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Review

Research Hotspots and Trends of Nitrification Inhibitors: A Bibliometric Review from 2004–2023

by
Huai Shi
*,
Guohong Liu
and
Qianqian Chen
Institute of Resources, Environment and Soil Fertilizer, Fujian Academy of Agricultural Sciences, Fuzhou 350003, China
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(10), 3906; https://doi.org/10.3390/su16103906
Submission received: 9 April 2024 / Revised: 28 April 2024 / Accepted: 2 May 2024 / Published: 7 May 2024
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Abstract

:
Nitrification inhibitors are essential in agricultural and environmental production practices. They play a crucial role in promoting agricultural and environmental sustainability by enhancing nitrogen use efficiency, boosting crop yields, and mitigating the adverse environmental effects of nitrogen losses. This bibliometric analysis covers the period from 2004 to 2023, offering a detailed examination of the development of nitrification inhibitor research. The study demonstrates a consistent growth in research publications, indicating sustained interest and dedication to advancing the field. It identifies key contributors, such as institutions and researchers, and underscores the significance of their work through citation analysis. Keyword co-occurrence analysis reveals four distinct clusters focusing on enhancing crop yields, understanding microbial community dynamics, exploring grazing pasture applications, and addressing environmental impact mitigation. The cutting-edge area of keyword burst detection research has transitioned from fundamental research to comprehensive nitrogen management practices. This analysis provides insights into the current research landscape of nitrification inhibitors and proposes future research directions, underscoring the critical role of this field in tackling global agricultural and environmental challenges.

1. Introduction

Nitrogen (N) is a crucial element in living organisms, playing a significant role in regulating primary production in the biosphere [1]. Although nitrogen is abundant in the atmosphere, it primarily exists as inert nitrogen gas. Reactive nitrogen (Nr), which is commonly found as ammonium (NH4+) and nitrate (NO3−) ions, is the limiting factor for ecosystem productivity [2]. The development of the Haber–Bosch process and its application in nitrogen fertilizer production greatly boosted food production, supporting global population growth [3]. However, human-induced nitrogen emissions surpass natural biological nitrogen fixation, with agricultural activities such as nitrogen fertilizer use in crops and intensive grazing livestock excretion being major contributors [4,5]. As population, food demand, and agriculture continue to increase, anthropogenic nitrogen emissions are projected to rise. Our understanding of Nr and the N cycle has evolved from solely focusing on its agricultural benefits to acknowledging the detrimental effects of excessive nitrogen emissions on the environment.
The primary forms of nitrogen losses and emissions in agricultural systems are leaching and gas volatilization [6]. Due to the nitrification process by microorganisms, nitrogen in most agricultural soils is rapidly converted from NH4+ to NO3−. NO3− is less easily absorbed by charged soil particles than NH4+, making it more prone to loss through soil moisture movement, surface runoff, and leaching, ultimately polluting water bodies. Additionally, during the nitrification and denitrification of NO3−, significant amounts of greenhouse gases such as NO and N2O are generated (Figure 1), impacting the climate. Therefore, managing the nitrification process in soil is crucial for enhancing nitrogen utilization efficiency, increasing crop yield, and reducing nitrogen emissions. The concept of nitrification inhibitors was first introduced as early as the mid-1950s. These inhibitors work by suppressing the activity of nitrifying bacteria and enzymes involved in the nitrification process, effectively slowing down the rate of nitrification and supporting the adoption of nitrogen management strategies to address climate change [7,8].
The research and application of nitrification inhibitors has a rich historical background. Existing review papers have primarily focused on specific types of nitrification inhibitors [9] or their application in particular fields [10,11,12]. However, there is a lack of comprehensive overviews detailing the overall research status, key areas of focus, and future directions. Utilizing the bibliometric method introduced by Pritchard, which involves analyzing and quantifying various document characteristics in related fields, offers significant advantages for macro-level research compared to traditional review methods [13]. This approach has become a prominent tool for analyzing large volumes of scientific literature. Bibliometric analysis has gained attention in recent years across various disciplines such as agriculture [14], biology [15], environment [16], and computer science [17]. Notably, there is currently a gap in bibliometric analysis specifically focusing on nitrification inhibitors. This study aims to offer a comprehensive overview of nitrification inhibitor research conducted in the last twenty years. It will emphasize current trends and areas of focus, and provide insights into potential new research avenues and challenges.

2. Bibliometric Analysis

2.1. Data Collection

The data analyzed in this article were retrieved from the Web of Science Core Collection using the keyword ‘*nitrification inhibitor*’ within the time frame of 1 January 2004 to 31 December 2023. The search was limited to English language publications. The total records and references of the literature were exported for analysis.

2.2. Data Visualization

Various tools can be utilized for knowledge graph analysis. In this research, VOSviewer v1.6.20 was primarily employed to visually represent the relationships among countries, institutions, authors, and keywords. Each node in the VOSviewer graph signifies an entity (e.g., country, institution, author, or keyword), with larger nodes indicating higher weight. The thickness of the lines connecting nodes reflects the strength of the correlation between them. Nodes of the same color typically signify that they belong to the same category or group. Additionally, Citespace, Pajek, and Microsoft Excel were also utilized to generate other visualizations.

