Terrestrial Nitrogen Cycle
- LAST REVIEWED: 07 January 2022
- LAST MODIFIED: 22 February 2018
- DOI: 10.1093/obo/9780199830060-0198
- LAST REVIEWED: 07 January 2022
- LAST MODIFIED: 22 February 2018
- DOI: 10.1093/obo/9780199830060-0198
The importance of nitrogen (N) has been recognized for nearly 180 years when it was understood that plants could not grow without the N contained within precipitation. Nitrogen is widely recognized as being one of the main constraints to ecosystem productivity globally. As a consequence of this, plants and microorganisms have developed a number of strategies to facilitate the capture of N in a highly competitive but often mutualistic setting, and in certain cases (e.g., legumes), symbiotic relationships. Reactive N (Nr) is present in a number of forms in soils, with the bulk soil dominated by organic N in the solid phase and thus not directly available for uptake by plants and microorganisms. The small fraction of N in the dissolved phase, which is potentially available for uptake by plants and microorganisms, can be divided into inorganic and organic pools. The dissolved organic N (DON) pool is highly complex and still very poorly characterized, but can be operationally separated into high molecular weight (>1 kDa) and low molecular weight (<1 kDa) compounds. The prevailing paradigm was that DON must be mineralized to NH4+ and NO3- before uptake by plants, thus the vast majority of literature on terrestrial N cycling has focused on understanding this mineralization process and factors that affect it. Since the late 20th century, focus has increased on the importance of DON as a potential direct source of N for plants, and our recognition of the complexity of competition for Nr is evolving rapidly. At the same time, significant advances have been made in understanding feedback effects between other biogeochemical cycles (particularly carbon [C] and phosphorus [P]) and how these vary at scales from the micro- to the macroscale. At this large scale, a major risk for natural ecosystems is N enrichment. Prior to the advent of the Haber-Bosch process that has enabled mass-production of synthetic N, the main sources of Nr were biological N fixation or oxidation by lightening. Consequently, the advent of industrial production Nr, accounting for 165 Tg N y-1 at the turn of the millennium, has increased the amount of reactive N in the biosphere by 50 percent. Coupled with land-use intensification in general and the risks posed by climate change, one of the great challenges of future research in terrestrial ecosystems is to facilitate strategies to understand and mitigate the effects of Nr enrichment.
Nitrogen is regarded as the limiting nutrient in most terrestrial ecosystems (Vitousek and Howarth 1991). However, since the industrial revolution, and more recently through the Haber-Bosh process in the 20th century, the amount of anthropogenically fixed Nr in the biosphere has increased by 50 percent (Galloway, et al. 2004), resulting in large perturbations to the biogeochemical processes of Nr. This additional Nr in the terrestrial biosphere manifests itself both through diffuse chronic enrichment from atmospheric deposition (Sutton, et al. 2014) and through point additions to the environment as a result of fertilizer use and agricultural intensification (Cameron, et al. 2013). Once present in the soil, N is subjected to many biologically and chemically mediated reactions. Even when N enters the soil as mineral fertilizer in the NH4+ or NO3- form, it is likely to at least spend some of its time in the microbial biomass pool. Despite its small size, containing on average only 2.8 percent of the world’s terrestrial N supplies (Wardle 1992), the soil microbial community is now recognized as the major processor of terrestrial N inputs. Biological uptake of available N and its subsequent redeposition means that the majority of N present in soils is organic in nature. Despite it making up the bulk of the total soil N pool, we know remarkably little about its composition. A multitude of analytical tools are available to probe the composition of this N, but no single tool offers comprehensive coverage of all forms, nor are most fully quantitative. From multiple lines of evidence, we know that proteins dominate, with heterocyclics and amino sugars being the other major forms (Schulten and Schnitzer 1998), but a clear picture is still lacking. Despite this limited information on chemical composition, Bingham and Cotrufo 2016 argues that N stabilization occurs as a result of physical and chemical protection by clays and aggregates. The most visible sink for Nr is uptake by plants. Despite common wisdom being that plants can only take up inorganic N forms, Hutchinson and Miller 1912 demonstrates plant growth on a multitude of organic N compounds in the early 20th century. Schimel and Bennett 2004 proposes a new framework whereby the importance of various potentially available N pools changed with overall nutrient status of the system, and this has been progressed with recent advances that further broaden the evidence base for organic N uptake by plants in many ecosystems (Paungfoo-Lonhienne, et al. 2012).
Bingham, A. H., and M. F. Cotrufo. 2016. Organic nitrogen storage in mineral soil: Implications for policy and management. Science of the Total Environment 551–552:116–126.
