User:Boldbiker/Nitrogen cycling on organic farms

Organic farming relies on additions of organic matter for the maintenance of soil fertility. The nitrogen cycle is essential to transforming the nitrogen contained within this organic matter into forms of nitrogen that plants can use, particularly ammonium (NH4+) and nitrate (NO3-). In this way, the nitrogen cycle is inextricably linked to soil fertility and plant nutrition on organic farms. Fundamentally different fertilization strategies on organic farms versus conventional farms result in a number of significant differences related to the nitrogen cycle on organic farms, including higher levels of soil organic matter (SOM), a larger and more functionally diverse microbial community, a higher NH4+ to NO3- ratio, increased transformation rates, smaller pools of inorganic nitrogen, and others (see references below). Understanding how and why these differences exist must include consideration of the terrestrial nitrogen cycle. This article explains the pools and flows of the nitrogen cycle with an emphasis on the transformations important for agriculture. This article is not meant to address organic farming practices, but rather facilitate an understanding of the crucial role of the nitrogen cycle in fertility on organic farms.

Overview of the terrestrial nitrogen cycle
The terrestrial nitrogen cycle is the flow and transformation of nitrogen through various biological intermediaries. Nitrogen is essential for the growth of all organisms because it is a constituent of various biological molecules, including proteins and nucleic acids. Since it is an element, it cannot be produced by the plant; it must be obtained from the environment. The supply of biologically available nitrogen is limited in most terrestrial ecosystems, so it is often the primary limitation to plant growth. This limitation is particularly important in agricultural systems, where consistently high yields are desired. At first glance, nitrogen limitation may be counterintuitive, since 78% of the atmosphere is composed of nitrogen gas. This nitrogen, and most forms of nitrogen found in terrestrial ecosystems, is not directly available to plants. The nitrogen cycle is the mechanism by which nitrogen is made available to plants, and thus, to humans.

SOM and Depolymerization
Soil organic matter (SOM) is the primary driver of the soil N cycle and provides the basis for long-term fertility and soil structure. Typical N-rich inputs on an organic farm include compost, crop residues, manure, and cover crops (particularly legumes). When decomposition of these inputs has progressed to the point where the original material is no longer identifiable, they are considered SOM. SOM is comprised of approximately 50% carbon and 5% nitrogen; however, less than 5% of the nitrogen is in a form that can be easily processed by microbes. Nitrogen present in SOM is incorporated into large polymeric biological molecules such as proteins, nucleic acids, and chitin, all of which were at one time constituents of living organisms. These molecules are too large to pass through the microbial cell membrane, and thus cannot be utilized by microbes in their current form; furthermore, they cannot be used directly by plants, so the nitrogen contained within them is inaccessible without further processing. In order to gain access to this nitrogen, microbes (including bacteria and fungi) secrete extracellular enzymes (exoenzymes) into the soil medium that breakdown the large polymers into smaller, soluble pieces (monomers) – known collectively as dissolved organic nitrogen (DON). This process, called depolymerization (Fig. 1, arrow 1), regulates the overall N cycle and is the rate-limiting step.

The use of organic matter for fertilization results in more SOM buildup over time on organic farms than on conventional farms that use inorganic fertilizers . Many factors influence the buildup of SOM, including tillage, type and amount of organic and inorganic fertilizer, crop rotations, water availability, etc, which all interact with local soil properties to determine SOM levels ; however, when these other factors are controlled for, the type and amount of fertilizer has a significant effect on the buildup of SOM. This buildup has been quantitatively demonstrated in several long-term experiments that compare organic and conventional fertilization management. For example, the Rodale Institute Farming Systems Trial compared a conventional corn-soybean rotation with more complex organic rotations, including one that used animal manure for fertilizer and one that relied on legumes. Net inputs of carbon and nitrogen were similar in all systems. When the trial began in 1981, levels of soil carbon and nitrogen (measures of SOM) were similar in all systems. After 22 years of distinct management, soil carbon was significantly higher in both organic systems than the conventional system, increasing 27.9% and 15.1% in the organic animal and organic legume, respectively, with the conventional plots increasing 8.6%. Similarly, soil nitrogen increased 6.4% and 12.9% in the organic animal and organic legume systems, respectively, while soil nitrogen levels in the conventional system did not change.