2.3. Publications Outputs

For a specific research field, the number of scientific papers within a period of time is an important indicator of its development, reflecting the field’s growth rate and historical patterns. A total of 2020 documents related to nitrification inhibitors were published between 2004 and 2023, based on the Web of Science core database. These documents encompass various types such as articles, reviews, proceeding papers, and books, with articles comprising 90.3% of all publications and reviews accounting for 6.1% (Figure 2b). Given the minimal contribution of proceeding papers and potential duplication with articles, our bibliometric analysis focuses on articles and reviews, totaling 1948 publications. The annual output has shown a consistent increase over time, indicating a growing interest in related research fields (Figure 2a). The S curve and logistic model fitting suggest that research on nitrification inhibitors will remain the focus of scholarly attention for the next 5–10 years (Figure 2c). Analyzing research and development trends in the nitrification inhibitors field continues to hold significant academic value and research potential.
The literature examined was sourced from 376 academic journals. The top 10 journals with high h-index values focused extensively on research related to nitrification inhibitors and held significant influence (Table 1). Noteworthy journals include Agriculture, Ecosystems & Environment, Science of the Total Environment, and Soil Biology & Biochemistry, which rank highly in terms of h-index, total publications, and citations. Figure S1 illustrates the publication trend of nitrification inhibitor-related research papers in these journals, showing a consistent output of relevant papers each year. Of particular interest is the remarkable growth in the annual publication volume of Science of the Total Environment since 2017, contrasting with the declining trend in Agronomy Journal. This trend underscores the increasing attention towards research on the impacts of nitrification inhibitors on the ecological environment.

2.4. Country and Institution of the Author

Statistics pertaining to the country or region of the author can provide insights into the overall investment and impact of scientific research in a specific field. The collaboration network between countries offers a visual representation of research activities and international partnerships across different nations. Countries with higher weights signify greater influence and competitiveness on a global scale. Within the research scope, a total of 75 countries have contributed to studies on nitrification inhibitors. The top 10 countries with the highest number of published papers are listed in Table S1. Chinese researchers lead with 641 papers and 17,873 citations, followed closely by New Zealand (258 articles, 10,968 citations) and Australia (273 articles, 7286 citations). Figure 3 illustrates the collaboration patterns among 35 countries that have published over 10 papers, clustering them based on cooperation closeness. Cluster 1 (orange) includes seven Pacific Rim countries, with China, New Zealand, and Australia at the forefront, showcasing active research and close collaboration. Cluster 2 (blue) is dominated by European nations, while clusters 3 (green) and 4 (red) span various regions like Europe, Asia, and North and South America. Among the top 10 countries in terms of published articles (by corresponding author), the proportion of MCP exceeds 20%, indicating significant global interest in nitrification inhibitor research and extensive international cooperation.
In the past 20 years, a total of 1666 institutions have contributed to research on nitrification inhibitors, with 77 institutions publishing more than 10 papers. The Chinese Academy of Sciences leads with 236 publications, followed by AgResearch—New Zealand and the University of Chinese Academy of Sciences with 120 and 98 publications, respectively, showcasing their strength in the field. Geographical location does not limit cooperation between institutions, as shown in the cooperation network (Figure S2). Close cross-regional cooperation enhances knowledge exchange and drives progress in nitrification inhibitor research.

2.5. Prominent Authors and Highly Cited Publications

Author analysis is a crucial method for identifying key researchers in the field. Among the top 10 most influential authors listed in Table 2, Professors Hong J. Di and Keith C. Cameron from Lincoln UniversityNew Zealand, as well as Professor Cecile A.M. De Klein from AgResearch—New Zealand, hold the top three positions in terms of h-index. Their paper output and citations are notably high. Professor Jizheng He from Fujian Normal University stands out for having the highest average number of citations at 75.36. The collaborative map of main authorship (Figure S3) reveals that in the realm of nitrification inhibitors, multiple collaborative teams have been established among researchers with more than 10 papers. Professors Hong J. Di and Keith C. Cameron emerge as the central nodes with the largest number of collaborators.
The top 10 papers with the highest number of mutual citations within the search scope are primarily published in journals related to soil and agriculture (Table 3). Among them, Soil Biology & Biochemistry (IF2022 = 9.7) stands out with three articles having the most citations. The most cited paper is a meta-analysis that assessed the effectiveness of enhanced-efficiency fertilizers, including nitrification inhibitors, in reducing N2O and NO emissions [18]. The second most cited study is a one-year field experiment that investigated the impact of urease and nitrification inhibitors on nitrogen conversion, ammonia and nitrous oxide emissions, pasture yield, and nitrogen uptake in grazing systems [19]. The third paper examines the effect of dicyandiamide (DCD) in decreasing N2O emissions from urine spots in four different soils in New Zealand [20]. Overall, these highly cited papers focus on the impact of nitrification inhibitors on greenhouse gas emissions and nitrate losses.

