A review of the importance of mineral nitrogen cycling in the plant-soil-microbe system of permafrost-affected soils – changing the paradigm

The paradigm that permafrost-affected soils show restricted mineral nitrogen (N) cycling in favor of organic N compounds is based on the observation that net N mineralization rates in these cold climates are negligible. However, we find here that this perception is wrong. By synthesizing published data on N cycling in the plant-soil-microbe system of permafrost ecosystems we show that gross ammonification and nitrification rates in active layers were of similar magnitude and showed a similar dependence on soil organic carbon (SOC) and total nitrogen (TN) concentrations as observed in temperate and tropical systems. Moreover, high protein depolymerization rates and only marginal effects of C:N stoichiometry on gross N turnover provided little evidence for N limitation. Instead, the rather short period when soils are not frozen is the single main factor limiting N turnover. High gross rates of mineral N cycling are thus facilitated by released protection of organic matter in active layers with nitrification gaining particular importance in N-rich soils, such as organic soils without vegetation. Our finding that permafrost-affected soils show vigorous N cycling activity is confirmed by the rich functional microbial community which can be found both in active and permafrost layers. The high rates of N cycling and soil N availability are supported by biological N fixation, while atmospheric N deposition in the Arctic still is marginal except for fire-affected areas. In line with high soil mineral N production, recent plant physiological research indicates a higher importance of mineral plant N nutrition than previously thought. Our synthesis shows that mineral N production and turnover rates in active layers of permafrost-affected soils do not generally differ from those observed in temperate or tropical soils. We therefore suggest to adjust the permafrost N cycle paradigm, assigning a generally important role to mineral N cycling. This new paradigm suggests larger permafrost N climate feedbacks than assumed previously.

N-cycling microbiome recruitment differences between modern and wild Zea mays

Rewilding modern agricultural cultivars by reintroducing beneficial ancestral traits is a proposed approach to improve sustainability of modern agricultural systems. In this study, we compared recruitment of the rhizosphere microbiome among modern inbred maize and wild teosinte to assess whether potentially beneficial plant microbiome traits have been lost through maize domestication and modern breeding. To do this, we surveyed the bacterial and fungal communities along with nitrogen cycling functional groups in the rhizosphere of 6 modern domesticated maize genotypes and ancestral wild teosinte genotypes, while controlling for environmental conditions and starting soil inoculum. Using a combination of high-throughput sequencing and quantitative PCR, we found that the rhizosphere microbiomes of modern inbred and wild teosinte differed substantially in taxonomic composition, species richness, and abundance of N-cycling functional genes. Furthermore, the modern vs wild designation explained 27% of the variation in the prokaryotic microbiome, 62% of the variation in N-cycling gene richness, and 66% of N-cycling gene abundance. Surprisingly, we found that modern inbred genotypes hosted microbial communities with higher taxonomic and functional gene diversity within their microbiomes compared to ancestral genotypes. These results imply that modern maize and wild maize differ in their interaction with N-cycling microorganisms in the rhizosphere and that genetic variation exists within Zea to potentially ‘rewild’ microbiome-associated traits (i.e., exudation, root phenotypes, etc.).

Thawing Yedoma permafrost is a neglected nitrous oxide source

In contrast to the well-recognized permafrost carbon (C) feedback to climate change, the fate of permafrost nitrogen (N) after thaw is poorly understood. According to mounting evidence, part of the N liberated from permafrost may be released to the atmosphere as the strong greenhouse gas (GHG) nitrous oxide (N2O). Here, we report post-thaw N2O release from late Pleistocene permafrost deposits called Yedoma, which store a substantial part of permafrost C and N and are highly vulnerable to thaw. While freshly thawed, unvegetated Yedoma in disturbed areas emit little N2O, emissions increase within few years after stabilization, drying and revegetation with grasses to high rates (548 (133–6286) μg N m−2 day−1; median with (range)), exceeding by 1–2 orders of magnitude the typical rates from permafrost-affected soils. Using targeted metagenomics of key N cycling genes, we link the increase in in situ N2O emissions with structural changes of the microbial community responsible for N cycling. Our results highlight the importance of extra N availability from thawing Yedoma permafrost, causing a positive climate feedback from the Arctic in the form of N2O emissions.

Contrasting microbiome dynamics of putative denitrifying bacteria in two octocoral species exposed to dissolved organic carbon (DOC) and warming

Mutualistic nutrient cycling in the coral-algae symbiosis depends on limited nitrogen (N) availability for algal symbionts. Denitrifying prokaryotes capable of reducing nitrate or nitrite to dinitrogen could thus support coral holobiont functioning by limiting N availability. Octocorals show some of the highest denitrification rates among reef organisms, however little is known about the community structures of associated denitrifiers and their response to environmental fluctuations. Combining 16S rRNA gene amplicon sequencing with nirS in-silico PCR and quantitative PCR, we found differences in bacterial community dynamics between two octocorals exposed to excess dissolved organic carbon (DOC) and concomitant warming. While bacterial communities of the gorgonian Pinnigorgia flava remained largely unaffected by DOC and warming, the soft coral Xenia umbellata exhibited a pronounced shift towards Alphaproteobacteria dominance under excess DOC. Likewise, the relative abundance of denitrifiers was not altered in P. flava , but decreased by one order of magnitude in X. umbellata under excess DOC likely due to decreased proportions of Ruegeria spp. Given that holobiont C:N ratios remained stable in P. flava but showed a pronounced increase with excess DOC in X. umbellata host, our results suggest that microbial community dynamics may reflect the nutritional status of the holobiont. Hence, denitrifier abundance may be directly linked to N availability. This suggests a passive regulation of N cycling microbes, which could help stabilize nutrient limitation in the coral-algal symbiosis and thereby support holobiont functioning in a changing environment. Importance Octocorals are important members of reef-associated benthic communities that can rapidly replace scleractinian corals as the dominant ecosystem engineers on degraded reefs. Considering the substantial change in the (a)biotic environment that is commonly driving reef degradation, maintaining a dynamic and metabolically diverse microbial community might contribute to octocoral acclimatization and ecological adaptation. Nitrogen (N) cycling microbes, in particular denitrifying prokaryotes, may support holobiont functioning by limiting internal N availability, but little is known about the identity and (a)biotic drivers of octocoral-associated denitrifiers. Here, we show contrasting dynamics of bacterial communities associated with two common octocoral species, the soft coral Xenia umbellata and the gorgonian Pinnigorgia flava after a six-week exposure to excess dissolved organic carbon (DOC) under concomitant warming conditions. The specific responses of denitrifier communities associated with the two octocoral species aligned with the nutritional status of holobiont members. This suggests a passive regulation of this microbial trait based on N availability in the coral holobiont.