Mineralization and immobilization
Dissolved organic nitrogen (DON – see above) is a complex assortment of nitrogen-containing compounds that can be absorbed by plants, fungi, and microbes. However, plant use of DON – either by direct uptake and/or uptake mediated by mycorrhizal fungi (see below) – is likely significant for only some ecosystems, such as tundra. Particularly in agricultural ecosystems, most DON proceeds through microbes for further processing. This processing can result in a net release of inorganic nitrogen (mineralization) or a net microbial uptake of inorganic nitrogen (immobilization), depending on whether microbial growth is carbon-limited or not. (Inorganic nitrogen, such as NH4+ or NO3-, is nitrogen that is not part of an organic molecule. This type of nitrogen is the primary source of nitrogen for many plants, especially in agriculture.)  If microbial growth is carbon-limited, then microbes break down DON for its carbon constituents in order to support their energy requirements. Under this scenario, excess nitrogen is released into the soil as a waste product, NH4+, a process called mineralization (Fig 1, arrow 2). If, on the other hand, microbes are nitrogen-limited, then they process DON and retain the nitrogen as well as scavenging and incorporating inorganic nitrogen from existing pools, thereby making nitrogen temporarily unavailable for use by plants, a process called immobilization (Fig 1, arrow 3). As a result of temporal and spatial heterogeneity in the soil medium, some microbial communities may be carbon-limited while others are nitrogen-limited, so mineralization and immobilization can occur simultaneously in different soil micro-environments (microsites). Net accumulation of NH4+ (a measure called net mineralization) occurs in soils that are overall more carbon-limited than nitrogen-limited (from the perspective of the microbial decomposer community). Agricultural ecosystems are generally more limited by carbon than by nitrogen, the opposite situation of most unmanaged ecosystems.

The greater the mineralization rate, the greater the capacity of the soil to supply usable nitrogen to plants. Several factors influence the rate of nitrogen mineralization, including the availability of DON and inorganic nitrogen, soil microbial activity (higher with increasing temperature and moisture), SOM composition (see C:N ratios below), and others. As described elsewhere in this article, organic systems have significantly higher levels of SOM, microbial biomass and diversity, as well as other soil organisms that contribute to rates of mineralization that can be twice as great as those of conventional systems.

The influence of C:N ratios
The ratio of carbon to nitrogen in SOM is one particularly important measure of SOM composition and quality from a microbial perspective. This ratio is important because microbes are composed of different amounts of carbon and nitrogen; a typical microbial carbon-to-nitrogen ratio (C:N) is around 10:1. Microbes incorporate about 40% of carbon during breakdown of organic matter, with the remainder used for respiration and released into the soil atmosphere as CO2. Since a majority of the carbon in organic matter is used for respiration, microbes require more than a 10:1 C:N ratio for growth. The necessary ratio is approximately 25:1. If the ratio is higher, then N will be limiting and it must be imported from other sources (immobilization). If the ratio is lower, then excess nitrogen will be exported to the soil (mineralization). Different cover crops, manures and compost mixtures have different C:N ratios, thus effecting the relative amount and rate of mineralization. The importance of the C:N ratio also highlights the fact that the carbon cycle and the nitrogen cycle are inextricably linked in soils.

Fates of ammonium
After mineralization, ammonium is readily assimilated by plants, but plants compete for nitrogen with microbial populations, particularly decomposers that are nitrogen-starved and thus scavenging for inorganic nitrogen (as previously described). Microbes are likely to win “head-to-head” competitions with plants because they have much larger surface area to volume ratios, they are in close proximity to mineralized nitrogen, and their populations can grow very quickly. However, the ultimate outcome of competition is dependent on the spatial and temporal scale considered. Nitrogen diffuses between microsites of mineralization and immobilization, and plants have an opportunity to capture nitrogen as it diffuses. High turnover rates of microbial populations (ie high rates of “boom and bust”) releases nitrogen and makes it available for plants. Since plants are much longer-lived than microorganisms, accumulation of even a small portion of mineralized nitrogen at each time step will result in effective competition with microbes over time.