2.6. Keywords

2.6.1. Keyword Co-Occurrence Analysis

Keywords play a crucial role in summarizing and classifying research content. Analyzing the logical relationship between keywords and conducting co-occurrence analysis can unveil research trends and hotspots in a specific field [21]. In the search scope, a total of 158 keywords appear with a frequency of at least 20 times. The co-occurrence network visualization is illustrated in Figure 4, showcasing the division of keywords into four clusters, each denoted by a distinct color. These clusters signify four prominent research hotspots.
  • Cluster A (green)
As shown in Table 4, Cluster A primarily focuses on the utilization of nitrification inhibitors to enhance nitrogen management in agricultural production, thereby increasing crop nitrogen use efficiency and yield. In modern agriculture, optimizing nitrogen fertilizer usage is crucial for improving crop yields and sustainability. Research has shown that employing nitrification inhibitors can boost average crop yield by 7.5% and nitrogen use efficiency by 12.9% [22]. This positive impact is largely attributed to the ability of nitrification inhibitors to enhance nitrogen fertilizer availability, enabling crops to absorb nitrogen from the soil over an extended period. Furthermore, the efficacy of nitrification inhibitors is closely linked to agricultural system management. Implementing appropriate fertilization and management practices can further enhance the effectiveness of nitrification inhibitors, promoting efficient nitrogen fertilizer utilization and environmental conservation [23,24].
Other keywords include urea, ammonia volatilization, urease inhibitor, and NBPT. Urea, a widely used nitrogen fertilizer, suffers from poor stability in soil and is prone to decomposition and volatilization by urease, leading to nitrogen loss [25]. NBPT (N-(n-butyl) phosphorothiotriamide), a common urease inhibitor, is frequently employed to mitigate ammonia volatilization loss following urea application and enhance nitrogen fertilizer utilization efficiency [26]. Recent studies on the combined use of nitrification inhibitors and urease inhibitors have garnered significant attention, demonstrating dual reduction effects on NH3 and N2O emissions [27,28].
  • Cluster B (red)
Cluster B delves into the correlation between nitrification inhibitors and associated microorganisms, shedding light on the molecular mechanism of nitrification inhibition through a microbiological lens. 3,4-Dimethylpyrazole phosphate (DMPP), one of the three most commonly used commercial nitrification inhibitor products, is the largest node in this cluster.
The nitrification process is a crucial step in the nitrogen cycle, involving the conversion of ammonia nitrogen into nitrite and nitrate through biochemical reactions. It was believed that this process was predominantly carried out by two types of microbial communities: ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA). These microorganisms oxidize NH4+ to NO2− using their unique ammonia oxidase, after which nitrite oxidizing bacteria (NOB) further convert NO2− to NO3−. In 2015, a new group known as complete ammonia oxidizers (comammox) was discovered. Comammox bacteria express all the necessary proteins for both ammonia and nitrite oxidation, allowing them to independently complete the nitrification process [29].
The composition and structure of microbial communities involved in nitrification play a crucial role in the efficiency and stability of this process. Factors like pH, temperature, organic matter content, and the presence of other microorganisms influence the abundance, growth rate, and activity of nitrifying microorganisms [30,31,32]. Nitrification inhibitors like DMPP can effectively reduce nitrate production by inhibiting microbial activity and altering their abundance in the soil [33].
Among these keywords, biological nitrification inhibitors (BNIs) have the most recent average publication year. BNIs are natural compounds produced by certain plants that can also suppress nitrification in soil. These environmentally friendly and renewable types of nitrification inhibitors [34] are currently a prominent focus of research.
  • Cluster C (yellow)
The core keyword of Cluster C is DCD, another commonly used commercial nitrification inhibitor. In grazed pastures, animal urine is the primary nitrogen input source. Nitrification inhibitors can effectively reduce NO3− leaching and N2O emissions in pasture soils resulting from urine patches [20]. New Zealand has developed a treatment method that involves spraying DCD in solution form across the entire soil surface of grazing pastures before the nitrification of urine nitrogen post grazing, maximizing the treatment and suppression of AOB in the surface soil [35]. Although the use of DCD on farms was temporarily halted due to the detection of DCD residues in milk [36], subsequent studies indicated a low risk to human health [37]. The average publication years of related keywords mainly fall within the range of 2014–2017.
The effects of nitrification inhibitors can be influenced by environmental factors, such as temperature, leading to variations in different climate and soil conditions [38]. Furthermore, researchers have investigated the impact of nitrification inhibitors on soil microbial biomass, as microbial biomass serves as a crucial indicator of soil fertility and ecosystem function.
  • Cluster D (blue)
Cluster D delves into the interconnected topics of greenhouse gas emissions and the nitrogen cycle in agricultural soils. The primary focus of this cluster is on the role of nitrification inhibitors in mitigating emissions of N2O and other greenhouse gases like CO2 and CH4, and their implications for climate change. Agricultural activities are significant contributors to global greenhouse gas emissions [39], with N2O and CH4 accounting for 84% and 52% of these emissions, respectively [40]. Nitrification inhibitors work by delaying the oxidation process of NH4+, thereby reducing N2O emissions. Additionally, these inhibitors indirectly decrease nitrate production, which in turn limits the substrate available for denitrification, another process that leads to N2O emissions [41]. Furthermore, the use of nitrification inhibitors extends to the treatment of livestock and poultry manure, such as cow and pig manure. When these manures are utilized as fertilizer in agricultural soils, nitrification inhibitors play a crucial role in lowering ammonia emissions and nitrous oxide production [42].
The impact of nitrification inhibitors on CO2 and CH4 emissions is a complex issue, with varying results in different studies. While some research indicates that nitrification inhibitors do not have a substantial influence on CO2 and CH4 emissions [38,43], other studies suggest that these inhibitors can decrease CH4 emissions while potentially elevating CO2 emissions [44]. Conversely, a study conducted in India reported higher CH4 emissions in the group treated with nitrification inhibitors [45].

2.6.2. Burst Detection Analysis

Burst keywords are terms that experience a sudden increase in frequency within a specific period. High-frequency keywords with low burst intensity are considered stable terms used consistently over time, while those with high burst intensity indicate a concentrated focus during a certain period, potentially highlighting emerging research trends. The top 20 keywords with the highest burst intensity, identified using Citespace 6.1.6, are presented in Table 5. The length of the last column lines (red and green) signifies the research period from 2004 to 2023, with the red portion indicating the burst period.
Analysis of burst keywords in the field of nitrification inhibitors over the past two decades has revealed three distinct periods of research focus. Between 2004 and 2009, the emphasis was on fundamental topics such as ammonia, nitrogen, water quality, and denitrification. From 2006 to 2016, attention shifted towards the practical application of nitrification inhibitors in grazing grasslands, with significant overlap with Cluster C in co-occurrence analysis. The period spanning 2019 to 2023 witnessed the emergence of two new research areas centered on optimizing nitrogen utilization efficiency with nitrification inhibitors. Researchers explored strategies involving the simultaneous control of urease-guided hydrolysis and urea volatilization [46], as well as delved into the effects of rhizosphere soil acidification resulting from increased NH4+ absorption by crops on phosphorus utilization [47].

