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The nitrogen cycle

Nitrogen is an essential element for all living organisms and is the main nutrient of concern in aquaponics. It occurs in amino acids (parts of proteins), nucleic acids (DNA and RNA), and in the energy transfer molecule adenosine triphosphate (Pratt & Cornely 2014). As nitrogen occurs in many chemical forms, the nitrogen cycle is very complex (Figure 3).

image-20210212133431271Figure 3: The general form of nitrogen cycle (Encyclopaedia Britannica)

The majority of Earth's atmosphere (78%) is atmospheric nitrogen gas, which is molecular dinitrogen (N2). Nitrogen gas is very nonreactive and of no use for most organisms. Nitrogen fixation are all processes that convert atmospheric nitrogen gas into compounds that can be termed reactive nitrogen (Nr). Nr includes all biologically active, photochemically reactive, and radiatively active N compounds in the atmosphere and biosphere. It includes inorganic reduced forms of N (e.g., NH3 and NH +), inorganic oxidized forms (e.g., NO , HNO , N O, and NO –), and organic compounds (e.g., urea, amines, and proteins) (Galloway et al. 2008).

Nitrogen fixation can occur naturally by lightning, as the very hot air breaks the bonds of N2 starting the formation of nitrous acid. It can be performed chemically in a reaction called the Haber-Bosch process. Biological nitrogen fixation occurs when N2 is converted to ammonia by an enzyme called a nitrogenase. Microorganisms that fix N2 are mostly anaerobic. Most legumes (beans, peas etc) have nodules in their root systems that contain symbiotic bacteria called rhizobia that help the plant to grow and compete with other plants. When the plant dies, the fixed nitrogen is released, making it available to other plants.

Figure 4 shows the nitrogen cycle as it occurs in aquaponics. In aquaponics two parts of the food chain (primary producers and consumers) which usually occur together are spatially separated into the aquaculture and hydroponic compartments. The synergistic effects that allow for efficient nutrient utilisation are mediated by microorganisms.

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Figure 4: The nitrogen cycle in aquaponics.

Nitrogen enters the aquaponic system via fish feed, which is ingested by fish and later excreted as total ammonia nitrogen (TAN, ammonia - NH3 and ammonium – NH4+) (Wongkiew et al. 2017). The nitrogen is converted to either ammonium (NH4 +) under acidic or neutral pH conditions, or ammonia (NH3) at higher pH levels. The ammonia concentration is dependent on the ammonium content, pH and temperature (Figure 5, Table 3). Ammonia is less soluble in water than NH4 +; therefore, NH3 is rapidly converted to a gaseous form and emitted from the water (Gay & Knowlton 2009).

Whilst ammonium (NH +) is not toxic, ammonia (NH ) is. Therefore, TAN ought to be removed from the system water and ideally converted to nitrate for two reasons: (i) ammonia and nitrite, a secondary product of nitrification, are both harmful to fish, while nitrate is tolerated by the fish up to 150-300 mg/L (Graber & Junge 2009); (ii) TAN is not optimal for plants, which require predominantly nitrates or a mix of ammonium and nitrate for growth (Hu et al. 2015). This process of biological oxidation of ammonia or ammonium to nitrite followed by the oxidation of the nitrite to nitrate is called nitrification and mostly takes place in the biofilter of aquaponic systems (Table 4). Nitrification is an aerobic process performed by small groups of autotrophic bacteria and archaea and was discovered by the Russian microbiologist Sergei Winogradsky (1892).

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Figure 5: Ammonia-ammonium equilibrium as a function of different temperatures and pH (from Cofie et al., 2016)

Table 3: Percentage (%) of un-ionized ammonia in aqueous solution at different pH values and temperatures. To calculate the amount of un-ionized ammonia present, the Total Ammonia Nitrogen (TAN) concentration must be multiplied by the appropriate factor selected from this table using the pH and temperature from your water sample and divided by 100. If the resulting concentration is larger than 0.05 mg/L the ammonia is harming the fish (adapted after Francis-Floyd et al. 2009)

image-20210212133525153

Table 4: Chemical equations of nitrification. Nitrification is usually a two-step process, performed by a specialised group of bacteria, called nitrifiers

Equation Involved bacteria
$NH4^+ +1.5 O2 → NO2^- +2H^+ +H2O + energy$ nitritation; ammonia oxidizing bacteria (AOB)
$HO2^- +0.5O2→NO_3^-+ energy$ nitratation; nitrite oxidizing bacteria (NOB)
$NH4^+ + 2.0O2 →NO3^-+2H^++H2O+energy$ nitrifiers

The transformation of ammonia to nitrite is usually the rate limiting step of nitrification. This is because AOB (bacteria of the genus Nitrosomonas, Nitrosospira, Nitrosovibrio sp., etc.) and NOB (bacteria of the genus Nitrobacter, Nitrospira, Nitrococcus, etc.) have different growth rates, causing partial nitrification, especially during the start-up period, leading to NO - accumulation until nitrifiers are fully established, which can take up to 4 weeks (Figure 6).