Despite a lack of understanding of the true chemical forms of organic nitrogen in soils, this review presents a clear framework for how nitrogen is stabilized in soils. The paper takes a stepwise approach to collating knowledge on how organic nitrogen is preserved in soils and protected from loss. It also highlights that it is important to understand that most nitrogen in soils is not macromolecular, and thus management strategies that take these properties into consideration are required to ensure effective restoration practices and limits on N loss.
Cameron, K. C., H. J. Di, and J. L. Moir. 2013. Nitrogen losses from the soil/plant system: A review. Annals of Applied Biology 162:145–173.
A recent review focusing on the environmental impacts of imbalance between plant uptake and N availability in agricultural systems, detailing processes involved in N loss pathways and the factors affecting the magnitude of losses. It identifies that current best management practices as a result of environmental legislation and newer technologies can reduce the impact of N enrichment from agriculture.
Galloway, J. N., F. J. Dentener, D. G. Capone, et al. 2004. Nitrogen cycles: Past, present, and future. Biogeochemistry 70:153–226.
Galloway has produced several landmark overviews, perspectives, and synthesis papers on the global state of the nitrogen cycle, how humans have impacted it, and the implications of this. This paper is an excellent overview of the extent of anthropogenic interference in the terrestrial N cycle and the impacts of this at the regional and global level.
Hutchinson, H. B., and N. Miller. 1912. The direct assimilation of inorganic and organic forms of nitrogen by higher plants. Journal of Agricultural Science 4:282–303.
Some of the first evidence for the ability of plants to take up and grow on a variety of organic and inorganic nitrogen compounds, albeit with the caveat that the authors will have struggled to control for microbial mineralization of nitrogen in their studies. This study predates the advent of synthetic fertilizer, and thus presents a viewpoint from a time where sources of N for agricultural production came from manures and other waste products.
Paungfoo-Lonhienne, C., J. Visser, T. G. A. Lonhienne, and S. Schmidt. 2012. Past, present and future of organic nutrients. Plant and Soil 359:1–18.
Recognizing that despite many advances in our understanding of the role of organic N in plant nutrition, there are still effectively two “camps” of understanding. This review probes the reasons for this and reinforces the earlier findings of other keynote reviews. The review is one of the first that incorporates the latest experimental findings that other organic N compounds beyond amino acids are taken up by plants in fulfillment of their N requirements.
Schimel, J. P., and J. Bennett. 2004. Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85:591–602.
Still seen as the default overview of N dynamics and competition in soils over ten years after its publication, this transformative review clearly articulates how the paradigm of N availability has evolved over time. It clearly makes the case that proteolysis, not mineralization, is the step that potentially limits the release of available N, and it builds a conceptual framework for when different N forms are likely most important for plant nutrition based upon the overall nutrient status of the ecosystem.
Schulten, H. R., and M. Schnitzer. 1998. The chemistry of soil organic nitrogen: A review. Biology and Fertility of Soils 26:1–15.
A classic and as-yet unsurpassed review of the chemical form of organic nitrogen in soils. The authors perhaps optimistically suggested that at the time of writing in 1998, they expected more complete progress to be made on this topic, but alas instrumental difficulties still defeat true quantification.
Sutton, M. A., K. E. Mason, L. J. Sheppard, H. Sverdrup, R. Haeuber, and W. K. Hicks, eds. 2014. Nitrogen deposition, critical loads and biodiversity. Dordrecht, The Netherlands: Springer Science & Business Media.
This edited book provides a recent comprehensive view of the effects of atmospheric nitrogen deposition on biodiversity, with a goal of integrating many sources of evidence of the effects, components, and indeed magnitudes of atmospheric N deposition in different locations. The chapters cover a wide range of topics and aim to build and integrate understanding of the effects of atmospheric deposition on terrestrial and freshwater biodiversity, taking a critical-loads approach to better understand tipping points where ecosystem services may become degraded.
Vitousek, P. M., and R. W. Howarth. 1991. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115.
A classic reference that investigates how N limitation occurs in the knowledge that N fixers should have a competitive advantage relative to species that cannot fix N. The authors probe the biogeochemical mechanisms for N limitation, and discuss the factors that could prevent biological fixation from reversing limitation.
Wardle, D. A. 1992. A comparative assessment or factors which influence microbial biomass carbon and nitrogen levels in soil. Biological Reviews of the Cambridge Philosophical Society 67:321–358.
An important synthesis that sets out and discusses much of the theory behind the role of the soil microbial community in carbon and nitrogen cycling. Despite it predating most modern molecular microbiology techniques, such as next-generation sequencing, this paper remains a key reference that has retained its ecological relevance.
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