3. The Mechanism and Application of Nitrification Inhibitors

Nitrifying microorganisms are classified into two categories: autotrophic and heterotrophic. Early studies suggested heterotrophic nitrification was weak, leading to a focus on autotrophic nitrifiers in understanding nitrification. The classic autotrophic nitrification process involves two main steps. Firstly, ammonia is oxidized to hydroxylamine, which then forms NO2−. This ammonia oxidation step is considered the rate-limiting stage of the nitrification reaction. Subsequently, NO2- is further oxidized to NO3−.
Previous studies initially attributed ammonia oxidation primarily to chemoautotrophic bacteria known as AOB. However, since 2004, advancements in metagenomics and enrichment culture have revealed that some microorganisms within the archaeal domain, referred to as AOA, also exhibit the ability to oxidize ammonia [48]. The discovery of comammox bacteria in 2015 is particularly notable as these microorganisms are capable of autonomously completing the entire nitrification process, converting ammonia to nitrite and then further to nitrate [49]. AOA, AOB, and comammox bacteria all possess an ammonia monooxygenase (AMO), a crucial enzyme in the ammonia oxidation pathway. It is worth noting that the majority of nitrification inhibitors operate by targeting and inhibiting AMO [50].
AMO belongs to the Cu-containing membrane-bound monooxygenase superfamily, characterized by copper ions in its active site and a diverse range of substrates [51]. Compounds capable of chelating Cu or competing with NH4+ as substrates can potentially inhibit the AMO-mediated ammonia oxidation process. Nitrification inhibitors exhibit varying inhibitory effects on different types of ammonia-oxidizing microorganisms, possibly due to structural disparities in their AMOs. AOB’s AMO comprises three subunits (amoC, amoA, and amoB) forming a trimer membrane-bound protein, with the Cu-binding catalytic site located in amoB [52]. AOA’s AMO typically includes amoX, with the order of the four subunits varying among different AOA species, and the conservation of amoB in AOA is not uniform [53,54]. Comammox bacteria’s AMO contains an amoCAB operon and two additional amoC genes, showing a closer relationship to AOB [55]. These distinctions can impact the selection and efficacy of nitrification inhibitors in specific environmental contexts.
Hydroxylamine is converted into NO2− in AOB and comammox bacteria through the action of hydroxylamine oxidoreductase (HAO). Recent studies have revealed the involvement of a third unidentified enzyme in the ammonia oxidation pathway [56]. HAO, which is soluble and contains the heme P460 active site, is the most extensively studied functional component in this process and is not easily inhibited by Cu chelators [57]. While the enzyme responsible for catalyzing hydroxylamine conversion in AOA has not been definitively identified, it is known that NO serves as an intermediate product [58]. The addition of NO scavengers has been shown to significantly impede the ammonia oxidation of AOA, leading to reduced production of NO2− [59].
The second step of nitrification is carried out by nitrite oxidoreductase (NXR), with related microorganisms such as NOB and comammox bacteria. There is a limited amount of research on inhibitors of NXR. Inhibiting the activity of NOB bacteria is the primary method of inhibiting the second step of the nitrification process [60].

3.1. Classification and Inhibition Mechanism of Nitrification Inhibitors

3.1.1. Hydrocarbon Compounds and Their Derivatives

Hydrocarbons and their derivatives, such as alkanes, alkenes, and alkynes, can act as substrates that compete with NH4+ for the active sites of AMO, thereby weakening nitrification [51]. The catalytic products of hydrocarbons can further disrupt the ammonia oxidation process of AMO and may even lead to its inactivation [61]. Short-chain alkynes like acetylene specifically bind to the amoA subunit, inhibiting the ammonia oxidation of both AOB and AOA simultaneously [62]. Aromatic hydrocarbons also possess nitrification inhibitory properties, but due to their potential environmental harm, additional toxicological and ecotoxicological studies are necessary before considering practical applications in agriculture [63].

3.1.2. Sulfur Compounds

Compounds with S-containing structures like C=S or P=S, such as thiosulfate, sulfur-containing amino acids, sulfonates, and thiocarbamates, have nitrification inhibitory effects. However, the mechanisms of nitrification inhibition vary based on their chemical structures. Compounds with C=S bonds like thiourea and CS2 are known as Cu chelators [64]. Allylthiourea (ATU) has a lower inhibitory effect on AOA compared to AOB [65].

3.1.3. Cyanamide Compounds

Some studies suggest that cyanamide compounds like DCD inhibit nitrification by affecting electron transfer and cytochrome oxidase function in ammonia-oxidizing bacteria [66]. Currently, it is believed that DCD’s effectiveness lies in its competitive substrate properties [67]. Research has also demonstrated DCD’s ability to inhibit comammox bacteria [68].

3.1.4. Nitrogen Heterocyclic Compounds

Nitrogen heterocyclic compounds with five- or six-membered rings are known to be superior reactive groups. Some of them, such as 2-chloro-6-trichloromethylpyridine (Nitrapyrin) and DMPP, have been successfully utilized as nitration inhibitors and are commercially available. These compounds function by acting as chelating agents for Cu. The inhibitory efficacy of nitrogen-containing heterocyclic compounds is influenced by the positioning of N atoms. When the hetero-N atom is adjacent to a carbon atom bonded to a chlorine atom or trichloromethyl group, the inhibitory effect is enhanced [69].

3.1.5. NO Scavengers

NO scavengers such as 2-phenyl-4,4,5,5,-tetramethylimidazoline-1-oxyl-3-oxide (PTIO) and its derivatives are believed to hinder electron transfer to HAO pairing by reacting with NO, thereby inhibiting the nitrification process of AOA [70]. PTIO shows particular effectiveness against AOA while having no inhibitory effect on the nitrification of AOB, highlighting significant differences in the ammonia oxidation pathways between AOB and AOA [71].

