Different Biochar Characteristics on Soil Nitrogen Transformation Processes

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This entry is adapted from the peer-reviewed paper 10.3390/su152316446

Biochar, a carbonaceous product, is formed from organic feedstock pyrolysised in the absence of air and, therefore, is a potential means of recycling organic waste. However, different feedstock and pyrolysis conditions result in a biochar with a range of altered characteristics. These characteristics influence nitrogen transformation processes in soil and result in the metabolism of different substrates and the formation of different products, which have different effects on agricultural yield.

biochar nitrogen fixation mineralisation denitrification soil amendment

1. Introduction

Every year, 2 billion tonnes of solid waste are generated globally ^[1], 30 billion tonnes of carbon dioxide (CO₂) ^[2] are emitted and 12 million hectares of agricultural land are lost to soil degradation, leading to a potential loss of 20 million tonnes of grain per annum ^[3]. This, as well as an ever-growing food and energy requirement as tastes shift towards a more technologically driven lifestyle, means that further stress is placed on Earth’s already depleted and increasingly polluted resources ^[4]^[5]. Hence, there is now a focus on technologies that can reuse waste, reduce emissions, mitigate climate change, generate energy and support food production. One such technology is pyrolysis and the production of biochar. Pyrolysis generally refers to a reaction in an inert environment ^[6].

Since 1993, interest in biochar has focused on whether it can be used to store carbon in soil whilst improving soil properties for improved crop production ^[7]^[8]. Carbon storage in soils is seen as a means to mitigate greenhouse gas (GHG) emissions through the sequestration of CO₂. Woolf et al. ^[9] analysed what level of carbon sequestration, through the production of dedicated biomass for biochar, might be practical to mitigate climate change, without compromising food security, habitat or soil conservation. They estimated that a maximum of 1.8 Pg CO₂-C equivalent (CO₂-Ce) per year (or 12% of current anthropogenic emissions) might be achievable, although estimates range from 0.7 to 1.8 Gt CO₂ eq y⁻¹ ^[10].

Biochar improves the fertility of some soils through the direct provision of nutrients such as nitrogen, phosphorus and potassium. Biochar can also have a liming effect, influencing pH such that nutrients become more available ^[11]^[12]. Most biochars have a high pH (when compared to soil), which results from their ash content and base cations, but also due to intrinsic alkaline organic functional groups ^[13]. However, these values are governed by both feedstock and pyrolysis conditions. For instance, one study found that the pH of herbaceous biochars was two units higher (9.4) than woody biochars (7.4) due to higher concentrations of ash ^[14]. pH was also found to be higher in biochars from leguminous feedstock (9.02 to 10.35) than in non-leguminous feedstock (8.00 to 9.24) ^[15].

Hence, these differences in biochar qualities result in different effects on crop yield. For instance, corncob biochar on infertile acidic soil reduced maize yield, which may have resulted from the biochar’s high volatile matter content and bioavailable carbon. This labile carbon fuelled an increase in micro-organism growth, drawing nutrients from the soil and resulting in nitrogen immobilisation ^[16]. The availability of nitrogen for crop growth is a key agronomic parameter. Nitrogen is an essential plant nutrient and a key element in the development of organic molecules including amino acids, amino sugars, proteins, deoxynucleic acid (DNA), chlorophyll, etc. Nitrogen is very reactive and therefore has a very complex cycle through the soil system, sometimes transforming quickly between inorganic forms as gasses such as NH₃, N₂, N₂O, and NO, in ionic form in soil, NH₄⁺, NO₂⁻ and NO₃⁻, and organic forms. Soils vary considerably in their total nitrogen concentrations from around 0.06% to 0.30%, and more than 90% of this is in organic form ^[17].

Biochar has been reported to reduce nitrogen leaching losses ^[18]. However, these ameliorative effects can vary depending on the carbon content of the amended soil, the biochar’s carbon content, soil textural differences, soil water-holding capacity and the soil micro-organism community amongst other parameters ^[19]^[20]^[21]^[22]^[23].

However, biochar’s influence on the native micro-organism community can exacerbate nitrogen losses from soil systems, depleting nitrogen from soil but also increasing pollutant release. For example, whilst several studies have reported that the incorporation of biochar into different soils reduced N₂O emissions ^[24]^[25]^[26]^[27]^[28], other studies have reported that biochar incorporation results in an increase in N₂O emissions ^[29]^[30]. However, the magnitude of change in N₂O emission because of biochar incorporation is dependent upon experimental conditions, biochar type, application rate, soil properties, and chemical forms of added fertilizer ^[27].

