Decoupling of soil nutrient cycles as a function of aridity in global drylands.

The biogeochemical cycles of carbon (C), nitrogen (N) and phosphorus (P) are interlinked by primary production, respiration and decomposition in terrestrial ecosystems. It has been suggested that the C, N and P cycles could become uncoupled under rapid climate change because of the different degrees of control exerted on the supply of these elements by biological and geochemical processes. Climatic controls on biogeochemical cycles are particularly relevant in arid, semi-arid and dry sub-humid ecosystems (drylands) because their biological activity is mainly driven by water availability. The increase in aridity predicted for the twenty-first century in many drylands worldwide may therefore threaten the balance between these cycles, differentially affecting the availability of essential nutrients. Here we evaluate how aridity affects the balance between C, N and P in soils collected from 224 dryland sites from all continents except Antarctica. We find a negative effect of aridity on the concentration of soil organic C and total N, but a positive effect on the concentration of inorganic P. Aridity is negatively related to plant cover, which may favour the dominance of physical processes such as rock weathering, a major source of P to ecosystems, over biological processes that provide more C and N, such as litter decomposition. Our findings suggest that any predicted increase in aridity with climate change will probably reduce the concentrations of N and C in global drylands, but increase that of P. These changes would uncouple the C, N and P cycles in drylands and could negatively affect the provision of key services provided by these ecosystems.

Catalytic power of enzymes decreases with temperature: New insights for understanding soil C cycling and microbial ecology under warming.

Most current models of soil C dynamics predict that climate warming will accelerate soil C mineralization, resulting in a long-term CO2 release and positive feedback to global warming. However, ecosystem warming experiments show that CO2 loss from warmed soils declines to control levels within a few years. Here, we explore the temperature dependence of enzymatic conversion of polymerized soil organic C (SOC) into assimilable compounds, which is presumed the rate-limiting step of SOC mineralization. Combining literature review, modelling and enzyme assays, we studied the effect of temperature on activity of enzymes considering their thermal inactivation and catalytic activity. We defined the catalytic power of enzymes (Epower ) as the cumulative amount of degraded substrate by one unit of enzyme until its complete inactivation. We show a universal pattern of enzyme's thermodynamic properties: activation energy of catalytic activity (EAcat ) < activation energy of thermal inactivation (EAinact ). By investing in stable enzymes (high EAinact ) having high catalytic activity (low EAcat ), microorganisms may maximize the Epower of their enzymes. The counterpart of such EAs' hierarchical pattern is the higher relative temperature sensitivity of enzyme inactivation than catalysis, resulting in a reduction in Epower under warming. Our findings could explain the decrease with temperature in soil enzyme pools, microbial biomass (MB) and carbon use efficiency (CUE) reported in some warming experiments and studies monitoring the seasonal variation in soil enzymes. They also suggest that a decrease in soil enzyme pools due to their faster inactivation under warming contributes to the observed attenuation of warming effect on soil C mineralization. This testable theory predicts that the ultimate response of SOC degradation to warming can be positive or negative depending on the relative temperature response of Epower and microbial production of enzymes.

Soil carbon cycling proxies: Understanding their critical role in predicting climate change feedbacks.

The complexity of processes and interactions that drive soil C dynamics necessitate the use of proxy variables to represent soil characteristics that cannot be directly measured (correlative proxies), or that aggregate information about multiple soil characteristics into one variable (integrative proxies). These proxies have proven useful for understanding the soil C cycle, which is highly variable in both space and time, and are now being used to make predictions of the fate and persistence of C under future climate scenarios. However, the C pools and processes that proxies represent must be thoughtfully considered in order to minimize uncertainties in empirical understanding. This is necessary to capture the full value of a proxy in model parameters and in model outcomes. Here, we provide specific examples of proxy variables that could improve decision-making, and modeling skill, while also encouraging continued work on their mechanistic underpinnings. We explore the use of three common soil proxies used to study soil C cycling: metabolic quotient, clay content, and physical fractionation. We also consider how emerging data types, such as genome-sequence data, can serve as proxies for microbial community activities. By examining some broad assumptions in soil C cycling with the proxies already in use, we can develop new hypotheses and specify criteria for new and needed proxies.