3.1.6. Biological Nitrification Inhibitors

Certain plant roots can secrete compounds known as biological nitrification inhibitors (BNIs) that inhibit nitrification when exposed to an NH4+ environment [72]. Various BNIs have been identified, including 1,9-decanediol [73], zeanone [74], sakuranetin, and sorgoleone [75], with terpenoids and phenolic compounds being the most studied [76]. The majority of BNIs are thought to impact the activities of both AMO and HAO, although their specific molecular targets and mechanisms of action remain unclear. Wendeborn outlined four potential modes of action based on existing research: interference with electron transfer; competition with NH4+ as a substrate for AMO and HAO; binding to the active site of AMO; and non-specific interaction with enzymes or cellular components involved in nitrification [77]. Due to their connection to plant responses to the environment, BNIs can be released more precisely in terms of timing and location compared to commercial nitrification inhibitors. Consequently, breeding high BNI-yielding crops or intercropping BNI-producing crops with conventional crops represents a promising strategy for enhancing nitrogen utilization efficiency.

3.1.7. NOB Inhibitors

Certain compounds have the ability to inhibit the activity of NOB and prevent the conversion of NO2− to NO3−. These compounds, which can also be categorized as nitrification inhibitors, are primarily utilized in wastewater treatment rather than agricultural activities. Examples include chloride [78], sulfide [79], hydroxylamine [80], and peroxide [81]. Additionally, some of them like chlorate can also hinder the activity of complete ammonia-oxidizing bacteria [82].
Different nitrification inhibitors operate through distinct mechanisms and exhibit varying impacts depending on the specific circumstances in which they are used. Figure 5 provides an overview of the target microorganisms and enzymes of these categories of nitrification inhibitors. Broad-spectrum inhibitors must be capable of targeting microorganisms from various ammonia oxidation pathways simultaneously. Until such broad-spectrum nitrification inhibitors are developed, using a combination of existing products may be a viable solution [83].

3.2. Nitrification Inhibitors Commonly Used in Agricultural Production

Nitrification inhibitors have been extensively utilized in agriculture to enhance fertilizer efficiency and minimize adverse environmental effects. Three synthetic nitrification inhibitors, Nitrapyrin, DCD, and DMPP, are predominantly utilized on a large scale.
Nitrapyrin, known by its trade name N-Serve®®, was developed and brought to market by Dow Chemical Company in the 1960s. It has proven to be effective at nanomolar (nM) concentrations [84]. The active ingredient in Nitrapyrin is 2-Chloro-6-(trichloromethyl) pyridine, a white crystalline solid with a molecular weight of 230.9 and a melting point of 62–63 °C. This compound can be dissolved in various organic solvents. Due to its insolubility in water, Nitrapyrin must be dry mixed with fertilizer or used in emulsion form [85]. To prevent volatilization losses, Nitrapyrin should be applied at a depth of at least 5–10 cm in the soil, as it has a high vapor pressure [86]. Widely utilized in corn-growing regions of the Midwest in the United States, Nitrapyrin has demonstrated significant yield-increasing effects [87]. However, its tendency to volatilize and photolyze poses challenges in both application and storage. Additionally, as an organochlorine compound, excessive application of Nitrapyrin can have adverse effects on the environment and crops, necessitating careful consideration during application.
DCD, a cyanamide nitrification inhibitor, is a white crystal powder with a molecular weight of 84.08 and a melting point of 210 °C. It is highly soluble in water and completely degrades into CO2 and NH3 in the soil, leaving no long-term residue. The positive impact of DCD on enhancing nitrogen use efficiency, increasing crop yields, and reducing N2O emissions has been extensively validated. In countries with advanced animal husbandry practices like New Zealand and Ireland, DCD is primarily utilized in pasture management to mitigate nitrogen losses and greenhouse gas emissions. In addition to direct application on grazing grass, DCD is also included in animal feed, enabling its excretion with urine into the environment, resulting in a more focused approach. [88,89].
The active ingredient in DMPP is 3,4-dimethylpyrazole (DMP), which is applied in the form of water-soluble phosphate at a dosage that is only 1/10 of DCD. Due to its positive charge and low mobility in soil, the inhibitory effect of a single application can last for 4–10 weeks [90,91]. A meta-analysis indicated that while DMPP may have a slightly lower effect in reducing N2O emissions compared to DCD, it demonstrates higher efficiency in reducing NO3− leaching [92]. Beyond its impact on food crops, DMPP also holds significant value for the cultivation of vegetables and fruit trees [93,94,95].

3.3. Application of Nitrification Inhibitors in Other Fields

The application of nitrification inhibitors extends beyond agricultural planting and grazing, showing promise in areas like composting and wastewater treatment.

3.3.1. Composting

Composting is a valuable resource recovery method that transforms organic solid waste into stable and safe products. It is commonly utilized for treating livestock and poultry manure, urban domestic waste, and biological sludge [96]. However, there is a significant loss of nitrogen during high-temperature composting, which not only diminishes the quality of compost products but also leads to environmental pollution [97]. The primary nitrogen loss pathways are gaseous emissions such as NH3 and N2O, accounting for over 80% of total nitrogen loss in compost [98]. To address this issue, nitrification inhibitors are incorporated into the composting process to mitigate nitrogen loss, enhance compost quality, and minimize environmental impact [99,100]. Nevertheless, the effectiveness of nitrification inhibitors may be compromised under high-temperature conditions during composting. Some studies propose applying nitrification inhibitors by surface broadcasting on the pile where the temperature is lower and oxygen content is higher [101], or using them in the later stages of composting [102].
Despite debates on NH3 emissions, nitrification inhibitors are proven to reduce N2O and N2 emissions, effectively offsetting overall nitrogen loss. Research indicates that when nitrification inhibitors are combined with urease inhibitors [103] or solid particles like natural zeolites [104], phosphate rocks such as struvite crystals [102], phosphogypsum [105], etc., they can effectively reduce both NH3 and N2O emissions during composting.