2. Phases of the Nitrogen Cycle

The soil system is open to the atmosphere and nitrogen cycles between them. The first input of nitrogen from the atmosphere is either through lightening, deposition or biological nitrogen fixation (BNF) (Figure 1). This is an important phase of the nitrogen cycle, capturing N₂ and transforming it to NH₄⁺. This process fixes a considerable level of nitrogen year on year. For instance, prior to human intervention, BNF is estimated to have provided 58 Tg N yr⁻¹ worldwide, and it still plays a critical role in maintaining soil fertility ^[31]. It uses the soil’s natural resources (native micro-organisms) and is, therefore, a free and potentially ecologically sound means of crop fertilisation.

Figure 1. Simplified nitrogen cycle.

BNF is carried out by several groups of prokaryotes, including Azotobacter, Azospirillum, Rhizobium and Bradyrhizobium ^[32]. These are either free living in the soil or form symbiotic relationships with plants (around or on the root surface) and both utilise enzymatic processes to catalyse the conversion of N₂ into NH₃. This conversion to ammonia (or ammonification) is then followed by a process of nitrification to nitrites and nitrates. This process is undertaken by both heterotrophic and autotrophic micro-organisms with the bacterium, such as Nitrosomonas, converting NH₃ into NO₂⁻, and Nitrobacter converting NO₂⁻ to NO₃⁻ ^[32]. It is in these forms that plants and micro-organisms can assimilate NH₃ and NO₃⁻ into their structures and the nitrogen then exists in organic form. Upon their death, or through excreta, these forms are then mineralised back again into inorganic form.

They are mineralised by micro-organisms that derive energy from the oxidation of organic nitrogen to NH₄⁺. This is then available to be assimilated and incorporated into amino acids or used for other metabolic purposes. If micro-organisms produce NH₄⁺ in excess of their own requirements, the surplus is excreted into, in this case, the soil, and is available for assimilation by plants, or as the substrate for nitrification ^[33].

Finally, denitrification releases the N₂ originally acquired from the atmosphere by nitrogen-fixing bacteria. Again, it is a process facilitated by micro-organisms where NO₃⁻ is reduced through a series of nitrogen oxide products of decreasing oxidation states until molecular nitrogen (N₂) is all that remains. The process is of particular interest to climate change researchers as some of the intermediate products, nitric oxide and N₂O, are GHGs ^[34].

3. The Influence of Key Biochar Parameters on the Nitrogen Cycle

3.1. The Influence of Recalcitrant and Metabolisable Carbon

Critical to biochar’s ability to store carbon in soil are its aromatic rings, which are highly stable. Aromatic rings include six carbon structures such as benzene, which have strong chemical bonds very resistant to attack by micro-organisms ^[35]. It is this resistance that confers recalcitrance to biochar stored in soil and, hence, its role as a climate change mitigation tool. However, biochar contains other carbon compounds, such as aliphatic carbon chains. These structures have weaker chemical bonds easily broken by micro-organism enzymes and are thus used as an energy source for respiration and therefore result in the ultimate release of CO₂. Hence, although biochar has a carbon content that can range from 50 to 95%, some of this is metabolically available and will therefore influence micro-organism growth in the short term ^[36]^[37]. The amount of metabolically available carbon depends on the biochar feedstock and pyrolysis condition.

In general, the effect of biochar on soil micro-organism mass (and therefore soil respiration) is not well understood ^[38]. For example, some studies have found a 30% degradation of carbon in the first 30 years and very little thereafter (over a 100-year timeframe) ^[39], whereas others estimated a loss of 47% C within a 50-year timeframe ^[40]. Confounding factors include whether the response is dictated by the metabolisable fraction of the biochar or whether the native micro-organisms have the necessary enzymes to mineralise that available carbon ^[41]^[42].

There are potentially negative agronomic consequences resulting from the provision of metabolisable carbon. Although biochar may improve nutrient assimilation by micro-organisms, there may be a consequent decrease in assimilation by crop plants. For instance, biochars with a high aliphatic concentration are more easily degraded by soil organisms, causing an increase in their growth rates and consequent short-term assimilation and immobilisation of nitrogen, impeding supply to crop plants and reducing yield ^[16]^[43].