Opposing effects of different soil organic matter fractions on crop yields.

Soil organic matter is critical to sustainable agriculture because it provides nutrients to crops as it decomposes and increases nutrient- and water-holding capacity when built up. Fast- and slow-cycling fractions of soil organic matter can have different impacts on crop production because fast-cycling fractions rapidly release nutrients for short-term plant growth and slow-cycling fractions bind nutrients that mineralize slowly and build up water-holding capacity. We explored the controls on these fractions in a tropical agroecosystem and their relationship to crop yields. We performed physical fractionation of soil organic matter from 48 farms and plots in western Kenya. We found that fast-cycling, particulate organic matter was positively related to crop yields, but did not have a strong effect, while slower-cycling, mineral-associated organic matter was negatively related to yields. Our finding that slower-cycling organic matter was negatively related to yield points to a need to revise the view that stabilization of organic matter positively impacts food security. Our results support a new paradigm that different soil organic matter fractions are controlled by different mechanisms, potentially leading to different relationships with management outcomes, like crop yield. Effectively managing soils for sustainable agriculture requires quantifying the effects of specific organic matter fractions on these outcomes.

Genomics in a changing arctic: critical questions await the molecular ecologist.

Molecular ecology is poised to tackle a host of interesting questions in the coming years. The Arctic provides a unique and rapidly changing environment with a suite of emerging research needs that can be addressed through genetics and genomics. Here we highlight recent research on boreal and tundra ecosystems and put forth a series of questions related to plant and microbial responses to climate change that can benefit from technologies and analytical approaches contained within the molecular ecologist's toolbox. These questions include understanding (i) the mechanisms of plant acquisition and uptake of N in cold soils, (ii) how these processes are mediated by root traits, (iii) the role played by the plant microbiome in cycling C and nutrients within high-latitude ecosystems and (iv) plant adaptation to extreme Arctic climates. We highlight how contributions can be made in these areas through studies that target model and nonmodel organisms and emphasize that the sequencing of the Populus and Salix genomes provides a valuable resource for scientific discoveries related to the plant microbiome and plant adaptation in the Arctic. Moreover, there exists an exciting role to play in model development, including incorporating genetic and evolutionary knowledge into ecosystem and Earth System Models. In this regard, the molecular ecologist provides a valuable perspective on plant genetics as a driver for community biodiversity, and how ecological and evolutionary forces govern community dynamics in a rapidly changing climate.

Climate change alters ecological strategies of soil bacteria.

The timing and magnitude of rainfall events are expected to change in future decades, resulting in longer drought periods and larger rainfall events. Although microbial community composition and function are both sensitive to changes in rainfall, it is unclear whether this is because taxa adopt strategies that maximise fitness under new regimes. We assessed whether bacteria exhibited phylogenetically conserved ecological strategies in response to drying-rewetting, and whether these strategies were altered by historical exposure to experimentally intensified rainfall patterns. By clustering relative abundance patterns, we identified three discrete ecological strategies and found that tolerance to drying-rewetting increased with exposure to intensified rainfall patterns. Changes in strategy were primarily due to changes in community composition, but also to strategy shifts within taxa. These moisture regime-selected ecological strategies may be predictable from disturbance history, and are likely to be linked to traits that influence the functional potential of microbial communities.

Rhizosphere stoichiometry: are C : N : P ratios of plants, soils, and enzymes conserved at the plant species-level?

As a consequence of the tight linkages among soils, plants and microbes inhabiting the rhizosphere, we hypothesized that soil nutrient and microbial stoichiometry would differ among plant species and be correlated within plant rhizospheres. We assessed plant tissue carbon (C) : nitrogen (N) : phosphorus (P) ratios for eight species representing four different plant functional groups in a semiarid grassland during near-peak biomass. Using intact plant species-specific rhizospheres, we examined soil C : N : P, microbial biomass C : N, and soil enzyme C : N : P nutrient acquisition activities. We found that few of the plant species' rhizospheres demonstrated distinct stoichiometric properties from other plant species and unvegetated soil. Plant tissue nutrient ratios and components of below-ground rhizosphere stoichiometry predominantly differed between the C4 plant species Buchloe dactyloides and the legume Astragalus laxmannii. The rhizospheres under the C4 grass B. dactyloides exhibited relatively higher microbial C and lower soil N, indicative of distinct soil organic matter (SOM) decomposition and nutrient mineralization activities. Assessing the ecological stoichiometry among plant species' rhizospheres is a high-resolution tool useful for linking plant community composition to below-ground soil microbial and nutrient characteristics. By identifying how rhizospheres differ among plant species, we can better assess how plant-microbial interactions associated with ecosystem-level processes may be influenced by plant community shifts.

