nitrogen fixation

NITROGEN FIXATION Bhaskar S. Patil, Micro Flow Chemistry and Process Technology, Department of Chemical Engineering and Chemistry, Eindhoven University of Technology, P.O. Box 513, 5600 MB Eindhoven, The Netherlands Volker Hessel, Micro Flow Chemistry and Process Technology, Department of Chemical Engineering and Chemistry, Eindhoven University of Technology, P.O. Box 513, 5600 MB Eindhoven, The Netherlands Lance C. Seefeldt, Department of Chemistry and Biochemistry, Utah State University, Logan, UT 84322 Dennis R. Dean, Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 Brian M. Hoffman, Department of Chemistry, Northwestern University, Evanston, IL 60208 Brian J. Cook, Center for Catalysis, Department of Chemistry, University of Florida, Gainesville, Florida 32611-7200, United States Leslie J. Murray, Center for Catalysis, Department of Chemistry, University of Florida, Gainesville, Florida 32611-7200, United States

Table of Contents Nitrogen Fixation ................................................................................................................................1 1

Introduction................................................................................................................................2

2

Biological nitrogen fixation ...........................................................................................................3 2.1

3

2.1.1

Mo-nitrogenase .............................................................................................................3

2.1.2

Fe protein cycle ............................................................................................................4

2.1.3

MoFe protein cycle ........................................................................................................5

Chemical nitrogen fixation ...........................................................................................................8 3.1

Industrial processes for nitrogen fixation ...............................................................................8

3.1.1

Plasma assisted nitrogen fixation: Birkeland-Eyde arc process..........................................9

3.1.2

Frank and Caro cyanamide process .............................................................................. 10

3.1.3

Haber-Bosch process (HBP): A century of heterogeneous ammonia catalysis .................. 11

3.2

4

Nitrogenases ........................................................................................................................3

Lab-scale efforts for chemical nitrogen fixation ..................................................................... 13

3.2.1

Electrocatalytic nitrogen fixation .................................................................................. 13

3.2.2

Photocatalytic nitrogen fixation .................................................................................... 14

3.2.3

Homogeneous catalytic nitrogen reduction to ammonia ................................................. 14

3.2.4

Non-thermal plasma (NTP) assisted nitrogen fixation .................................................... 17

References ............................................................................................................................... 19

1

INTRODUCTION

Nitrogen (Dinitrogen or N2), which makes up to ~ 78.08% of the Earth’s atmosphere, is an essential element for sustaining all living organisms [1]. Nitrogen is found in nucleic acids, chlorophyll, and amino acids, to name a few biological constituents [2]. Even though dinitrogen is abundantly available, it is not directly accessible to plants and animals. Dinitrogen can only be used in its “fixed” form, like ammonium (NH4+) and nitrate (NO3-). To become metabolically available, the N≡N triple bond must be broken and the resulting atomic nitrogen must be chemically bonded with other elements such as oxygen and/or hydrogen through a process called “nitrogen fixation” [3]. Atomic nitrogen can also be combined with carbon through process known as “nitrogen assimilation” [3]. Some prokaryotes are capable of directly fixing atmospheric dinitrogen and supplying it to plants in a process known as biological nitrogen fixation [4,5], through which almost half of N2 is fixed on Earth. Biological fixation of dinitrogen takes places in the ocean and water bodies, during farming, and in forest and non-agricultural land. The other important natural sources for fixed nitrogen, which is non-biological, are lightning that result from the electric discharge between two clouds and combustion processes, where conditions are optimum for the NOx formation [6]. The increasing food demand from the exploding global population necessitated intensified agricultural practices, which means that biologically fixed nitrogen was no longer sufficient and thus, chemical processes to artificially fix nitrogen were developed [7–9]. Today almost all the chemically fixed nitrogen comes from Haber-Bosch process (discussed in section 3.1.1) [10]. The estimation of global nitrogen fixation quantities, as reported in 2010, are shown in Figure 1 [6]. In this figure, the ‘Farming, Ocean, Forest’ segments represent nitrogen fixation by nitrogenase in microorganisms present in those locales.

Figure 1. Estimation of quantities of fixed nitrogen in million metric tons per year in 2010 [6]. The farming, ocean, and forest segments all represent nitrogen fixation by nitrogenase in microorganisms present in those locales. Reprinted from [9] with kind permission of Elsevier B.V.

Besides using fixed nitrogen as a fertilizer in agriculture, chemically fixed nitrogen in the form of ammonia is also used for large scale applications in chemical industry, e.g. pharmaceuticals, explosives, and plastic manufacturing [9,11]. A complete picture of the range of products derived from ammonia is presented in Figure 2.

Figure 2. Range of applications of chemically fixed nitrogen in the form of ammonia, reprinted from [9] with kind permission of Elsevier B.V.