3.3.2. Wastewater Treatment

In the field of wastewater treatment, the application strategy of nitrification inhibitors differs from that in agriculture. While in agriculture, nitrification inhibitors are primarily utilized to hinder the initial stage of the nitrification process by inhibiting the oxidation of NH4+ to NO2−, in wastewater treatment, the focus shifts to removing, rather than retaining, the significant amount of nitrogen-containing pollutants present. Here, nitrification inhibitors are employed to selectively inhibit NOB, preventing the second stage of the nitrification process.
In the conventional biological denitrification process, organic nitrogen in wastewater is converted to N2 via the ammoniation–nitrification–denitrification pathway and escapes [106]. To enhance the cost-effectiveness of denitrification and decrease the reliance on energy and carbon sources, alternative pathways like Partial Nitrification (PN)–denitrification (NH4+ → NO2− → N2) [107] and PN-Anammox (NH4+ → NO2−, NH4+ + NO2− → N2) [108] have been devised. The key to successful Partial Nitrification is the stable accumulation of NO2− [109]. To achieve this, specific inhibitors of NOB are incorporated into the wastewater treatment process [110,111,112].

4. Challenges and Prospects

Research on nitrification inhibitors in agricultural production has made significant progress over the decades. Despite the discovery of over a hundred compounds with nitrification inhibitory properties, only three have been commercially utilized. The latest inhibitor, DMPP, has been on the market for over 20 years. However, these three commercial inhibitors still have practical limitations [113]. The development of new nitrification inhibitors has been slow, partly due to the traditional screening and evaluation system lacking the capacity for rapid large-scale assessment. A recent study by Beeckman et al. introduced a drug discovery-based method for identifying new nitrification inhibitors [114], offering valuable insights for future research.
Although autotrophic microorganisms are primarily responsible for nitrification, the role of heterotrophic nitrifying bacteria in soil should not be underestimated. A comprehensive review of 491 observations from 84 publications revealed that heterotrophic nitrification contributes significantly to NO3- production, with percentages of 24%, 32%, and 43% in forest, farmland, and grassland soils, respectively [115]. In specific environments like acidic soils found in subtropical forests [116], greenhouse vegetable fields [117], and dairy farms [118], heterotrophic nitrification can even surpass autotrophic nitrification. Unfortunately, current nitrification inhibitors only target autotrophic nitrification, neglecting the heterotrophic aspect. Given the diversity and complexity of heterotrophic nitrifying bacteria, there is a lack of specific inhibitors targeting this process [119].
Over the past two decades, there has been a continuous deepening of our understanding of the fundamental principles of nitrification. Based on the results of bibliometric analysis, we propose that future research should focus on the following areas:
  • Addressing the limitations of current commercial products: Existing commercial nitrification inhibitor products still have limitations, including unstable effects and short duration. Future research should prioritize enhancing the effectiveness of nitrification inhibitors by developing innovative formulations, optimizing processes, and implementing precise management practices. This is essential for enhancing crop yields, lowering fertilizer expenses, and ultimately fostering sustainable agricultural development.
  • Delving into the intricate molecular mechanisms of microbial-mediated nitrification: Understanding the molecular mechanisms of microbial-mediated nitrification is crucial for identifying new nitrification inhibitors. This knowledge serves as a foundation for the development of more efficient and specific inhibitors.
  • Exploring the biosynthetic pathway of BNIs (Biological Nitrification Inhibitors): In-depth research on the synthesis and secretion of BNIs in plants, along with the understanding of the interaction mechanism between BNIs and soil microorganisms, can improve our understanding and facilitate the development of crop varieties with higher BNI content, as well as optimize agricultural practices. Additionally, insights from BNI research may have the potential to enhance or refine the currently employed chemically synthesized nitrification inhibitors.
  • Developing a novel comprehensive system for screening and evaluation: Simplifying the development and testing process of new nitrification inhibitors is crucial for efficiently obtaining potential products on a larger scale. This process may involve steps such as computer-aided design, high-throughput virtual and actual screening, activity assessment of model strains, optimization of structural modifications, environmental and ecotoxicological safety evaluations, and field trials.

5. Conclusions

Over the last two decades, there has been a steady increase in research publications on nitrification inhibitors, indicating the active engagement and keen interest of researchers in this area. The research focuses on areas such as enhancing crop nitrogen utilization and yield, application in grazing grasslands, addressing greenhouse gas emissions and climate change, and exploring the interaction between nitrification inhibitors and nitrifying microorganisms. Advancements in molecular biology technology have led to a deeper understanding of how nitrification inhibitors function. Furthermore, the integration of urease inhibitors and consideration of phosphorus absorption alongside nitrification inhibitors demonstrate a holistic approach in nitrogen management strategies. In addition to their traditional application in agricultural production, nitrification inhibitors also have significant implications in the composting process and wastewater treatment. Overall, nitrification inhibitors are essential tools for promoting sustainable agricultural development and addressing environmental concerns.
Despite facing challenges, research on nitrification inhibitors presents both challenges and opportunities. Future studies could concentrate on enhancing the effectiveness of existing products, gaining a deeper understanding of the molecular mechanisms of nitrification mediated by various microorganisms, investigating the biosynthesis and utilization of BNIs, and establishing a comprehensive screening–evaluation system to further drive the development and application of nitrification inhibitors.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su16103906/s1, Figure S1: The trend and total number of publications of the top 10 journals in past 20 years; Figure S2: Collaboration network of core institutions; Figure S3: The prominent authors in the field of nitrification inhibitors; Table S1: Top 10 countries with the highest number of published papers.