Conversely, biochar also stimulates the growth of micro-organisms able to mineralise recalcitrant nitrogen found in soil organic matter ^[44]. For instance, one N¹⁵ isotope tracing study using maize biochar found that nitrogen mineralised to NH₄⁺ came from soil organic matter, which was otherwise generally resistant to micro-organism attack ^[25]. They hypothesised that this was due mainly to improved metabolisable carbon availability supplied by biochar pyrolysised at a low temperature. The subsequent elevated growth in micro-organism population could not be met with available nitrogen sources in the soil resulting in the mineralisation of recalcitrant soil organic matter ^[25]^[45]^[46].

A key phase within nitrogen transformations is denitrification, because, if incomplete, it can lead to the emission of N₂O. In their work with wood and poultry manure biochars, Singh et al. ^[20] found that, generally, biochar-amended soils produced significantly lower N₂O emissions than their respective controls but its efficacy in this regard was soil-dependent. They subjected two contrasting soils with different biochar treatment rates to wet–dry cycles. By the third cycle, they found that all biochar treatments consistently decreased N₂O emissions, cumulatively by 14 to 73% from the Alfisol and by 23 to 52% from the Vertisol, relative to their controls. However, some biochars produce higher N₂O emissions ^[20]^[27]^[47].

Biochar influences the cycles of carbon already in the soil, most notably organic matter and humus. Organic matter plays a vital role in the functioning of a healthy soil. Derived from the biomass of both plants and animals (for example, roots and manure), organic matter has a high CEC, helps retain water in the soil and provides soil structure. Organic matter decays over time, releasing its nutrients. When the level of decay slows significantly or stops, and the organic matter becomes stable, it is referred to as humus. Humic acids comprise a large group of chemicals, which perform a vital role in soil health contributing to soil moisture and nutrient retention, as well as the bulk density of soil ^[48]. There is now some evidence to suggest that biochar serves to protect humic acids from decomposition ^[49].

3.2. The Influence of Mineral Ions, Provision, Availability and Uptake

Biochar offers the opportunity to improve soil fertility through the direct provision of mineral ions. The quantity and type of minerals depend on pyrolysis conditions and feedstock. Hardwood biochars tend to have lower mineral contents (5–10%), whereas chicken litter waste can have an ash content of up to 64% ^[50]. The presence of mineral ions can have a significant effect on fixation rates. For instance, Rondon et al. ^[28] found that biochar significantly enhanced biological fixation by Phaseolus vulgaris and accounted for the increase in fixation rate through the increased availability of molybdenum and boron provided by biochar. They noted that the improvement in BNF, as well as the increase in biomass, of Phaseolus vulgaris (5–39%) was above those normally provided by recommended commercial fertiliser applications. Similarly, in Glycine max L., the enhancement of nodulation and BNF response to carbonized organic materials was due to an increase in available sulphur ^[51].

Even low-nutrient biochar has the potential to elevate nutrient availability. In their greenhouse experiment with seven different biochars, ^[52] stripped the biochars of mineral or volatile matter, or both, and left some untreated. The untreated biochar soil treatment planted with Phaseolus vulgaris resulted in an increase of 2126% in nitrogen fixation over the control average (as well as a 262% increase in shoot biomass, a 164% increase in root biomass and a 3575% increase in nodule biomass). The stripped biochar revealed that simple mineral nutrients provided by the biochar were only slightly responsible for these increases. For instance, although the amount of nitrogen fixed was significantly correlated with plant phosphorus uptake, it was not correlated with biochar phosphorus addition but rather improved phosphorus nutrition resulting from 360% greater mycorrhizal colonization with biochar additions.

Mycorrhizal root colonisation and hyphal responses to different biochars can vary substantially ^[53]. This may be due to different responses to a range of volatile matter compounds from contrasting biochars with mycorrhizal response being governed by carbohydrate availability or due to biochar providing physical protection from fungal grazers or the facilitation of root and hyphal exploration, facilitating improved access to nutrients for crop plants ^[52]^[53]^[54].

The provision of nutrients by biochar influences several different assimilation mechanisms. For instance, where biochar provides an increased cation concentration, plant water uptake increases due to the net increase in accumulated osmotically active ions such as potassium. This is key because it improves drought tolerance ^[55]. In addition, biochar appears to increase tap-root growth (and potentially fine root mass), which would increase water uptake from biochar pores ^[56]. Evidence for this improved water status with biochar has been demonstrated through lower proline (an amino acid associated with cell osmotic adjustment in leaves) concentrations and higher osmotic values in leaves, which may reflect an increased tolerance to drought conditions ^[57].