The chemical process for nitrogen fixation is notorious for high CO2 emission, energy consumption, and harsh operating conditions. On the other hand, biological nitrogen fixation takes place at mild conditions, thus it gives hope for development of a new artificial nitrogen fixation process operating under mild operating conditions [9,12]. This possibility has opened doors for different research areas in biological and chemical nitrogen fixation and have been the subject of increasing efforts since 1960’s. In this chapter we will be briefly discussing various approaches and key concepts involved in biological and chemical nitrogen fixation processes. Only chemical processes could be industrialized for nitrogen fixation for commercial applications, so far, which are also briefly discussed. See also, Ammonia, 3. Production plants, chap. 5. Plasma processes

2

BIOLOGICAL NITROGEN FIXATION

2.1

Nitrogenases

More than half of the N2 fixed on Earth is accomplished by microorganisms through the action of the enzyme nitrogenase [10]. Nitrogenases are found in two of the three domains of life:

Bacteria and

Archaea [13–16]. Nitrogenases are found in a wide-array of these microbes, which are often times referred to as diazotrophs. Nitrogenases have not been found in any Eukaryotes. Diazatrophs are found in most ecosystems, including aquatic (e.g., oceans) and terrestrial [16]. Three different nitrogenases have been identified, with some microbes containing all three. The most commonly found and best studied nitrogenase is called the Mo-nitrogenase, reflecting the presence of the element Mo as part of the complex metal cluster that forms the site of N2 binding and reduction [17]. The other two nitrogenase types are often referred to as “alternative” nitrogenases, because they are not as often found and not as well studied [18]. These alternative nitrogenases are called the V-nitrogenase and the Fe-only nitrogenase, with the names reflecting the replacement of Mo by these metals in the active site metal cluster. The alternative nitrogenases are coded for by unique gene clusters, so are distinct enzymes. However, the overall architecture of the protein complexes and metal clusters appear to be very similar to the Mo-nitrogenase. For this reason, and especially because of the prevalence of the Mo-nitrogenase, this enzyme is taken as the paradigm for nitrogenases and is the focus of this presentation. Reviews on the alternative nitrogenases can be found elsewhere [18,19].

2.1.1 Mo-nitrogenase The Mo-nitrogenase is composed of two protein complexes, referred to as the MoFe protein (also called dinitrogenase or component I) and the Fe protein (also referred to as dinitrogenase reductase or component II) (Error! Reference source not found.) [17]. The MoFe protein is an α2β2

heterotetramer, with each αβ dimer constituting a minimal catalytic unit [20,21]. Each αβ dimer contains an 8Fe-7S cluster called the P cluster and an 7Fe-9S-Mo-C-homocitrate cluster called FeMo-cofactor [22]. The FeMo-cofactor is the site of substrate binding and reduction [23]. The P cluster is proposed to serve as an electron ‘shuttle’, delivering electrons to FeMo-co [24]. The Fe protein component is an α2 homodimer, having a single 4Fe-4S cluster bridging the two subunits [25]. Each subunit of the Fe protein contains a ATP binding site. During catalysis, the Fe protein transiently associates with the MoFe protein, during which an electron is transferred from the Fe protein to the MoFe protein and the two ATP molecules are hydrolyzed to two ADP and two inorganic phosphate (Pi) [26]. The complete catalytic cycle of nitrogenase involves a number of steps in each protein component. While the steps in each protein component are intertwined, for convenience the events associated with the Fe protein delivery of electrons are often called the “Fe protein cycle”, while the events associated with the MoFe protein are called the “MoFe protein cycle”. Key steps in each of these cycles are now summarized.

Figure 3. Mo-Nitrogenase. Schematic representation of the MoFe protein and Fe protein components of nitrogenase (top). Only one half of the MoFe protein is shown with a symmetrical ab half not shown. The Fe protein contains one 4Fe-4S cluster and two ATP binding sites. Each ab half of the MoFe protein contains an 8Fe-7S cluster (called the P cluster) and a FeMo-cofactor (called FeMo-co or M cluster). Structures of the metal clusters are shown (below). Fe is shown in rust, S in yellow, C in gray, O in red, and Mo in magenta.

2.1.2 Fe protein cycle The Fe protein functions to deliver electrons to the MoFe protein during the transient association of the two proteins [27]. The Fe protein cycle is initiated when the Fe protein, with a reduced [4Fe-4S]1+ cluster and two bound ATP, associates with one αβ unit of the MoFe protein. A series of X-ray structures of Fe protein docked to the MoFe protein have shown that the Fe protein binds to the surface of the MoFe protein directly over a P cluster [28–30]. Kinetic studies show the association of the Fe protein with the MoFe protein to be fast relative to other key steps [26]. Following association of the Fe protein with the MoFe protein, a sequence of steps happens rapidly (Figure 4). A recent pre-steady state study revealed that electron transfer (ET) from the Fe protein to the MoFe protein is the first step after protein association, with a pseudo-first order rate constant of 140 s-1 [31]. This electron transfer event has been shown to be conformationally gated, with large scale protein changes in the structure of the complex preceding and controlling electron transfer [32]. The involvement of the P cluster in the ET events has been established [24], with available evidence suggesting a ‘deficit spending’ order of ET steps [32]. Following protein-protein association, the P cluster transfers one electron to the FeMo-co in a gated step, which is followed by fast ET from the Fe protein to the oxidized P cluster. The net result of the ET events is oxidation of the reduced Fe protein and the transfer of an electron to FeMo-cofactor. This ET process in