Author Contributions

Conceptualization, H.S.; methodology, H.S.; validation, H.S.; formal analysis, H.S. and G.L.; writing—original draft preparation, H.S.; writing—review and editing, G.L. and Q.C.; visualization, H.S.; supervision, H.S.; project administration, H.S.; funding acquisition, H.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Fujian Special Fund for Public Interest Research, grant number 2021R1034004.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Publicly available datasets were analyzed in this study. The data can be found here: https://www.webofscience.com/wos/ (accessed on 1 May 2024).

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Schematic of nitrogen transformation in agricultural soil.
Figure 1. Schematic of nitrogen transformation in agricultural soil.
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Figure 2. Publication output related to nitrification inhibitors over the past 20 tears. (a) Annual and cumulative output, (b) publication types, (c) trend forecast.
Figure 2. Publication output related to nitrification inhibitors over the past 20 tears. (a) Annual and cumulative output, (b) publication types, (c) trend forecast.
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Figure 3. Collaboration network between countries in nitrification inhibitors research. (a) Geovisualization. (b) Top 10 relevant countries by corresponding author, SCP: Single Country Publications, MCP: Multiple Country Publications.
Figure 3. Collaboration network between countries in nitrification inhibitors research. (a) Geovisualization. (b) Top 10 relevant countries by corresponding author, SCP: Single Country Publications, MCP: Multiple Country Publications.
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Figure 4. Cluster analysis of the keywords’ co-occurrence.
Figure 4. Cluster analysis of the keywords’ co-occurrence.
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Figure 5. Schematic diagram of the mechanisms of different nitrification inhibitors.
Figure 5. Schematic diagram of the mechanisms of different nitrification inhibitors.
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Table 1. Top 10 most influential journals.
Table 1. Top 10 most influential journals.
RankJournalIndexIFJCITCNPACPPY Start
hgm
1Agriculture, Ecosystems & Environment45752.2506.61.71597610855.332005
2Science of the Total Environment36563.0009.81.68378112330.742013
3Soil Biology & Biochemistry32561.5249.72.0234395661.412004
4Biology and Fertility of Soils27441.2866.51.3520666233.322004
5Plant and Soil23421.1504.91.2717934837.352005
6Agronomy Journal18310.9002.10.7810584822.042005
7Field Crops Research18211.3855.81.9615792175.192012
8Chemosphere17210.8508.81.558292139.482005
9Geoderma17271.4176.11.557743124.972013
10Journal of Soils and Sediments17301.1333.60.729374023.432010
IF: Impact Factor 2022, JCI: Journal Citation Indicator, TC: Total Citations, NP: Number of Publications, ACP: Average Citation per Paper, PY_start: Publication Year Start.
Table 2. Top 10 impact authors during 2000–2023 (no distinction between corresponding authors and other authors).
Table 2. Top 10 impact authors during 2000–2023 (no distinction between corresponding authors and other authors).
RankAuthorInstitutionIndexTCNPACPPY Start
hgm
1Di, Hong J.Lincoln University—New Zealand35661.66744828056.03 2004
2Cameron, Keith C.Lincoln University—New Zealand32631.52440997058.56 2004
3De Klein, Cecile A. M.AgResearch—New Zealand23291.1512712943.83 2005
4He JizhengFujian Normal University21321.31322853271.41 2009
5Vallejo, AntonioUniversidad Politécnica de Madrid21301.0518643062.13 2005
6Chen, DeliTsinghua University19331.26717573353.24 2010
7Saggar, SurinderLandcare Research—New Zealand19331.11813733341.61 2008
8Zaman, MohammadFood & Agriculture Organization of the United Nations (FAO)19341.11815503445.59 2008
9Chadwick, David R.Bangor University18271.2009162733.93 2010
10Ledgard, Stewart F.AgResearch—New Zealand18210.9008062138.38 2005
TC: Total Citations; NP: Number of Publications; ACP: Average Citation per Paper; PY_start: Publication Year Start.
Table 3. Top 10 local cited papers.
Table 3. Top 10 local cited papers.
RankAuthorJournalYearDOITLCAuthors Keywords
1Akiyama, Hiroko Global Change Biology201010.1111/j.1365-2486.2009.02031.x170Controlled-release fertilizer, nitrification inhibitor, polymer-coated fertilizers, slow-release fertilizer, urease inhibitor
2Zaman, MohammadSoil Biology & Biochemistry200910.1016/j.soilbio.2009.03.011140Agrotain, DCD, inhibitors, mitigation, NH3, N2O, pasture, pH, urine
3Di, Hong J.Soil Use and Management200710.1111/j.1475-2743.2006.00057.x120Nitrous oxide, greenhouse gas, mitigation, grassland, nitrification inhibitor, dicyandiamide
4Kelliher, Francis M. Soil Biology & Biochemistry200810.1016/j.soilbio.2008.03.013102Dicyandiamide (DCD), DCD degradation, Temperature, nitrous oxide, nitrification inhibitor, bovine urine
5Di, Hong J.Agriculture, Ecosystems & Environment200510.1016/j.agee.2005.03.00699Nitrate leaching, pasture yield, dairy pastures, water quality, environment, soil, nitrification inhibitor, dicyandiamide, cation leaching
6Menéndez, Sergio Soil Biology & Biochemistry201210.1016/j.soilbio.2012.04.02693Carbon dioxide (CO2), 3,4-Dimethylpyrazole phosphate (DMPP), methane (CH4), nitrification inhibitor, Nitrous oxide (N2O), water-filled pore space (WFPS)
7Zaman, MohammadAgriculture, Ecosystems & Environment201010.1016/j.agee.2009.07.01089Agrotain, DCD, inhibitors, mitigation, nitrogen, NH3, N2O, NO3-, pasture, urine