Is bacterial moisture niche a good predictor of shifts in community composition under long-term drought?

Both biogeographical and rainfall manipulation studies show that soil water content can be a strong driver of microbial community composition. However, we do not yet know if these patterns emerge because certain bacterial taxa are better able to survive at dry soil moisture regimes or if they are due to other drought-sensitive ecosystem properties indirectly affecting microbial community composition. In this study, we evaluated (1) whether bacterial community composition changed under an 11-year drought manipulation and (2) whether shifts under drought could be explained by variation in the moisture sensitivity of growth among bacterial taxa (moisture niche partitioning). Using 454 pyrosequencing of 16S rRNA, we observed shifts in bacterial community composition under drought, coincident with changes in other soil properties. We wet-up dry soils from drought plots to five moisture levels, and measured respiration and the composition of actively growing communities using bromodeoxyuridine (BrdU) labeling of DNA. The field drought experiment affected the composition of the active community when incubated at different moisture levels in the laboratory, as well as short-term (36-hour) respiration rates. Independent of history, bacterial communities also displayed strong niche partitioning across the wet-up moisture gradient. Although this indicates that moisture has the potential to drive bacterial community composition under long-term drought, species distributions predicted by response to moisture did not reflect the community composition of plots that were subjected to long-term drought. Bacterial community structure was likely more strongly driven by other environmental factors that changed under long-term drought, or not shaped by response to water level upon wet-up. The approach that we present here for linking niches to community composition could be adapted for other environmental variables to aid in predicting microbial species distributions and community responses to environmental change.

Soil microbial and nutrient responses to 7 years of seasonally altered precipitation in a Chihuahuan Desert grassland.

Soil microbial communities in Chihuahuan Desert grasslands generally experience highly variable spatiotemporal rainfall patterns. Changes in precipitation regimes can affect belowground ecosystem processes such as decomposition and nutrient cycling by altering soil microbial community structure and function. The objective of this study was to determine if increased seasonal precipitation frequency and magnitude over a 7-year period would generate a persistent shift in microbial community characteristics and soil nutrient availability. We supplemented natural rainfall with large events (one/winter and three/summer) to simulate increased precipitation based on climate model predictions for this region. We observed a 2-year delay in microbial responses to supplemental precipitation treatments. In years 3-5, higher microbial biomass, arbuscular mycorrhizae abundance, and soil enzyme C and P acquisition activities were observed in the supplemental water plots even during extended drought periods. In years 5-7, available soil P was consistently lower in the watered plots compared to control plots. Shifts in soil P corresponded to higher fungal abundances, microbial C utilization activity, and soil pH. This study demonstrated that 25% shifts in seasonal rainfall can significantly influence soil microbial and nutrient properties, which in turn may have long-term effects on nutrient cycling and plant P uptake in this desert grassland.

Predicted responses of arctic and alpine ecosystems to altered seasonality under climate change.

Global climate change is already having significant impacts on arctic and alpine ecosystems, and ongoing increases in temperature and altered precipitation patterns will affect the strong seasonal patterns that characterize these temperature-limited systems. The length of the potential growing season in these tundra environments is increasing due to warmer temperatures and earlier spring snow melt. Here, we compare current and projected climate and ecological data from 20 Northern Hemisphere sites to identify how seasonal changes in the physical environment due to climate change will alter the seasonality of arctic and alpine ecosystems. We find that although arctic and alpine ecosystems appear similar under historical climate conditions, climate change will lead to divergent responses, particularly in the spring and fall shoulder seasons. As seasonality changes in the Arctic, plants will advance the timing of spring phenological events, which could increase plant nutrient uptake, production, and ecosystem carbon (C) gain. In alpine regions, photoperiod will constrain spring plant phenology, limiting the extent to which the growing season can lengthen, especially if decreased water availability from earlier snow melt and warmer summer temperatures lead to earlier senescence. The result could be a shorter growing season with decreased production and increased nutrient loss. These contrasting alpine and arctic ecosystem responses will have cascading effects on ecosystems, affecting community structure, biotic interactions, and biogeochemistry.

