to warming.

Recent empirical and theoretical advances inform us about multiple drivers of soil organic matter (SOM) decomposition and microbial responses to warming. Absent from our conceptual framework of how soil respiration will respond to warming are adequate links between microbial resource demands, kinetic theory, and substrate stoichiometry. Here, we describe two important concepts either insufficiently explored in current investigations of SOM responses to temperature, or not yet addressed. First, we describe the complete range of responses for how warming may change microbial resource demands, physiology, community structure, and total biomass. Second, we describe how any relationship between SOM activation energy of decay and carbon (C) and nitrogen (N) stoichiometry can alter the relative availability of C and N as temperature changes. Changing availabilities of C and N liberated from their organic precursors can feedback to microbial resource demands, which in turn influence the aggregated respiratory response to temperature we observe. An unsuspecting biogeochemist focused primarily on temperature sensitivity of substrate decay thus cannot make accurate projections of heterotrophic CO2 losses from diverse organic matter reservoirs in a warming world. We establish the linkages between enzyme kinetics, SOM characteristics, and potential for microbial adaptation critical for making such projections. By examining how changing microbial needs interact with inherent SOM structure and composition, and thus reactivity, we demonstrate the means by which increasing temperature could result in increasing, unchanging, or even decreasing respiration rates observed in soils. We use this exercise to highlight ideas for future research that will develop our abilities to predict SOM feedbacks to climate.

Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2.

The earth's future climate state is highly dependent upon changes in terrestrial C storage in response to rising concentrations of atmospheric CO2. Here we show that consistently enhanced rates of net primary production (NPP) are sustained by a C-cascade through the root-microbe-soil system; increases in the flux of C belowground under elevated CO2 stimulated microbial activity, accelerated the rate of soil organic matter decomposition and stimulated tree uptake of N bound to this SOM. This process set into motion a positive feedback maintaining greater C gain under elevated CO2 as a result of increases in canopy N content and higher photosynthetic N-use efficiency. The ecosystem-level consequence of the enhanced requirement for N and the exchange of plant C for N belowground is the dominance of C storage in tree biomass but the preclusion of a large C sink in the soil.

The ecology of algal biodiesel production.

Sustainable energy production represents one of the most formidable problems of the 21st century, and plant-based biofuels offer significant promise. We summarize the potential advantages of using pond-grown microalgae as feedstocks relative to conventional terrestrial biofuel crop production. We show how pond-based algal biofuel production, which requires significantly less land area than agricultural crop-based biofuel systems, can offer additional ecological benefits by reducing anthropogenic pollutant releases to the environment and by requiring much lower water subsidies. We also demonstrate how key principles drawn from the science of ecology can be used to design efficient pond-based microalgal systems for the production of biodiesel fuels.