8Di, Hong J.Australia Journal of Soil Research200410.1071/SR0405087Nitrogen, nitrate, leaching, pastures, dairying, water quality
9Hatch, D. Biology and Fertility of Soils200510.1007/s00374-005-0836-980Nitrous oxide, slurry, greenhouse gases, air quality, nitrification inhibitor
10Zaman, MohammadBiology and Fertility of Soils200810.1007/s00374-007-0252-479Urea, urease inhibitor (NBPT), nitrification inhibitor (DCD), NH3 and N2O emissions, NO3- leaching, pasture
TLC: Total Local Citations.
Table 4. Top 20 keywords of keywords cluster.
Table 4. Top 20 keywords of keywords cluster.
Cluster ANCAPYACCluster BNCAPYACCluster CNCAPYACCluster DNCAPYAC
nitrification inhibitor11922017.07 28.87 DMPP4302017.99 26.49 DCD5832016.25 32.85 N2O emission8492017.56 32.16
soil4972016.68 28.13 nitrate2472016.11 28.63 temperature1502016.10 26.25 N2O4682017.27 34.38
fertilizer2812016.87 32.36 nitrification2272016.42 39.42 grassland1332015.71 33.97 greenhouse gas emission3122018.20 32.89
ammonia volatilization2282017.82 32.46 nitrogen2022015.91 29.99 agriculture1302015.41 35.91 denitrification2712016.63 31.67
yield2232018.11 19.99 AOB1882017.92 41.88 pasture812014.70 34.94 agricultural soil1382018.73 28.39
oxide emission2192018.22 33.88 community structure1492018.74 31.11 urine782014.56 36.09 NO1262016.96 46.62
urea1582017.22 27.47 archaea1272018.06 27.69 urine patch692016.71 38.13 ammonia1242017.32 35.57
urease inhibitor1532018.74 29.93 oxidation1272016.04 39.09 microbial biomass652016.75 38.97 mitigation1242015.34 51.65
management1522017.49 22.93 AOA1122018.09 39.07 cattle urine632016.25 33.24 CO21102017.27 33.78
loss1382016.57 31.28 ammonium1122015.68 17.40 nitrate leaching632015.57 31.75 greenhouse gas952017.08 38.06
nitrogen use efficiency1342018.31 32.65 bacteria1032018.17 24.51 grazed grassland572015.37 59.33 fluxe882016.09 36.05
emission1252018.47 25.66 growth882016.90 23.34 animal urine442014.77 50.39 impact872018.63 22.32
efficiency1222018.36 23.00 abundance802018.98 39.01 grazed pasture412014.56 30.78 methane682013.96 35.79
wheat1122017.15 21.13 diversity712017.79 37.18 pasture soil392017.38 27.05 methane emission682016.46 44.12
use efficiency1112018.47 22.60 fertilization712018.65 21.93 New Zealand362014.81 77.28 manure652017.29 39.35
field1072016.93 30.54 nitrifier denitrification662018.91 27.91 degradation352016.26 15.71 cattle slurry472015.43 44.13
NBPT1022017.54 38.08 carbon612017.97 22.30 emission factor342016.97 50.56 pig slurry412014.32 32.73
urease882019.19 19.92 BNI592019.15 28.15 fate272015.74 32.63 climate change402018.05 38.00
nitrogen fertilizer862017.21 27.77 mineralization592016.80 12.44 different rate262016.62 30.77 tillage372016.62 27.84
system802017.89 22.71 organic matter592017.88 22.85 mineral nitrogen242016.33 27.33 ammonia emission332018.03 44.91
NOC: Number of Citations, APY: Average Publication Year, AC: Average Citation.
Table 5. Top 20 keywords with bursts.
Table 5. Top 20 keywords with bursts.
KeywordsYearStrengthBeginEnd2004–2023
nitrogen20047.2720042009▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
ammonium20046.2620042009▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
water quality20045.1620042011▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
denitrification20057.7120052011▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
methane20056.0320052014▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
grazed pasture200611.0720062016▂ ▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂
agriculture20047.5420062012▂ ▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
temperature20065.9220062015▂ ▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
grassland20046.6420072016▂ ▂ ▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂
urine200813.0420082016▂ ▂ ▂ ▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂
New Zealand20086.7220082016▂ ▂ ▂ ▂ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂
fluxe20055.2720102013▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
oxidation20045.0220122013▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
urine patches20116.7120132015▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
rate20135.0520132015▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
dairy pasture20055.6420142016▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂
dynamics20055.220142015▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂
phosphorus20135.0120192021▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▃ ▂ ▂
strategy20177.0620202023▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▃ ▃
urease20056.2820212023▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▂ ▃ ▃ ▃
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Shi, H.; Liu, G.; Chen, Q. Research Hotspots and Trends of Nitrification Inhibitors: A Bibliometric Review from 2004–2023. Sustainability 2024, 16, 3906. https://doi.org/10.3390/su16103906

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Shi H, Liu G, Chen Q. Research Hotspots and Trends of Nitrification Inhibitors: A Bibliometric Review from 2004–2023. Sustainability. 2024; 16(10):3906. https://doi.org/10.3390/su16103906

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Shi, Huai, Guohong Liu, and Qianqian Chen. 2024. "Research Hotspots and Trends of Nitrification Inhibitors: A Bibliometric Review from 2004–2023" Sustainability 16, no. 10: 3906. https://doi.org/10.3390/su16103906

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