Soil nitrogen and water management by winter-killed catch crops

Improving N cycling in agroecosystems is one of the key challenges in reducing the environmental footprint of agriculture. Further, uncertainty in precipitation makes crop water management relevant in regions where it has not been necessary thus far. Here, we focus on the potential of winter-killed catch crops to reduce N leaching losses from N mineralization over the winter and soil water management. We compared four single catch crops (white mustard, phacelia, Egyptian clover and bristle oat) and a fallow treatment with two catch crop mixtures with 4 and 12 plant species (Mix4 and Mix12). High-resolution soil mineral N (Nmin) monitoring in combination with modelling of spatiotemporal dynamics served to assess N cycling under winter-killed catch crops, while soil water was continuously monitored in the rooting zone. Catch crops depleted the residual Nmin pools by between 40 and 72 % compared to the fallow. The amount of residual N uptake was lowest for clover and not significantly different among the other catch crops. Catch crops that produce high N litter materials, such as clover and mustard leaves, showed an early N mineralization flush immediately after their termination and the highest leaching losses from litter mineralization over the winter. Except for clover, all catch crops showed Nmin values between 18 and 92 % higher on the sowing date of the following maize crop. However, only Mix12 was statistically significant. Catch crops depleted the soil water storage in the rooting zone during their growth in autumn and early winter, but preserved water later on when their residues cover the ground. The shallow incorporation of catch crop residues increased water storage capacity during the cropping season of the main crop even under drought conditions. Hence, catch cropping is not just a simple plant cover during the winter but improved the growth conditions for the following crop at decreased N losses. Mixtures have been shown to compensate for the weaknesses of individual catch crop species in terms of nutrient capture, mineralization and transfer to the following main crop as well as for soil water management. Detailed knowledge about plant performance during growth and litter mineralization patterns is necessary to make optimal use of their full potential.

Water-driven microbial nitrogen transformations in biological soil crusts causing atmospheric nitrous acid and nitric oxide emissions

Biological soil crusts (biocrusts) release the reactive nitrogen gases (Nr) nitrous acid (HONO) and nitric oxide (NO) into the atmosphere, but the underlying microbial process controls have not yet been resolved. In this study, we analyzed the activity of microbial consortia relevant in Nr emissions during desiccation using transcriptome and proteome profiling and fluorescence in situ hybridization. We observed that < 30 min after wetting, genes encoding for all relevant nitrogen (N) cycling processes were expressed. The most abundant transcriptionally active N-transforming microorganisms in the investigated biocrusts were affiliated with Rhodobacteraceae, Enterobacteriaceae, and Pseudomonadaceae within the Alpha- and Gammaproteobacteria. Upon desiccation, the nitrite (NO2−) content of the biocrusts increased significantly, which was not the case when microbial activity was inhibited. Our results confirm that NO2− is the key precursor for biocrust emissions of HONO and NO. This NO2− accumulation likely involves two processes related to the transition from oxygen-limited to oxic conditions in the course of desiccation: (i) a differential regulation of the expression of denitrification genes; and (ii) a physiological response of ammonia-oxidizing organisms to changing oxygen conditions. Thus, our findings suggest that the activity of N-cycling microorganisms determines the process rates and overall quantity of Nr emissions.

Nitrogen Use Efficiency in Parent vs. Hybrid Canola under Varying Nitrogen Availabilities

Improving nitrogen use efficiency (NUE) is essential for sustainable agriculture, especially in high-N-demanding crops such as canola (Brassica napus). While advancements in above-ground agronomic practices have improved NUE, research on soil and below-ground processes are limited. Plant NUE—and its components, N uptake efficiency (NUpE), and N utilization efficiency (NUtE)—can be further improved by exploring crop variety and soil N cycling. Canola parental genotypes (NAM-0 and NAM-17) and hybrids (H151857 and H151816) were grown on a dark brown chernozem in Saskatchewan, Canada. Soil and plant samples were collected at the 5–6 leaf stage and flowering, and seeds were collected at harvest maturity. Soil N cycling varied with phenotypic stage, with higher potential ammonium oxidation rates at the 5–6 leaf stage and higher urease activity at flowering. Seed N uptake was higher under higher urea-N rates, while the converse was true for NUE metrics. Hybrids had higher yield, seed N uptake, NUtE, and NUE, with higher NUE potentially owing to higher NUtE at flowering, which led to higher yield and seed N allocation. Soil N cycling and soil N concentrations correlated for improved canola NUE, revealing below-ground breeding targets. Future studies should consider multiple root characteristics, including rhizosphere microbial N cycling, root exudates, and root system architecture, to determine the below-ground dynamics of plant NUE.