Denitrification (Table 5) is conversion of nitrate (NO3-) to nitrite (NO2-), nitric oxide (NO), nitrous oxide (N2O) and finally to nitrogen gas (N2) under anoxic and anaerobic conditions (very low or zero levels of dissolved oxygen). Denitrification is carried out by dentrifiers, who belong to taxonomically different groups of archaea and facultative heterotrophic bacteria. As N2O is a more potent greenhouse gas than CO2, its production has to be reduced to a minimum (Zou et al. 2016) in order to maximize the rates of incorporation of N into plant biomass.

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Figure 6: Starting the biofilter: development of ammonia, nitrite, and nitrate concentrations over time. (LECA denotes Light Expanded Clay Aggregate, a medium often used in hydroponics)

Table 5: Chemical equations of denitrification reactions. Denitrification generally proceeds through some combination of the following half reactions, with the enzyme catalysing the reaction in parentheses

Equations Enzyme catalysing the reaction
$𝑁𝑂^−3 + 2𝐻^+ + 2 𝑒^−→ 𝑁𝑂^−2 + 𝐻_2𝑂$ Nitrate reductase
$𝑁𝑂2^− + 2𝐻^+ + 𝑒^− → 𝑁𝑂 + 𝐻2𝑂$ Nitrite reductase
$2 𝑁𝑂 + 2 𝐻^+ + 2 𝑒^− → 𝑁2𝑂 + 𝐻2𝑂$ Nitric oxide reductase
$𝑁2𝑂 + 2 𝐻^+ + 2 𝑒^− → 𝑁2 + 𝐻_2𝑂$ Nitrous oxide reductase
$2𝑁𝑂^−3 + 12 𝐻^+ + 10 𝑒^− → 𝑁2 + 6𝐻_2𝑂$ The complete process can be expressed as a net balanced redox reaction

Anaerobic ammonium oxidation (anammox). The bacteria mediating this process were identified in 1999 (Strous et al. 1999). Anammox could exist in aquaponic systems because the water characteristics are similar to those in aquaculture systems, where the anammox process has been shown to occur (Wongkiew et al. 2017). However, the anammox rate is 10-fold slower than the nitrification rate. The anammox process has been reported to contribute to nitrogen loss in different ecosystems (Burgin & Hamilton 2007, Hu et al. 2010). Since ammonia and nitrite are available in aquaponic systems, nitrogen gas could be formed via the anammox process under anoxic conditions in the biofilter (Table 6).

Table 6: Chemical equation of annamox reaction

Equation Involved bacteria
$𝑁𝐻^+4 + 𝑁𝑂^−2 → 𝑁2 + 2 𝐻2 𝑂 + 𝑒𝑛𝑒𝑟𝑔𝑦$ anammox bacteria

Phosphorus cycle

Phosphorus (P) is the second most important macronutrient for plant growth and it is required in relatively large amounts. It plays a role in respiration and cellular division and is used in the synthesis of energy compounds. P enters the aquaponic system by the way of fish feed, tap water, and fertilizer additions (if applicable). The chemical form in which P is present in the nutrient solution depends on the pH. The pKs (quantitative measure of acidity) for the dissociation of H3PO4 into H2PO4 - and then into HPO4 2- are 2.1 and 7.2 respectively (Schachtman et al. 1998, cited in da Silva Cerozi & Fitzsimmons 2016). Therefore, in the pH range maintained in aquaponic systems, P is mostly present in the form H2PO 4 -, and less as H3 PO4 or HPO4 2-. Plants can only absorb P as the free orthophosphate ions H2PO4 - and HPO4 2-. Experimental and simulation studies have shown that P availability decreases with increasing pH of aquaponic water due to precipitation (Figure 7).

If the pH in aquaponic nutrient solution increases, P binds to several cations, so that fewer free P ions (PO4) are available in solution, but there are more insoluble calcium phosphate species, which precipitate from the solution. These insoluble complexes can accumulate either in the fish sludge (Schneider et al. 2005) or in the sediments and periphyton on the walls and piping of the aquaponic system. Yogev et al. (2016) estimated that this loss can be up to 85%. One option to prevent this massive loss of P via sludge is to add a digestion compartment to the aquaponic system. During aerobic or anaerobic digestion, the P is released into the digestate and can be re-introduced into the circulating water (Goddek et al. 2016). da Silva Cerozi & Fitzsimmons (2016) also demonstrated the importance of organic matter and alkalinity in keeping free phosphate ions in solution at high pH ranges. It is recommended though that pH in aquaponic systems is maintained at a range of 5.5–7.2 for optimal availability and uptake by plants.

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Figure 7: Speciation of the major forms of P in aquaponic solution as a function of pH as simulated in Visual MINTEQ. Note that not all PO4 species are described in the chart (from da Silva Cerozi & Fitzsimmons 2016)

The precise dynamics of phosphorus in aquaponics is still not understood. The main input of phosphorus in the system is the fish feed, and in un-supplemented systems phosphorus tends to be limiting (Graber & Junge 2009; Seawright et al. 1998). This is also the reason why up to 100% of phosphorus present in the fish water can be recycled in the plant biomass, depending on the design of the system (Graber & Junge 2009).

Copyright © Partners of the [email protected] Project. [email protected] is an Erasmus+ Strategic Partnership in Higher Education (2017-2020) led by the University of Greenwich, in collaboration with the Zurich University of Applied Sciences (Switzerland), the Technical University of Madrid (Spain), the University of Ljubljana and the Biotechnical Centre Naklo (Slovenia).

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