Stephanie N. Kivlin

A framework for representing microbial decomposition in coupled climate models

Accurate prediction of future atmospheric CO2 concentrations is essential for evaluating climate change impacts on ecosystems and human societies. One major source of uncertainty in model predictions is the extent to which global warming will increase atmospheric CO2 concentrations through enhanced microbial decomposition of soil organic carbon. Recent advances in microbial ecology could help reduce this uncertainty, but current global models do not represent direct microbial control over decomposition. Instead, all of the coupled climate models reviewed in the most recent Intergovernmental Panel on Climate Change (IPCC) report assume that decomposition is a first-order decay process, proportional to the size of the soil carbon pool. Here we argue for the development of a new generation of models that link decomposition directly to the size and activity of microbial communities in coupled global models. This process begins with the formulation and validation of fine-scale models that capture fundamental microbial mechanisms without excessive mathematical complexity. These mechanistic models must then be scaled up through an aggregation process and validated at ecosystem to global scales prior to incorporation into global climate models (GCMs). Parameterizing microbial models at the global scale is challenging because some microbial properties such as in situ extracellular enzyme activities are very difficult to measure directly. New parameter fitting procedures may therefore be needed to infer the values of important microbial variables. Validating decomposition models at the global scale is also a challenge, and has not yet been accomplished with the land carbon models embedded in current GCMs. Fortunately new global datasets on soil carbon stocks and fluxes offer promising opportunities to validate both existing land carbon models and new microbial models. If challenges in scaling, parameterization, and validation can be overcome, a new generation of microbially-based decomposition models could substantially improve predictions of carbon–climate feedbacks in the Earth system. Development of new models structures would also reduce any bias due to the assumption of first-order decomposition across all of the models currently referenced in reports of the IPCC.

Fungal symbionts alter plant responses to global change

While direct plant responses to global change have been well characterized, indirect plant responses to global change, via altered species interactions, have received less attention. Here, we examined how plants associated with four classes of fungal symbionts (class I leaf endophytes [EF], arbuscular mycorrhizal fungi [AMF], ectomycorrhizal fungi [ECM], and dark septate endophytes [DSE]) responded to four global change factors (enriched CO2, drought, N deposition, and warming). We performed a meta-analysis of 434 studies spanning 174 publications to search for generalizable trends in responses of plant-fungal symbioses to future environments. Specifically, we addressed the following questions: (1) Can fungal symbionts ameliorate responses of plants to global change? (2) Do fungal symbiont groups differ in the degree to which they modify plant response to global change? (3) Do particular global change factors affect plant-fungal symbioses more than others? In all global change scenarios, except elevated CO2, fungal symbionts significantly altered plant responses to global change. In most cases, fungal symbionts increased plant biomass in response to global change. However, increased N deposition reduced the benefits of symbiosis. Of the global change factors we considered, drought and N deposition resulted in the strongest fungal mediation of plant responses. Our analysis highlighted gaps in current knowledge for responses of particular fungal groups and revealed the importance of considering not only the nonadditive effects of multiple global change factors, but also the interactive effects of multiple fungal symbioses. Our results show that considering plant-fungal symbioses is critical to predicting ecosystem response to global change.

Fungal Symbionts Alter Plant Drought Response

Grassland productivity is often primarily limited by water availability, and therefore, grasslands may be especially sensitive to climate change. Fungal symbionts can mediate plant drought response by enhancing drought tolerance and avoidance, but these effects have not been quantified across grass species. We performed a factorial meta-analysis of previously published studies to determine how arbuscular mycorrhizal (AM) fungi and endophytic fungal symbionts affect growth of grasses under drought. We then examined how the effect of fungal symbionts on plant growth was influenced by biotic (plant photosynthetic pathway) and abiotic (level of drought) factors. We also measured the phylogenetic signal of fungal symbionts on grass growth under control and drought conditions. Under drought conditions, grasses colonized by AM fungi grew larger than those without mycorrhizal symbionts. The increased growth of grasses conferred from fungal symbionts was greatest at the lowest soil moisture levels. Furthermore, under both drought and control conditions, C3 grasses colonized by AM fungi grew larger than C3 grasses without symbionts, but the biomass of C4 grasses was not affected by AM fungi. Endophytes did not increase plant biomass overall under any treatment. However, there was a phylogenetically conserved increase in plant biomass in grasses colonized by endophytes. Grasses and their fungal symbionts seem to interact within a context-dependent symbiosis, varying with biotic and abiotic conditions. Because plant–fungal symbioses significantly alter plant drought response, including these responses could improve our ability to predict grassland functioning under global change.

Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment

Evolutionary trade-offs among ecological traits are one mechanism that could determine the responses of functional groups of decomposers to global changes such as nitrogen (N) enrichment. We hypothesised that bacteria targeting recalcitrant carbon compounds require relatively high levels of N availability to support the construction costs of requisite extracellular and transport enzymes. Indeed, we found that taxa that used more recalcitrant (i.e. larger and cyclic) carbon compounds were more prevalent in ocean waters with higher nitrate concentrations. Compared to recalcitrant carbon users, labile carbon users targeted more organic N compounds, were found in relatively nitrate-poor waters, and were more common in higher latitude soils, which is consistent with the paradigm that N-limitation is stronger at higher latitudes. Altogether, evolutionary trade-offs may limit recalcitrant carbon users to habitats with higher N availability.

Differentiating between effects of invasion and diversity: impacts of aboveground plant communities on belowground fungal communities

Exotic plant species can affect soil microbial communities with the potential for community and ecosystem feedbacks. Yet, separating the effects of exotics from confounded changes in plant community diversity still remains a challenge. We focused on how plant diversity and native or exotic life history affected root fungi because of their significant roles in community and ecosystem processes. Specifically, we examined how fungi colonizing plant roots were affected by plant richness (one, two or four species) replicated across a range of plant community mixtures (natives, exotics, native-exotic mixtures). Fungal biomass inside roots was affected independently by plant richness and mixture, while root fungal community composition was affected only by plant richness. Extraradical networks also increased in size with plant richness. By contrast, plant biomass was a function of plant mixture, with natives consistently smaller than exotics and native-exotic mixtures intermediate. Plant invasions may have an impact on the belowground community primarily through their effects on diversity, at least in the short-term. Disentangling the effects of diversity and invasion on belowground microbial communities can help us to understand both the controllers of belowground resilience and mechanisms of successful colonization and spread of exotic plants.

Responses of high-altitude graminoids and soil fungi to 20 years of experimental warming

High-elevation ecosystems are expected to be particularly sensitive to climate warming because cold temperatures constrain biological processes. Deeper understanding of the consequences of climate change will come from studies that consider not only the direct effects of temperature on individual species, but also the indirect effects of altered species interactions. Here we show that 20 years of experimental warming has changed the species composition of graminoid (grass and sedge) assemblages in a subalpine meadow of the Rocky Mountains, USA, by increasing the frequency of sedges and reducing the frequency of grasses. Because sedges typically have weak interactions with mycorrhizal fungi relative to grasses, lowered abundances of arbuscular mycorrhizal (AM) fungi or other root-inhabiting fungi could underlie warming-induced shifts in plant species composition. However, warming increased root colonization by AM fungi for two grass species, possibly because AM fungi can enhance plant water uptake when soils are dried by experimental warming. Warming had no effect on AM fungal colonization of three other graminoids. Increased AM fungal colonization of the dominant shrub Artemisia tridentata provided further grounds for rejecting the hypothesis that reduced AM fungi caused the shift from grasses to sedges. Non-AM fungi (including dark septate endophytes) also showed general increases with warming. Our results demonstrate that lumping grasses and sedges when characterizing plant community responses can mask significant shifts in the responses of primary producers, and their symbiotic fungi, to climate change.

Historical climate controls soil respiration responses to current soil moisture

Significance Ecosystems’ feedback to climate change remains a source of uncertainty in global models that project future climate conditions. That uncertainty rests largely on how much soil carbon will be lost as microbial respiration and how that loss varies across ecosystems. Although there has been a large emphasis on microbial temperature responses, how soil microorganisms respond to changes in moisture remains poorly understood. Here we show that historical rainfall controls soil respiration responses to current moisture. This finding was robust, with historical climate repeatedly limiting current respiration regardless of alterations to soil moisture, rainfall, or the arrival of new taxa. This study highlights the importance that legacies in microbial responses to climate change can have in future ecosystem responses. Ecosystem carbon losses from soil microbial respiration are a key component of global carbon cycling, resulting in the transfer of 40–70 Pg carbon from soil to the atmosphere each year. Because these microbial processes can feed back to climate change, understanding respiration responses to environmental factors is necessary for improved projections. We focus on respiration responses to soil moisture, which remain unresolved in ecosystem models. A common assumption of large-scale models is that soil microorganisms respond to moisture in the same way, regardless of location or climate. Here, we show that soil respiration is constrained by historical climate. We find that historical rainfall controls both the moisture dependence and sensitivity of respiration. Moisture sensitivity, defined as the slope of respiration vs. moisture, increased fourfold across a 480-mm rainfall gradient, resulting in twofold greater carbon loss on average in historically wetter soils compared with historically drier soils. The respiration–moisture relationship was resistant to environmental change in field common gardens and field rainfall manipulations, supporting a persistent effect of historical climate on microbial respiration. Based on these results, predicting future carbon cycling with climate change will require an understanding of the spatial variation and temporal lags in microbial responses created by historical rainfall.