Positive climate feedbacks of soil microbial communities in a semi-arid grassland.

Soil microbial communities may be able to rapidly respond to changing environments in ways that change community structure and functioning, which could affect climate-carbon feedbacks. However, detecting microbial feedbacks to elevated CO(2) (eCO(2) ) or warming is hampered by concurrent changes in substrate availability and plant responses. Whether microbial communities can persistently feed back to climate change is still unknown. We overcame this problem by collecting microbial inocula at subfreezing conditions under eCO(2) and warming treatments in a semi-arid grassland field experiment. The inoculant was incubated in a sterilised soil medium at constant conditions for 30 days. Microbes from eCO(2) exhibited an increased ability to decompose soil organic matter (SOM) compared with those from ambient CO(2) plots, and microbes from warmed plots exhibited increased thermal sensitivity for respiration. Microbes from the combined eCO(2) and warming plots had consistently enhanced microbial decomposition activity and thermal sensitivity. These persistent positive feedbacks of soil microbial communities to eCO(2) and warming may therefore stimulate soil C loss.

Managing Agroecosystems for Soil Microbial Carbon Use Efficiency: Ecological Unknowns, Potential Outcomes, and a Path Forward.

Agricultural systems are increasingly managed for improving soil carbon (C) accumulation. However, there are limits to C returns in agricultural systems that constrain soil C accumulation capacity. Increasing the efficiency of how soil microbes process C is gaining interest as an important management strategy for increasing soil C and is a key feature of soil C dynamics in many new microbial-explicit models. A higher microbial C use efficiency (CUE) may increase C storage while reducing C system losses and is a fundamental trait affecting community assembly dynamics and nutrient cycling. However, the numerous ecological unknowns influencing CUE limit our ability to effectively manage CUE in agricultural soils for greater soil C storage. In this perspective, we consider three complex drivers of agroecosystem CUE that need to be resolved to develop effective C sequestration management practices in the future: (1) the environment as an individual trait moderator versus a filter, (2) microbial community competitive and faciliatory interactions, and (3) spatiotemporal dynamics through the soil profile and across the microbial lifecycle. We highlight ways that amendments, crop rotations, and tillage practices might affect microbial CUE conditions and the variable outcomes of these practices. We argue that to resolve some of the unknowns of CUE dynamics, we need to include more mechanistic, trait-based approaches that capitalize on advanced methods and innovative field research designs within an agroecosystem-specific context. By identifying the management-level determinants of CUE expression, we will be better positioned to optimize CUE to increase soil C storage in agricultural systems.

River channel connectivity shifts metabolite composition and dissolved organic matter chemistry.

Biogeochemical processing of dissolved organic matter (DOM) in headwater rivers regulates aquatic food web dynamics, water quality, and carbon storage. Although headwater rivers are critical sources of energy to downstream ecosystems, underlying mechanisms structuring DOM composition and reactivity are not well quantified. By pairing mass spectrometry and fluorescence spectroscopy, here we show that hydrology and river geomorphology interactively shape molecular patterns in DOM composition. River segments with a single channel flowing across the valley bottom export DOM with a similar chemical profile through time. In contrast, segments with multiple channels of flow store large volumes of water during peak flows, which they release downstream throughout the summer. As flows subside, losses of lateral floodplain connectivity significantly increase the heterogeneity of DOM exported downstream. By linking geomorphologic landscape-scale processes with microbial metabolism, we show DOM heterogeneity increases as a function of fluvial complexity, with implications for ecosystem function and watershed management.

Thermal adaptation of soil microbial respiration to elevated temperature.

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.