Ammonium has several other potential fates as well. Since NH4+ is positively-charged, it will readily bind to negatively-charged surfaces of SOM and certain clay minerals. This binding (or adsorption) onto the cation exchange complex (Fig 1, arrow 4), is a reversible process and serves as a reservoir for inorganic nitrogen (and other cations). As plants and microbes deplete the solution pool of NH4+, NH4+ from the exchangeable (bound) pool goes into solution. Different soils have different cation-exchange capacities (CEC), which is a measure of how many cations they can adsorb. Clay and organic matter content are important determinants of CEC. In the soil, a pH-dependent equilibrium exists between NH3 and NH4+, with more NH3 relative to NH4+ at higher pH values. Ammonia can turn into a gas (NH3; volatilization) and be released from the soil into the atmosphere (Fig 1, arrow 5). High concentrations of NH4+ and various environmental factors increase the rate of NH3 volatilization. Deposition of this gaseous nitrogen in other ecosystems can induce significant changes, including eutrophication and loss of biodiversity. Finally, NH4+ can be oxidized to NO3- by several groups of soil bacteria, a process called nitrification (Fig 1, arrow 6).

Nitrification
Nitrification is the oxidation of NH4+ to NO2- and finally to NO3-, catalyzed by nitrifying bacteria. The oxidation of NH4+ releases energy, which autotrophic nitrifiers use to fix carbon from the atmosphere (used to make energy-rich carbon compounds), in an analogous manner to plants’ use of solar energy to fix carbon by photosynthesis. Several factors influence the amount of NH4+ proceeding down the nitrification pathway. Ammonium concentration is the primary determinant of nitrification rate, since nitrifiers must compete with microbial heterotrophs, as well as plants, for NH4+. Nevertheless, nitrification persists even at low rates of mineralization and low concentrations of NH4+. Another important influence on nitrification rate is oxygen availability, which is affected by soil moisture, root and microbial respiration, as well as physical factors of soil like structure and texture. Most nitrifiers require oxygen for the oxidation of NH4+, so low oxygen availability decreases nitrification rates. While little nitrate typically accumulates on organic farms, nitrification rates can be much higher on organic farms , as discussed below.

Nitrogen losses: denitrification and leaching
Nitrate is particularly susceptible to loss from the ecosystem via leaching and denitrification. Both leaching and denitrification have deleterious effects on the environment, and they remove nitrogen from the agroecosystem, which is undesirable. Leaching occurs because most soils have little positive charge and NO3- is negatively-charged and soluble. As a result, NO3- is highly mobile and can leach into groundwater or through runoff and be lost from the ecosystem (Fig 1, arrow 7). This loss has great implications for downstream ecosystems, contributing to eutrophication. Denitrification is the conversion of NO3- to nitrogen gas (N2), with the release of nitric oxide (NO) and nitrous oxide (N2O) along the way (Fig 1, arrow 8). Denitrification occurs under conditions of low oxygen (as in water-saturated soils) and high nitrate concentrations when soil microbes use NO3- in place of oxygen during respiration. Nitrous oxide is an exceptionally potent greenhouse gas, 300 times more potent than CO2. Nitric oxide ultimately leads to the production of O3 (ozone) in the atmosphere, while N2 is benign (the form of nitrogen that comprises 78% of the air we breathe). Both NO and N2O are also produced to a limited extent during nitrification (Fig. 1, dotted arrow 6).

Synchronization of plant demand with nitrogen availability significantly reduces nitrogen loss, since plants rapidly assimilate NO3-. Organic systems typically accumulate less NO3- than conventional systems, but they are still subject to loss of nitrogen when pulses of available nitrogen occur, such as after incorporation of a legume cover crop combined with heavy precipitation or irrigation. Organic systems have been shown to have a higher NH4+ to NO3- ratio than conventional systems , which can help to limit losses. Studies comparing nitrogen losses between conventional and organic systems report variable results.

