Integrating microbial ecology into ecosystem models: challenges and priorities

Microbial communities can potentially mediate feedbacks between global change and ecosystem function, owing to their sensitivity to environmental change and their control over critical biogeochemical processes. Numerous ecosystem models have been developed to predict global change effects, but most do not consider microbial mechanisms in detail. In this idea paper, we examine the extent to which incorporation of microbial ecology into ecosystem models improves predictions of carbon (C) dynamics under warming, changes in precipitation regime, and anthropogenic nitrogen (N) enrichment. We focus on three cases in which this approach might be especially valuable: temporal dynamics in microbial responses to environmental change, variation in ecological function within microbial communities, and N effects on microbial activity. Four microbially-based models have addressed these scenarios. In each case, predictions of the microbial-based models differ—sometimes substantially—from comparable conventional models. However, validation and parameterization of model performance is challenging. We recommend that the development of microbial-based models must occur in conjunction with the development of theoretical frameworks that predict the temporal responses of microbial communities, the phylogenetic distribution of microbial functions, and the response of microbes to N enrichment

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe

Soil microorganisms are critical to ecosystem functioning and the maintenance of soil fertility. However, despite global increases in the inputs of nitrogen (N) and phosphorus (P) to ecosystems due to human activities, we lack a predictive understanding of how microbial communities respond to elevated nutrient inputs across environmental gradients. Here we used high-throughput sequencing of marker genes to elucidate the responses of soil fungal, archaeal, and bacterial communities using an N and P addition experiment replicated at 25 globally distributed grassland sites. We also sequenced metagenomes from a subset of the sites to determine how the functional attributes of bacterial communities change in response to elevated nutrients. Despite strong compositional differences across sites, microbial communities shifted in a consistent manner with N or P additions, and the magnitude of these shifts was related to the magnitude of plant community responses to nutrient inputs. Mycorrhizal fungi and methanogenic archaea decreased in relative abundance with nutrient additions, as did the relative abundances of oligotrophic bacterial taxa. The metagenomic data provided additional evidence for this shift in bacterial life history strategies because nutrient additions decreased the average genome sizes of the bacterial community members and elicited changes in the relative abundances of representative functional genes. Our results suggest that elevated N and P inputs lead to predictable shifts in the taxonomic and functional traits of soil microbial communities, including increases in the relative abundances of faster-growing, copiotrophic bacterial taxa, with these shifts likely to impact belowground ecosystems worldwide

Sensitivity of global soil carbon stocks to combined nutrient enrichment

Soil stores approximately twice as much carbon as the atmosphere and fluctuations in the size of the soil carbon pool directly influence climate conditions. We used the Nutrient Network global change experiment to examine how anthropogenic nutrient enrichment might influence grassland soil carbon storage at a global scale. In isolation, enrichment of nitrogen and phosphorous had minimal impacts on soil carbon storage. However, when these nutrients were added in combination with potassium and micronutrients, soil carbon stocks changed considerably, with an average increase of 0.04 KgCm−2 year−1 (standard deviation 0.18 KgCm−2 year−1). These effects did not correlate with changes in primary productivity, suggesting that soil carbon decomposition may have been restricted. Although nutrient enrichment caused soil carbon gains most dry, sandy regions, considerable absolute losses of soil carbon may occur in high‐latitude regions that store the majority of the world's soil carbon. These mechanistic insights into the sensitivity of grassland carbon stocks to nutrient enrichment can facilitate biochemical modelling efforts to project carbon cycling under future climate scenarios

Nitrogen Increases Early-Stage and Slows Late-Stage Decomposition Across Diverse Grasslands

To evaluate how increased anthropogenic nutrient inputs alter carbon cycling in grasslands, we conducted a litter decomposition study across 20 temperate grasslands on three continents within the Nutrient Network, a globally distributed nutrient enrichment experiment We determined the effects of addition of experimental nitrogen (N), phosphorus (P) and potassium plus micronutrient (Kμ) on decomposition of a common tree leaf litter in a long-term study (maximum of 7 years; exact deployment period varied across sites). The use of higher order decomposition models allowed us to distinguish between the effects of nutrients on early- versus late-stage decomposition. Across continents, the addition of N (but not other nutrients) accelerated early-stage decomposition and slowed late-stage decomposition, increasing the slowly decomposing fraction by 28% and the overall litter mean residence time by 58%. Synthesis. Using a novel, long-term cross-site experiment, we found widespread evidence that N enhances the early stages of above-ground plant litter decomposition across diverse and widespread temperate grassland sites but slows late-stage decomposition. These findings were corroborated by fitting the data to multiple decomposition models and have implications for N effects on soil organic matter formation. For example, following N enrichment, increased microbial processing of litter substrates early in decomposition could promote the production and transfer of low molecular weight compounds to soils and potentially enhance the stabilization of mineral-associated organic matter. By contrast, by slowing late-stage decomposition, N enrichment could promote particulate organic matter (POM) accumulation. Such hypotheses deserve further testing

Belowground biomass response to nutrient enrichment depends on light limitation across globally distributed grasslands

Anthropogenic activities are increasing nutrient inputs to ecosystems worldwide, with consequences for global carbon and nutrient cycles. Recent meta-analyses show that aboveground primary production is often co-limited by multiple nutrients; however, little is known about how root production responds to changes in nutrient availability. At twenty-nine grassland sites on four continents, we quantified shallow root biomass responses to nitrogen (N), phosphorus (P) and potassium plus micronutrient enrichment and compared below- and aboveground responses. We hypothesized that optimal allocation theory would predict context dependence in root biomass responses to nutrient enrichment, given variation among sites in the resources limiting to plant growth (specifically light versus nutrients). Consistent with the predictions of optimal allocation theory, the proportion of total biomass belowground declined with N or P addition, due to increased biomass aboveground (for N and P) and decreased biomass belowground (N, particularly in sites with low canopy light penetration). Absolute root biomass increased with N addition where light was abundant at the soil surface, but declined in sites where the grassland canopy intercepted a large proportion of incoming light. These results demonstrate that belowground responses to changes in resource supply can differ strongly from aboveground responses, which could significantly modify predictions of future rates of nutrient cycling and carbon sequestration. Our results also highlight how optimal allocation theory developed for individual plants may help predict belowground biomass responses to nutrient enrichment at the ecosystem scale across wide climatic and environmental gradients