Stoichiometry of soil enzyme activity at global scale.

Extracellular enzymes are the proximate agents of organic matter decomposition and measures of these activities can be used as indicators of microbial nutrient demand. We conducted a global-scale meta-analysis of the seven-most widely measured soil enzyme activities, using data from 40 ecosystems. The activities of beta-1,4-glucosidase, cellobiohydrolase, beta-1,4-N-acetylglucosaminidase and phosphatase g(-1) soil increased with organic matter concentration; leucine aminopeptidase, phenol oxidase and peroxidase activities showed no relationship. All activities were significantly related to soil pH. Specific activities, i.e. activity g(-1) soil organic matter, also varied in relation to soil pH for all enzymes. Relationships with mean annual temperature (MAT) and precipitation (MAP) were generally weak. For hydrolases, ratios of specific C, N and P acquisition activities converged on 1 : 1 : 1 but across ecosystems, the ratio of C : P acquisition was inversely related to MAP and MAT while the ratio of C : N acquisition increased with MAP. Oxidative activities were more variable than hydrolytic activities and increased with soil pH. Our analyses indicate that the enzymatic potential for hydrolyzing the labile components of soil organic matter is tied to substrate availability, soil pH and the stoichiometry of microbial nutrient demand. The enzymatic potential for oxidizing the recalcitrant fractions of soil organic material, which is a proximate control on soil organic matter accumulation, is most strongly related to soil pH. These trends provide insight into the biogeochemical processes that create global patterns in ecological stoichiometry and organic matter storage.

Within-species trade-offs in plant-stimulated soil enzyme activity and growth, flowering, and seed size.

Soil microbial communities affect species demographic rates of plants. In turn, plants influence the composition and function of the soil microbiome, potentially resulting in beneficial feedbacks that alter their fitness and establishment. For example, differences in the ability to stimulate soil enzyme activity among plant lineages may affect plant growth and reproduction. We used a common garden study to test differences in plant-stimulated soil enzyme activity between lineages of the same species across developmental stages. Lineages employed different strategies whereby growth, days to flowering and seed size traded-off with plant-stimulated soil enzyme activity. Specifically, the smaller seeded lineage stimulated more enzyme activity at the early stage of development and flowered earlier while the larger seeded lineage sustained lower but consistent enzyme activity through development. We suggest that these lineages, which are both successful invaders, employ distinct strategies (a colonizer and a competitor) and differ in their influence on soil microbial activity. Synthesis. The ability to influence the soil microbial community by plants may be an important trait that trades off with growth, flowering, and seed size for promoting plant establishment, reproduction, and invasion.

Soil bacterial community responses to altered precipitation and temperature regimes in an old field grassland are mediated by plants.

The structure and function of soil microbiomes often change in response to experimental climate manipulations, suggesting an important role in ecosystem feedbacks. However, it is difficult to know if microbes are responding directly to environmental changes or are more strongly impacted by plant responses. We investigated soil microbial responses to precipitation and temperature manipulations at the Boston-Area Climate Experiment in Massachusetts, USA, in both vegetated and bare plots to parse direct vs. plant-mediated responses to multi-factor climate change. We assessed the bacterial community in vegetated soils in 2009, two years after the experiment was initiated, and bacterial and fungal community in vegetated and bare soils in 2011. The bacterial community structure was significantly changed by the treatments in vegetated soils. However, such changes in the bacterial community across the treatments were absent in the 2011 bare soils. These results suggest that the bacterial communities in vegetated soils were structured via plant community shifts in response to the abiotic manipulations. Co-variation between bacterial community structure and temperature sensitivities and stoichiometry of potential enzyme activities in the 2011 vegetated soils suggested a link between bacterial community structure and ecosystem function. This study emphasizes the importance of plant-soil-microbial interactions in mediating responses to future climate change.

Understanding how microbiomes influence the systems they inhabit.

Translating the ever-increasing wealth of information on microbiomes (environment, host or built environment) to advance our understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes that they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here, we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system-level processes that they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted using constituent taxa (community-aggregated traits) from those properties that cannot currently be predicted using constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these three categories of microbial characteristics and connect them with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.