3.3. The Influence of Porosity on Soil Structure, Water and Gas Dynamics

Due to its porous nature, biochar can significantly increase gas transport in soil as well as a soil’s water-holding capacity (WHC) ^[58]^[59]^[60]^[61]. This is because pyrolysis results in an interconnected network of micropores, mesopores and macropores ^[41]. The distribution of pore sizes is governed by feedstock, with wood feedstock developing larger pores ^[59], and by pyrolysis conditions, with those biochars produced at high temperatures via a slow process more likely to produce more macropores (that is, greater than 50 μm in diameter) ^[59]^[62].

Biochar has been reported to improve crop yield through its effect on soil structure ^[63]. In some cases, biochar addition increased aggregate stability and reduced the detachment of colloidal material, improving soil structure ^[64]. However, in coarser soils, there was no such enhancement ^[65]. Where improvements were found, this may have been due to mechanisms such as carboxylic and phenolic functional groups on aged biochar surfaces, which form attachments with soil mineral surfaces. Also, a high CEC allows for cation bridge formation contributing to structural stabilisation ^[43].

Differences in biochar porosity resulting from different feedstocks have a direct influence on micro-organism population. This is because the adhesion of bacteria to biochar may be influenced by pore size ^[66]. Bacillus mucilaginosus and Acinetobacter sp. need a pore size of 2–4 μm if they are to enter ^[67]. In pores, they are better protected from dehydration and grazers and competitors. Surface tension holds water in the biochar, but it does so preferentially, with smaller pores exerting a greater holding capacity than larger ones.

3.4. The Sorption of Mineral Ions, Signalling Compounds, Heavy Metals and Organic Pollutants

Some biochars can be effective in adsorbing NH₄⁺ and NO₃⁻ from the soil ^[68]. This apparent disadvantage, however, may lead to an increase in the ability of the soil ecosystem to feed plants as this reduced nitrogen availability to plant roots stimulates increased nodulation in legumes ^[49]^[69]. Root nodulation can influence the rate of biological fixation, and both the nodulation rate and development, as well as nitrogenase activity, can be affected by the presence of biochar.

Even though biochar can influence the structure of a micro-organism community to promote one nitrogen process or another, its sorption powers can often confound the result. In an experiment comparing biochar alone and biochar that had been shaken with dairy effluent for 24 h, both biochar treatments reduced net ammonification by 220% compared with soil alone. This suggested that the rate of nitrification was higher than the rate of ammonification. However, it appears that these rates were not changed in response to an increase in nitrifiers because CO₂ emissions did not rise. Hence, it was postulated that the reduction in NH₄⁺ was more likely due to its adsorption to biochar rather than immobilisation ^[70].

Again, biochar may influence the denitrification process by limiting micro-organism access to substrates. For instance, in one study, an acidic biochar absorbed NH₄⁺, not only reducing the NH₄⁺ leaching rate but also decreasing the NH₃ volatilisation rate due to a reduction in substrate for the denitrification process ^[71]. However, the decrease in volatilisation rate was driven mainly by the acid–base reaction. Findings from another study concurred, concluding not only that the effectiveness of biochar to reduce N₂O emission was, in part, dependent on the sorption of NH₄⁺, decreasing the overall availability of nitrogen to denitrifiers, but that this ability changed over time ^[20]. With ageing, the effectiveness of biochar to reduce N₂O emission (and NH₄⁺ leaching) increased, as biochar surfaces become increasingly oxidised due to biotic and abiotic processes, potentially leading to an increase in cation exchange capacity ^[23], which may explain the reduction in available nitrogen ^[20].

The mechanism of root nodule formation and BNF in leguminous plants requires infection by nodule-forming bacteria. This process is governed by chemotaxis involving signalling pathways, which are initiated by polyphenolic signalling compounds (for example, flavonoids) released by the host plant ^[72]^[73]^[74]^[75]^[76]^[77]. Biochar is highly effective at adsorbing signalling compounds so any incorporation of biochar into soil, certainly at higher rates, may interfere with these signalling pathways, potentially interrupting nodule development and therefore nitrogen fixation ^[72]^[74]^[75]^[76]^[77].

