Microbial nitrogen use efficiency (NUE) describes the partitioning of organic N taken up between growth and the release of inorganic N to the environment (that is, N mineralization), and is thus central to our understanding of N cycling. Here we report empirical evidence that microbial decomposer communities in soil and plant litter regulate their NUE. We find that microbes retain most immobilized organic N (high NUE), when they are N limited, resulting in low N mineralization. However, when the metabolic control of microbial decomposers switches from N to C limitation, they release an increasing fraction of organic N as ammonium (low NUE). We conclude that the regulation of NUE is an essential strategy of microbial communities to cope with resource imbalances, independent of the regulation of microbial carbon use efficiency, with significant effects on terrestrial N cycling.

Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant‐centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be ‘limited’ by nutrients or carbon alone. Here, we outline how models aimed at predicting non‐steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant–microbe interactions in coupled carbon and nutrient models.

Summary: Plants rapidly release photoassimilated carbon (C) to the soil via direct root exudation and associated mycorrhizal fungi, with both pathways promoting plant nutrient availability. This study aimed to explore these pathways from the root's vascular bundle to soil microbial communities. Using nanoscale secondary ion mass spectrometry (NanoSIMS) imaging and ¹³C‐phospho‐ and neutral lipid fatty acids, we traced in‐situ flows of recently photoassimilated C of ¹³CO₂‐exposed wheat (Triticum aestivum) through arbuscular mycorrhiza (AM) into root‐ and hyphae‐associated soil microbial communities. Intraradical hyphae of AM fungi were significantly ¹³C‐enriched compared to other root‐cortex areas after 8 h of labelling. Immature fine root areas close to the root tip, where AM features were absent, showed signs of passive C loss and co‐location of photoassimilates with nitrogen taken up from the soil solution. A significant and exclusively fresh proportion of ¹³C‐photosynthates was delivered through the AM pathway and was utilised by different microbial groups compared to C directly released by roots. Our results indicate that a major release of recent photosynthates into soil leave plant roots via AM intraradical hyphae already upstream of passive root exudations. AM fungi may act as a rapid hub for translocating fresh plant C to soil microbes.

• Plant seasonal cycles alter carbon (C) and nitrogen (N) availability for soil microbes, which may affect microbial community composition and thus feed back on microbial decomposition of soil organic material and plant N availability. The temporal dynamics of these plant–soil interactions are, however, unclear. • Here, we experimentally manipulated the C and N availability in a beech forest through N fertilization or tree girdling and conducted a detailed analysis of the seasonal pattern of microbial community composition and decomposition processes over 2 yr. • We found a strong relationship between microbial community composition and enzyme activities over the seasonal course. Phenoloxidase and peroxidase activities were highest during late summer, whereas cellulase and protease peaked in late autumn. Girdling, and thus loss of mycorrhiza, resulted in an increase in soil organic matter-degrading enzymes and a decrease in cellulase and protease activity. • Temporal changes in enzyme activities suggest a switch of the main substrate for decomposition between summer (soil organic matter) and autumn (plant litter). Our results indicate that ectomycorrhizal fungi are possibly involved in autumn cellulase and protease activity. Our study shows that, through belowground C allocation, trees significantly alter soil microbial communities, which may affect seasonal patterns of decomposition processes.

Summary: Drought affects plants and soil microorganisms, but it is still not clear how it alters the carbon (C) transfer at the plant–microbial interface. Here, we tested direct and indirect effects of drought on soil microbes and microbial turnover of recent plant‐derived C in a mountain meadow. Microbial community composition was assessed using phospholipid fatty acids (PLFAs); the allocation of recent plant‐derived C to microbial groups was analysed by pulse‐labelling of canopy sections with ¹³CO₂ and the subsequent tracing of the label into microbial PLFAs. Microbial biomass was significantly higher in plots exposed to a severe experimental drought. In addition, drought induced a shift of the microbial community composition, mainly driven by an increase of Gram‐positive bacteria. Drought reduced belowground C allocation, but not the transfer of recently plant‐assimilated C to fungi, and in particular reduced tracer uptake by bacteria. This was accompanied by an increase of ¹³C in the extractable organic C pool during drought, which was even more pronounced after plots were mown. We conclude that drought weakened the link between plant and bacterial, but not fungal, C turnover, and facilitated the growth of potentially slow‐growing, drought‐adapted soil microbes, such as Gram‐positive bacteria.

Global terrestrial models currently predict that the Amazon rainforest will continue to act as a carbon sink in the future, primarily owing to the rising atmospheric carbon dioxide (CO₂) concentration. Soil phosphorus impoverishment in parts of the Amazon basin largely controls its functioning, but the role of phosphorus availability has not been considered in global model ensembles—for example, during the Fifth Climate Model Intercomparison Project. Here we simulate the planned free-air CO₂ enrichment experiment AmazonFACE with an ensemble of 14 terrestrial ecosystem models. We show that phosphorus availability reduces the projected CO₂-induced biomass carbon growth by about 50% to 79 ± 63 g C m⁻² yr⁻¹ over 15 years compared to estimates from carbon and carbon–nitrogen models. Our results suggest that the resilience of the region to climate change may be much less than previously assumed. Variation in the biomass carbon response among the phosphorus-enabled models is considerable, ranging from 5 to 140 g C m⁻² yr⁻¹, owing to the contrasting plant phosphorus use and acquisition strategies considered among the models. The Amazon forest response thus depends on the interactions and relative contributions of the phosphorus acquisition and use strategies across individuals, and to what extent these processes can be upregulated under elevated CO₂.