the Fe protein cycle is followed by ATP hydrolysis with a first order rate constant of about 40 s -1 [31,33]. This step is then followed by Pi release with a rate constant of about 20 s -1. Finally, the oxidized Fe protein, presumably with two bound ADP, dissociates from the MoFe protein. Earlier studies using the non-physiological reductant dithionite as the electron source for the reduction of Fe protein suggested that this dissociation step had a rate constant of 6 s -1, and thus was the rate limiting step [26]. However, a recent study using reduced flavodoxin, one of the natural reductants in the cell, revealed that the dissociation step was fast with this reductant, indicating that events associated with the Pi release step are rate limiting for the Fe protein cycle [34]. Once dissociated, the Fe protein is reduced (physiologically by flavodoxin or ferredoxin) and the ADP is replaced by ATP to “recharge” the Fe protein and complete the Fe protein cycle.

Figure 4. Schematic of the Fe protein cycle. One αβ unit of the MoFe protein is shown on top containing a P cluster (P) and FeMocofactor in the resting (M) or one electron reduced (Mr) state. The α2 dimer Fe protein is shown on the bottom with a 4Fe-4S cluster (box) in the reduced (R) or oxidized (ox) state. The rate constants for each step are shown.

2.1.3 MoFe protein cycle Electrons received by the MoFe protein from the Fe protein are ultimately accumulated on FeMo-cofactor. A kinetic scheme representing the accumulation of electrons into the MoFe protein was put forward by Lowe and Thorneley [26] from a series of kinetic and spectroscopic studies. In a modified and simplified Lowe and Thorneley (LT) scheme, the E0 state represents the resting state before any electrons are accumulated, with the number of electrons transferred to MoFe protein indicated with an n subscript (E n) as shown in Figure 5. Since the electrons are ultimately accumulated on FeMo-cofactor, the En state can be taken as the number of electrons accumulated in FeMo-cofactor or one of its bound, semi-reduced intermediates. Each electron accumulated on FeMo-cofactor is likely balanced by the accumulation of a proton, in proton coupled electron transfer. The accumulated protons also are indicated in the scheme of Figure 5. Several aspects of this kinetic scheme are noteworthy. First, the E 2(2H), E3(3H), and E4(4H) states can “relax” by formation of H2 back to lower E states. This reflects the long known fact that nitrogenase can evolve H2 in the absence of any other substrate [35]. It was also established from early kinetic studies that N2 does not bind until at least 3 or 4 electrons/protons are accumulated on FeMocofactor (shown binding to the E4 state in Figure 5) [26]. The mechanistic reason for the need to accumulate 4 electrons/protons on FeMo-cofactor before N2 can bind remained a mystery for decades. Even more so, the incorporation of a stoichiometric release of one H2 for each N2 bound, with a resulting stoichiometric requirement of 8 e- and H+ to form two NH3, remained a mystery, and indeed was not even

universally accepted [17]. Recent studies have validated this stoichiometry, and revealed the mechanistic reason for these phenomenon [36–38].

Figure 5. Simplified Lowe and Thorneley Scheme. E represents the MoFe protein that has accumulated n electrons from the Fe protein cycle.

A key breakthrough in understanding the mechanism of N 2 binding came from the trapping of a catalytically central intermediate using a combination of substitution of amino acids near the active site and freeze quenching samples during turnover [39–49]. Spectroscopic and kinetic examination of the trapped state using FeMo-cofactor

57

Fe,

95

Mo, 1H, and 2H isotopomers led to two important conclusions

about this intermediate: (i) the state is E4(4H), which has accumulated 4[e-/H+] and is activated to bind N2 for reduction with H2 release (denoted the Janus intermediate); ( ii) the E4(4H) state contains two bridging Fe-H-Fe hydrides (Figure 6) [36–38]. The observation of the two hydrides indicates that the metal core had not changed formal oxidation state even though 4 electrons had been transferred, and explains how FeMo-cofactor can accumulate four electrons at the constant potential of the Fe protein: the electrons are “parked” as metal hydrides.

Figure 6. Structure of FeMo-co and the E4(4H) state. Shown is the structure of the E4(4H) state with one FeS face highlighted with a red box (top) and one Fe-S face with two bridging Fe-H-Fe (bottom). The exact location of binding of the bridging hydrides is not known.