3.5. The Influence of pH, Cation Exchange Capacity and Electron Shuttle Services

The pH of soil is critical because it affects plant nutrient availability by controlling the chemical forms of various nutrients and influencing the chemical reactions they undergo. For instance, phosphorus, molybdenum and calcium become increasingly unavailable with decreasing pH, with a corresponding decrease in crop productivity ^[78]. Biochar influences pH because it is generally alkaline due to its ash content and release of base cations, but also due to intrinsic alkaline organic functional groups ^[12]. However, the pH of a biochar is governed by both feedstock and pyrolysis conditions. Streubel et al. ^[13] found that the pH of herbaceous biochars was two units higher (9.4) than woody biochars (7.4) due to higher concentrations of ash in their study on contrasting biochar types (all pyrolysed at 350 °C).

As pH influences the chemical form and availability of substrates, it can affect change in both ammonia-oxidising archaea (AOA) and ammonia-oxidising bacteria (AOB) communities, thereby affecting mineralisation rates ^[79]^[80]. Accordingly, the addition of biochar has been shown to increase fixation rates, albeit to a lesser extent, and this capability appears to diminish over time ^[28]^[52].

pH, as amended by biochar, may have a greater influence on mineralisation rates, but the results are highly inconsistent and will depend on the existing pH levels of the amended soil. For instance, autotrophic nitrification generally occurs in neutral and alkaline soils because a critical enzyme, ammonia monooxygenase, uses NH₃ as a substrate rather than NH₄⁺ with the balance affected by pH, with a higher pH favouring NH₃ ^[81]. Hence, although in an already alkaline soil, the addition of biochar resulted in a decrease in the number of nitrifiers ^[82]. However, an amended-acid soil resulted in a significant increase in the abundance of AOB correlating with an increased pH resulting from wheat biochar application ^[38].

3.6. The Influence of Inhibitory Substances

After pyrolysis of biomass, compounds toxic to micro-organisms may be present including polyaromatic hydrocarbons (PAHs) ^[83]^[84]^[85]. The presence of inhibitory substances due to biochar addition is of particular concern as once added to soil, it is almost impossible to remove, therefore any negative environmental consequences may be long-lasting. For instance, Anderson et al. ^[45] found that applying biochar to a silt-loam soil decreased the abundance of Nitrosovibrio—an AOB. As this is a rate-limiting step for nitrification, rates fell, which may be due to the introduction of inhibitory substances ^[30]. Wang et al. also found that phenolic compounds, which are retained by biochars, especially at low-pyrolysis temperatures, may inhibit microbial activity ^[86].

4. Summary of the Influence of Biochar on the Nitrogen Cycle

To conclude the above discussion, as the nitrogen cycle is governed by the activities of micro-organisms and biochar influences both micro-organism action and community composition, as well as other physical and chemical processes in the soil, it has a profound influence on fixation, assimilation, mineralisation and denitrification.

The main influences on fixation are through the promotion of mycorrhizal root colonisation due to the provision of carbohydrates that form part of the metabolisable fraction of carbon supplied by biochar or by providing physical protection from fungal grazers ^[52]^[53]^[54]. Biochar sorption capabilities may be hugely influential as they sorb nitrogen, reducing its availability in soil, thereby promoting nodulation ^[87]. It sorbs pollutants detrimental to micro-organism growth including fixers ^[72]^[88], but can also interfere with signal pathways, potentially interrupting nodule development ^[74]^[76]. Biochar can alter soil pH such that soil fixers benefit, although this process may diminish over time ^[89]. The provision of a metabolisable form of carbon, as well as recalcitrant forms, has been found to increase nitrogen-fixing organisms ^[28]^[52]. Figure 2 gives a summary of the substrates and products of fixation and how biochar influences the chemical and biological processes that lead to the products.

Figure 2. Potential mechanisms of biochar influence on fixation of atmospheric N₂ and production of inorganic nitrogen (arrows denote change in product formation rate).

Biochar influences the assimilation of nitrogen into micro-organisms and plants via several mechanisms. Firstly, it can reduce leaching, keeping nitrogen in the rhizosphere and available for uptake. It can do this through the adsorption of NH₄⁻ or organic nitrogen onto biochar, intercalation or cation or anion exchange reactions ^[90]. Secondly, it improves soil water-holding capacity in some soils, which aids root and hyphal elongation and nutrient capture ^[53]^[89] even under conditions of high water evaporation stress ^[61].

Much research has been conducted on the influence of biochar on mineralisation rates and responses vary with soil type. However, the main mechanisms of influence include the provision of a metabolisable carbon, which influences micro-organism growth (Figure 3).

Figure 3. Potential mechanisms of the influence of biochar on mineralisation of organic nitrogen to non-organic forms (arrows denote change in product formation rate).

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