Nitrate and ammonium pools on organic farms
Inorganic nitrogen pools (NH4+ and NO3-) on organic farms are generally either similar to or smaller than pools on conventional farms. Smaller pools of inorganic nitrogen do not necessarily result in lower nitrogen availability for plants. Instead, they may be indicative of a tightly coupled nitrogen cycle in which nitrogen mineralized by microbes is quickly absorbed by plants or other microbes, so little mineral nitrogen actually accumulates. Indeed, gross mineralization and nitrification rates (ie that measure production, but not consumption, of (NH4+ and NO3-) measured in an organic production system in California’s Central Valley were twice as high as a corresponding conventional system, although mineral pools were similar . Importantly, this means that organic systems have the capacity to provide adequate plant nutrition while avoiding the environmental problems of excess nitrogen.

Low accumulation of mineral N and delayed transformation of SOM in organically-managed soils make it difficult to assess plant available nitrogen. Common agronomic field tests for nitrogen, such as the pre-sidedress test for nitrate, do not capture the complexity of the nitrogen dynamics on organic farms since it tests for NO3-, which does not readily accumulate on organic farms. Organic farms also face additional difficulty in synchronizing nitrogen availability with plant demand. As microbial transformations are required to liberate plant-available nitrogen from organic matter inputs, a lag time exists between application or incorporation of organic matter and when the nitrogen is actually available to plants. This lag time is variable as a result of a number of environmental and management factors (eg tillage, soil moisture and temperature). Poor timing can lead to nitrogen limitations in crops as a result of microbial immobilization. Nevertheless, with high levels of SOM and robust microbial activity, organically-managed soils can produce sufficient nitrogen for crop production at similar yields to conventional systems.

Birkhofer, K., T. M. Bezemer, J. Bloem, M. Bonkowski, S. Christensen, D. Dubois, F. Ekelund, A. Fliessbach, L. Gunst, K. Hedlund, P. Mader, J. Mikola, C. Robin, H. Setala, F. Tatin-Froux, W. H. Van der Putten, and S. Scheu. 2008. Long-term organic farming fosters below and aboveground biota: Implications for soil quality, biological control and productivity. Soil Biology &amp; Biochemistry 40:2297-2308.

Bonkowski, M., C. Villenave, and B. Griffiths. 2009. Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant and Soil 321:213-233.

Clarholm, M. 1985. Interactions of Bacteria, Protozoa and Plants Leading to Mineralization of Soil-Nitrogen. Soil Biology &amp; Biochemistry 17:181-187.

Fliessbach, A., P. Mader, and U. Niggli. 2000. Mineralization and microbial assimilation of C-14-labeled straw in soils of organic and conventional agricultural systems. Soil Biology &amp; Biochemistry 32:1131-1139.

Hodge, A., C. D. Campbell, and A. H. Fitter. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297-299.

Jackson, L. E., M. Burger, and T. R. Cavagnaro. 2008. Roots nitrogen transformations, and ecosystem services. Annual Review of Plant Biology 59:341-363.

Javaid, A. 2009. Arbuscular Mycorrhizal Mediated Nutrition in Plants. Journal of Plant Nutrition 32:1595-1618. Kirchmann, H. and L. Bergstrom. 2001. Do organic farming practices reduce nitrate leaching? Communications in Soil Science and Plant Analysis 32:997-1028.

Leigh, J., A. Hodge, and A. H. Fitter. 2009. Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytologist 181:199-207.

Mader, P., S. Edenhofer, T. Boller, A. Wiemken, and U. Niggli. 2000. Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biology and Fertility of Soils 31:150-156.

Mader, P., A. Fliessbach, D. Dubois, L. Gunst, P. Fried, and U. Niggli. 2002. Soil fertility and biodiversity in organic farming. Science 296:1694-1697.

Read, D. J. and J. Perez-Moreno. 2003. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytologist 157:475-492.