The presence of metal hydrides in the E 4(4H) state allowed consideration of several different models for how N2 would bind and why H2 would be evolved. Each model was compared to a series of earlier observations that provided constraints on the mechanism of the nitrogenase reaction, ruling out all but one model [36–38]. Only a reductive elimination (RE) model was consistent with these observations (Figure 7). In this model, the two hydrides combine to form H 2, leaving behind a doubly reduced metal cluster [36–38]. N2 binding during this process is accompanied by the prompt addition of the two electrons and remaining two protons, yielding a cluster bound diazenido-level intermediate. This first step in the reduction of N2, cleavage of the N≡N triple bond and the two electron/two proton conversion to a cluster bound diazenido-intermediate, is by far the thermodynamically most difficult step of N2 fixation, and is thermodynamically driven by the H 2 release [36]. Studies of the native MoFe show that the Janus intermediate in the modified and native MoFe are identical, and that the process in Figure 7 is indeed a kinetically reversible and essentially thermoneutral equilibrium, driving the cleavage of the N≡N triple bond, whereas direct reduction of N2 to diazene is extremely endergonic [47–49]. Subsequent addition of

protons and electrons ultimately lead to the formation of two ammonia (NH 3) molecules. There are two alternatives as to when the first NH3 is released, after delivery of 5 e-/H+ to FeMo-cofactor, or after 7 e/H+, with the preponderance of the evidence favoring the latter [36,50,51].

Figure 7. Proposed reductive elimination (RE)-oxidative addition (OA) mechanism for reversible N2 binding and H2 release at the E4(4H) state of FeMo-co.

If N2 binding and reduction truly involves RE and is a readily reversible equilibrium, then in the presence of added H2 the equilibrium can be reversed, with oxidative addition ( OA) of H2 to E4(2N2H) generating the bridging hydrides and releasing N2 to form the E4(4H) state. Such a reaction would explain the observation that D2 is converted to two HD when nitrogenase is turned over under D 2 and N2 [17,52,53]. In this case, the D2 undergoes OA to load two Fe-D-Fe bridging deuterides [36]. These deuterides, not being exchangeable with solvent, can be protonated by the sulfur-bound protons derived from solvent, yielding two HD, corresponding to the relaxation steps of Figure 3. This proposed explanation for the HD formation associated with the RE mechanism for N2 activation was tested and confirmed by the demonstration that when the known substrate acetylene (C 2H2) was added along with N2 and D2, the acetylene intercepted the [Fe-D-Fe]-containing states, resulting in the reduction of acetylene to ethylenes with one or two D (C2DH3 and C2D2H2) [44]. In the absence of N2, deutero-acetylenes are not formed, because the bridging deuterides only form through RE/OA at the E4(4H) state. The photolysis of transition metal dihydride complexes commonly results in the reductive elimination of H2 [54], and it has been observed that cryogenic irradiation of nitrogenase E 4(4H) with visible light likewise results in the photoinduced RE of a H2 [46–49]. When the photolyzed sample was warmed to 217 K, the process was reversed, with OA of the released H2 to reform the E4(4H) state. Recent kinetic analysis of the rates of loss of the E4(4H) state and the formation of the E 4(2H)* state have uncovered the existence of an intermediate between these two state, which has been assigned to a H 2 bound state (Figure 8) [49]. The analysis further suggested that this H 2 functions as an intermediate in the thermal

RE of H2 that activates FeMo-co to break the N≡N triple bond during catalysis. While the order of H2 release and N2 binding has not been experimentally established, it is necessary that N 2 bind before H2 is released. Loss of H2 first essentially results in an E2(2H) state, which is not expected to bind N2. This suggests that N2 would at least associate with the H2 bound state (Figure 8).

Figure 8. Reversible N2 and H2 binding to E4. The RE and OA step at the E4 state is shown (top). Proposed mechanism for the reversible RE/OA of N2 and H2 at the E4 state of FeMo-cofactor (bottom). The exact order of N2 binding and H2 loss is unknown.

With these studies, the central elements of the nitrogenase mechanism have become clear. Similar studies will be needed to fill out the full reaction pathway for N 2 reduction. This will include a deepened understanding of how electrons/protons are accumulated in the early E states and how the FeMo-co bound diazene is stepwise reduced to two ammonia molecules. Many challenges remain to fully understand how nitrogenase catalyzes the reduction of N 2 to ammonia under mild conditions, but extensive studies over the last 5 decades have disclosed many aspects of this fascinating and complex molecular machine, while the last decade has begun to reveal the heart of its catalytic mechanism.

3

Chemical nitrogen fixation

The N≡N triple bond is one of the strongest, which needs 9.77 eV (941 kJ/mol) of energy to dissociate and has an ionization potential of 15.6 eV [55]. This indicates the extremely high energy required for cleaving or oxidation of the dinitrogen molecule. Moreover, dinitrogen can only be reduced by highly electropositive metals such as lithium (with electronegativity of 0.98). Thus, breaking the N≡N triple bond is often the rate limiting step in the nitrogen fixation process and is the subject of considerable research [12].