Tree species, spatial heterogeneity, and seasonality drive soil fungal abundance, richness, and composition in Neotropical rainforests

Tropical ecosystems remain poorly understood and this is particularly true for belowground soil fungi. Soil fungi may respond to plant identity when, for example, plants differentially allocate resources belowground. However, spatial and temporal heterogeneity in factors such as plant inputs, moisture, or nutrients can also affect fungal communities and obscure our ability to detect plant effects in single time point studies or within diverse forests. To address this, we sampled replicated monocultures of four tree species and secondary forest controls sampled in the drier and wetter seasons over 2 years. Fungal community composition was primarily related to vegetation type and spatial heterogeneity in the effects of vegetation type, with increasing divergence partly reflecting greater differences in soil pH and soil moisture. Across wetter versus drier dates, fungi were 7% less diverse, but up to four-fold more abundant. The combined effects of tree species and seasonality suggest that predicted losses of tropical tree diversity and intensification of drought have the potential to cascade belowground to affect both diversity and abundance of tropical soil fungi.

Temporal and Spatial Variation of Soil Bacteria Richness, Composition, and Function in a Neotropical Rainforest

The high diversity of tree species has traditionally been considered an important controller of belowground processes in tropical rainforests. However, soil water availability and resources are also primary regulators of soil bacteria in many ecosystems. Separating the effects of these biotic and abiotic factors in the tropics is challenging because of their high spatial and temporal heterogeneity. To determine the drivers of tropical soil bacteria, we examined tree species effects using experimental tree monocultures and secondary forests at La Selva Biological Station in Costa Rica. A randomized block design captured spatial variation and we sampled at four dates across two years to assess temporal variation. We measured bacteria richness, phylogenetic diversity, community composition, biomass, and functional potential. All bacteria parameters varied significantly across dates. In addition, bacteria richness and phylogenetic diversity were affected by the interaction of vegetation type and date, whereas bacteria community composition was affected by the interaction of vegetation type and block. Shifts in bacteria community richness and composition were unrelated to shifts in enzyme function, suggesting physiological overlap among taxa. Based on the observed temporal and spatial heterogeneity, our understanding of tropical soil bacteria will benefit from additional work to determine the optimal temporal and spatial scales for sampling. Understanding spatial and temporal variation will facilitate prediction of how tropical soil microbes will respond to future environmental change.

Tradeoffs in microbial carbon allocation may mediate soil carbon storage in future climates

Climate-induced changes in soil microbial physiology impact ecosystem carbon (C) storage and alter the rate of CO2 flux from soils to the atmosphere (Allison et al., 2010). The direction and magnitude of these microbial feedbacks depend on changes in saprotrophic bacterial and fungal C allocation in response to altered temperature, precipitation, and nutrient availability. Soil microbes may differentially allocate C in changing environments by altering processes such as enzyme production, C use efficiency (CUE), or biomass stoichiometry (Figure ​(Figure1).1). However, because these mechanisms may operate simultaneously and interact, microbial physiological feedbacks on soil C storage are difficult to predict. For example, initial increases in microbial CUE or biomass C:N may be counteracted by increases in enzyme production to acquire limiting organic nutrients. Figure 1 Three mechanisms through which microorganisms can shift C allocation: (A) extracellular enzyme activities, (B) carbon use efficiency, or (C) biomass stoichiometry. Each of these pathways can alter C storage in soils. Trend lines indicate expected responses ... Few studies have standardized microbial process rates, such as extracellular enzyme production or respiration, to the size of the microbial biomass. Examining process rates alone may obscure the microbial physiological mechanisms that underlie climate-induced changes in soil C cycling, leading to contradictory patterns among different studies. For instance, in a large-scale survey of soil protease activities from climate manipulations, drier and warmer conditions resulted in lower extracellular enzyme activities (EEA) compared to ambient conditions (Brzostek et al., 2012). In contrast, drier soils have also been found to stabilize extracellular enzymes in water films, reducing enzyme turnover rates and increasing potential activities (Lawrence et al., 2009; German et al., 2012).