3.1

Industrial processes for nitrogen fixation

Up to the beginning of the 19th century, the fixed nitrogen stockpiled in the form of organic or inorganic materials over millions of years was enough to sustain the demands of the Earth’s population [9]. An explosive growth of population, with increasing sizes of cities, demanded ways to provide more nitrogen through nitrogen fixation. Starting early in the 20th century, nitrogen obtained from artificial processes overtook the nitrogen obtained from the natural organic and inorganic sources [56]. The chemical nitrogen fixation processes could only be developed on industrial scale, including reactions for the production of nitric oxide (NO), ammonia (NH3), hydrogen cyanide (HCN) and nitric acid (HNO3), all these efforts could be combined into the following three main approaches with the corresponding industrial process as an example; 

Combining atmospheric nitrogen and oxygen to form nitric oxide: e.g. Birkeland-Eyde electric arc process [57,58]



Use of compounds capable of fixing nitrogen in their structure: e.g. Cyanamide process [56,59,60]



Combining atmospheric nitrogen with hydrogen to form ammonia: e.g. Haber-Bosch process [61,62]

These processes are discussed below. Figure 9 outlines the most significant events in the industrialized nitrogen fixation process development [56,63,64].

Figure 9. Major milestones in chemical nitrogen fixation process development [56,63,64].

Both, Birkeland-Eyde and Frank-Caro processes were very energy intensive [65] and eventually taken over by the Haber-Bosch process from 1930’s [10,60,62]. Comparatively less energy consumption and higher volumes of ammonia produced by Haber-Bosch process were the main reasons. The chronological progress is shown in Figure 10, which emphasizes the dramatic reduction in energy consumption for nitrogen fixation [66]. Significant development in technology over the last half century has made it possible to reduce the energy consumption of the Haber-Bosch nitrogen fixation process by almost 3 times to reach the present energy consumption of 28-36 GJ/ton N-fixed [61].

Figure 10. Comparison of energy consumption for three N-fixation processes [66].

3.1.1 Plasma assisted nitrogen fixation: Birkeland-Eyde arc process Nitrogen fixation was first realized through an electric arc process, known as “Birkeland-Eyde or Norwegian Arc Process”, which was developed by Prof. Christian Birkeland and Samuel Eyde in 1903 [57]. In fact, the Birkeland-Eyde process is also the first plasma process ever realized successfully on the industrial scale. This process employs the most fundamental means of chemically fixing dinitrogen by direct reaction with oxygen under plasma conditions to produce nitrogen oxides. The nitric oxide production is favored by high temperature processing with minimum thermodynamic energy requirement of 6.4 GJ/t of nitrogen [67] and has a positive standard Gibbs free energy of 86.55 kJ/mole. N2 + O2 ↔ 2NO

ΔH = 90 kJ. mol-1 = 1 eV

(R-1)

2NO + O2 ↔ 2NO2

(R-2)

2NO2 + H2 O ↔ HNO2 + HNO3

(R-3)

The typical process flow scheme for industrial the Birkeland-Eyde process is shown in Figure 11. The Birkeland and Eyde furnace was based on the phenomena of deflection of an electric arc by a magnetic field. This helped to spread the electric arc through the gas. First, air was rapidly passed through a zone of exceedingly high temperature in an electric arc furnace, producing ~1-2 vol% nitric oxide (R-1). In the second step, nitric oxide was oxidized to nitrogen dioxide (R-2). Finally, nitrogen dioxide was then

absorbed in water to produce dilute nitric acid (30%) in a train of absorption columns (R-3), including alkaline absorption columns for recovering unabsorbed NOx. The experiments were first carried out using a 2.24 kW power supply in 1903. In the next step, a commercial plant working on 111.8 kW was installed, whose successful operation led to installation of a 745.7 kW plant near Arendal, Norway. This successful demonstration resulted in a number of new plasma furnace installations, the biggest of which was a 238.6 MW plasma furnace, fixing 38 ktons of nitrogen in total per year (in 1928) [56,60].

Figure 11. The industrial scale model of Birkeland-Eyde nitrogen-fixation process; from the power station on the left of the figure to the final fertilizer product to the right. With kind permission from [57] Springer Science and Business Media.

For this process, the raw material (air) is available abundantly and almost for free. However, less than 3% of the supplied energy was utilized for the reaction, while the rest of the supplied energy (97%) was wasted in establishing conditions suitable for the reaction to take place - e.g. to obtain 1 ton of fixed nitrogen it was required to process 175 ton of air. Even though equipment had been built to rapidly cool the product gas to avoid decomposition of nitric oxide, it was believed that a large amount of nitric oxide decomposition actually took place [9,56]. Various efforts were attempted to improve the performance of the Birkeland-Eyde process, but this thermal plasma assisted nitrogen fixation process was found difficult to realize with sufficient product yield at affordable energy input. Because of the poor energy efficiency and high mechanical maintenance requirement, it was eventually abandoned as an industrial process [56,68].

3.1.2 Frank and Caro cyanamide process German scientists Frank and Caro developed the cyanamide process in 1895-1898 to fixed atmospheric dinitrogen and commercialized it around the same time as the Birkeland-Eyde process. The Frank-Caro process needs limestone and carbon as the main reactants, both of them solids, to produce nitrogen containing calcium cyanamide as a solid product. In this process, first limestone is heated to produce lime and carbon dioxide (R-4), which then reacts with carbon to give out calcium carbide (R-5). In the final step, dinitrogen was fixed in the form of calcium cyanamide by its reaction with calcium carbide at ~1000oC (R-6). The final product, calcium cyanamide, was applied as fertilizer, which, after reaction with water, hydrolyzes to calcium carbonate and ammonia (which is then used by plants) via reaction (R-7) [59,60]. ℎ𝑒𝑎𝑡

CaO + CO2

(R-4)

CaO 3C → CaC2 + CO

(R-5)

CaCO3 →

CaC2 +

~1000𝑜 𝐶

N2 →

CaCN2 + C

CaCN2 + 3H2 O → CaCO3 + 2NH3

(R-6) (R-7)

The cyanamide process grew rapidly, reaching its peak in 1918, with 35 plants and total rated capacity of fixing 350 ktons of nitrogen per year [56], mainly because of its 70-80% lower energy requirement than the Birkeland-Eyde process. However, this process had lower fixed nitrogen content in its final product, cyanamide. Moreover, the solid reactants and products made process operation and handling difficult. Eventually, the cyanamide process also phased out.

3.1.3 Haber-Bosch process (HBP): A century of heterogeneous ammonia catalysis The Birkeland-Eyde and the Frank-Caro process were eventually displaced by the “Haber-Bosch process”, developed in 1908 by Fritz Haber and commercialized in 1913 by Carl Bosch (and later Alwin Mattisch) [10,60,62]. Comparatively less energy consumption and higher volumes of ammonia produced by the Haber-Bosch process were the main reasons. After 1941, industrial (di)nitrogen fixation was exclusively carried out by the Haber-Bosch ammonia synthesis process [61]. This nitrogen fixation to ammonia (NH3) [3] process remains one of the most industrially important transformations for human civilization [69]. On a global scale, ammonia is produced at a rate of 140 million tonnes per annum [70]. The catalytic production of NH3 was first discovered to proceed by combining the respective elements as their diatomic gases at high temperature and pressure (300°C, 100 MPa) over a Fe catalyst, which was fused together with trace amounts of alumina, calcium oxide, and potassium oxide [11]. This mixture is such an effective NH3 production catalyst that it is still used in the present day [71]. The Fe catalyst is compositionally similar to that of magnetite (Fe3O4), and future generations of Fe-based NH3 production catalysts have utilized this iron oxide instead of elemental Fe. For 70 years after the discovery of the HBP, little progress was made in Fe-based NH3 production catalysts until the discovery of Fe 1-xO (Wüstite) as a replacement of elemental Fe in 1986, again calcined with the same additives as in the original composition [72]. Currently, this composition (Fe1-xO, Al2O3, CaO, K2O) is the most active Fe-based catalyst used in the HBP [73]. Significant research interest [74] was devoted to the development of rare metal-based catalysts to replace Fe, and were first introduced industrially at British Petroleum in the late 1970s. These “bariumpromoted” Ru catalysts are comprised of Ru and Ba supported on MgO [75]. Presently, a large majority of industrially active NH3 generation plants consist of either Fe3O4/Fe1-xO based catalysts (one-bed reactor) or Ba-Ru/MgO (two-bed) reactors [73]. Although the current reaction conditions are not as harsh or energetically costly as the initial discovery, NH 3 production continues to be an energy-intensive process and a challenge for the research community.

Figure 12. Proposed mechanism for Fe-based Haber Bosch catalysis [76].

The mechanism of nitrogen fixation at the catalyst surface in the HBP remains an active research area. Currently, the mechanism is proposed to proceed through a related step-wise pathway as shown in Figure 12 [77]. Here, local Fe centers are generated at high pressure and temperature on the surface of the Fe-based catalyst. These local Fe centers facilitate the cleavage of the N-N triple bond (BDE = 225 kcal/mol) to yield N adatoms on the catalyst surface, likely localized as Fe 3N units. Addition of one equivalent of H2 affords a bound Fe-NH2, with a subsequent equivalent of H 2 resulting in NH3 release and catalyst regeneration [78]. The Ru-based catalysts are thought to proceed through a similar mechanism, with five Ru atoms in a B5-type site activating one molecule of N 2 [79–84]. Due to the high energetic requirements of the HBP, there has been rich active research in developing new heterogeneous nitrogen fixation systems. Many of these systems are still based on the time-tested thermochemical approach that the HBP employs. Ru has been reported numerous times with alternative additives than BaO/MgO, with K [85] and Cs [86] used as promoters on carbon surfaces. Additional efforts have been made to reduce the energetic cost of producing NH 3 by recycling the steam used in the reactor towards more NH3 production [87]. Recently, chemical looping involving reduction of Mn 6N2.58 to Mn4N was used to drive the hydrogenation of Ca 3N2, Sr2N and SrH2 and produce NH3 catalytically from H2O under ambient sunlight as the heat source [88]. Finally, numerous computational studies have focused on developing new NH3 generation catalysts [89], highlighted by the design of an FeN3embedded graphene catalyst which is predicted to operate at room temperature [90].

Figure 13. Energy-flow diagram of the Haber-Bosch process, initially producing H2 to feed into a NH3 production reactor [91].

Today, this process sustains 40% of the global population and have doubled the number of humans supported per hectare of arable land [68,92], therefore it is considered as the most important discovery of the 20th century [62]. After the invention of the Haber - Bosch process, the global population started growing rapidly. The increase in global population and the nitrogen fertilizer consumption follow a very similar trend as shown in Figure 14 [6].

Figure 14. Global population increase and the nitrogen fertilizer consumption trends [3].

3.2

Lab-scale efforts for chemical nitrogen fixation

Several alternative approaches have been developed for sustainable nitrogen fixation at mild operating conditions, based on the biological one, such as electron driven electrocatalysis and photocatalysis, homogeneous and enzyme catalysis [12]. It is highly unlikely that these alternative processes would be more energy efficient than the extraordinarily well optimized Haber-Bosch process. However, the emphasis should be to minimize the substantial carbon foot print of nitrogen fixation by employing energy from sustainable sources such as wind, solar, or biomass. Furthermore, it would be desirable to focus on the localized, at the point of use, fixation of nitrogen for example fertilizer. This approach is expected to solve the problems associated with the transportation and empower the famers working at remote places such as in Africa.

3.2.1 Electrocatalytic nitrogen fixation Although the HBP makes use of dihydrogen as both the reducing agent and proton source for nitrogen fixation to ammonia, an alternative approach is to use an electrode to provide electrons [94] coupled to an exogenous proton source (see Figure 13) [95]. The overall thermodynamics of dinitrogen reduction are more favorable if electrochemical reduction and protonation are concerted or tightly-coupled (viz. proton-coupled electron-transfer or PCET) [96]. However, adventitious production of H 2 is often competitive with NH3 formation in these systems, decreasing the Faradaic efficiency (mol NH 3/mol epassed) [97]. To date, few systems have been shown to generate NH 3 electrocatalytically. Lambrou reported a Ru cathode on a carbon felt in a three electrode system that operated at elevated temperature and standard pressure; the highest Faradaic efficiency of 0.92% was achieved at 0.06 V and 90 °C [98]. In 2013, Tao showed catalytic NH 3 production at a Pt cathode and anode, in combination with an acidic Nafion 211 membrane [99–101]. Using air as their dinitrogen source, a maximum production rate of 3.5×109 mol s-1 cm-2 was obtained and the faradaic efficiency of this system is 0.7%, which improved to 2% when air is replaced by N2. Other more elaborate electrochemical setups have also been reported; these systems, however, require elevated temperatures to produce NH 3. Examples include a double Pd electrode cell separated by SrCe 0.95Yb0.05O3 (78%) [102], a petrovskite La0.6Sr0.4Fe0.8- with a Cu0.2O3- electrode [103], and the use of molten salts as an electroactive surface (23%) [104]. Other noteworthy ammonia synthesis and catalysis results include: dinitrogen hydrogenation on a polyaniline electrode [105], NH3 generation mediated by a complex of fullerene C 60 and [gamma]cyclodextrin [106,107], catalytic NH3 synthesis from steam and nitrogen at atmospheric pressure [108], catalytic production using of a dielectric-barrier discharge [109], the use of a stable electride in solution as the electron source [110], and the electro-synthesis of NH3 using Chatt-like W(Ph2PC2H4PPh2)2 complexes at vitreous carbon electrodes [111].

3.2.2 Photocatalytic nitrogen fixation One area of increasingly active research in heterogeneous nitrogen fixation is one that utilizes photocatalytic methods [112], in which incident photons (hν) provide the required energy for dinitrogen reduction to ammonia. Since the late 1970s [113], numerous heterogeneous systems were reported to produce ammonia from dinitrogen and sacrificial reductants using active photocatalysts, such as TiO 2 doped with known nitrogen fixation-active metals such as Fe and Ru [114–116]. Here, TiO2 photocatalytically splits H2O [117] generating H2 and O2, the former of which goes directly into NH 3 and N2H4 production. However, some (di)nitrogen oxidation is unavoidable and also observed (see Figure 15) [118]. Alcohols are also commonly employed as sacrificial reductants in addition to H 2O [116]. Indeed, photolysis in the presence of H2O2 was found to lead to NO production, not NH 3. Impressively, many of these systems show significant NH3 generation under ambient sunlight, highlighting the utility of this methodology [114]. Other photocatalytic systems employ semiconductors (i.e., ZnO, SrTiO3, CdS, and GaP) in lieu of TiO2 [119]. More recently, Chen et al. reported photocatalytic ammonia production using Bi5O7I nanosheets [120]. Other notable recent results include using solvated electrons and water to reduce nitrogen to ammonia on a photo-illuminated diamond surface [121], as well as photocatalytic production of NH3 Fe-oxide adsorbed to cross-linked graphene via photo-prompted “hot electrons” [122]. Despite significant progress, however, the rate of ammonia produced and the scalability from reported photocatalytic methods fails to compare favorably with that from current Haber-Bosch methods.

Figure 15. Photolytic production of H2 from H2O and Generation of NxHy Products

3.2.3 Homogeneous catalytic nitrogen reduction to ammonia Ammonia production using homogeneous catalysts offers numerous advantages to that of heterogeneous systems. Chief among these benefits are uniform reaction conditions, favorable kinetics (and thus high turnover frequency), as well the ability for study by using spectroscopic methods [123]. The latter in principle allows for an iterative approach to improving catalyst design. Inspired by the iron-molybdenum cofactor

(FeMoco)

from

the

molybdenum-dependent

nitrogenases

[36,124–126],

two

major

homogeneous catalytic systems have been developed thus far: those based on Mo and Fe [127,128]. It is worth noting that many low-valent transition metal complexes are known to bind and activate N 2 and subsequently liberate NH3 upon protonation; however, the vast majority of these systems only offer stoichiometric, or sub-stoichiometric, conversion [129,130]. Our discussion here will focus on Group 6 and 8 transition metal complexes that are catalytic for dinitrogen to ammonia conversion.

3.2.3.1 Catalytic homogeneous systems with group 6 transition metals

Major advancements towards homogeneous ammonia production were made in the 1960s with the synthesis of Group 6 dinitrogen complexes featuring bidentate phosphines ligands were pioneered by Joseph Chatt, among others, which showed synthesis of ammonia from nitrogen, albeit not catalytically [131]. Reduction of nitrogen to ammonia was first achieved in a catalytic fashion in the seminal report from Yandulov and Schrock in 2003, with the development of a monometallic Mo complex featuring a trisamidate ligand with bulky hexaisopropylterphenyl (HIPT) groups (Figure 16, top) [132]. The conversion to ammonia was accomplished catalytically by the controlled stepwise addition of protons and electrons rather than molecular hydrogen, although H 2 is produced as a side-product. The use of protons and electrons as opposed to molecular hydrogen was unique, and set the standard for future dinitrogen reduction catalytic systems. Subsequent structural and computational studies support a monometallic mechanism involving distal protonation of a terminal N 2 ligand, followed by N–N bond scission to release one equivalent of NH3 and a MoVI nitrido species [133–135]; the proposed mechanism is shown below in Figure 16.

Figure 16. Mo-based NH3 generation catalysts

Schrock’s success using Mo was followed by other reports, most notably those published by Nishibayashi et al. in 2011 [136]. This system utilized a low-valent Mo(0) center supported by a PNP pincer ligand, in contrast to the higher valent Mo intermediates observed for the Schrock system. The Nishibiyashi system generates more equivalents of NH3/Mo before catalyst death; however, the mechanism remains unclear as only the structure of the resting state after initial reduction of the (PNP)MoCl 3 starting material is known (Figure 16, bottom) [137]. The combination of protons and electrons rather than molecular hydrogen is used here as in the Schrock system with the source of acid and electrons similar to previous reports. Of note, the Nishibayashi system utilizes a more mild reductant (Cp 2Co, E = –1.33 V vs. Fc/Fc+) [138] compared to the Schrock system (Na/Hg, E = –2.36 V vs. Fc/Fc+). A subsequent report using a cationic MoVN supported by a PPP version of this ligand shows a maximum TON of 63 equiv. NH 3/Mo [139].

3.2.3.2 Catalytic homogeneous systems with group 8 transition metals Nearly 100 years after the development of the Haber-Bosch process, catalytic ammonia production from homogeneous Fe systems was finally achieved in 2013 by J. Peters et al. featuring low-valent Fe center supported by a trisphosphine donor ligand with an apical heteroatom, E (Figure 17 top, E=B, Si, C, N) [140,141]. The structural and vibrational data on the isolated formally Fe(0) and Fe(-I) terminal N2 complexes evidence significant activation of the N2 triple bond. Catalytic NH3 production is achieved for these systems at -78°C using strong reductants and acids, KC 8 and [H(Et2O)2]BArF4 respectively.

Expectedly, dihydrogen is an adventitious by-product of this reaction; however, the relative rate of N 2 reduction is competitive with H2 formation. Subsequent studies support a mechanism that proceeds through a primarily monometallic distal pathway (Figure 18) with protonation occurring at the -N of bound N2 [51,142,143]. Recently, Nishibayashi et al. have also developed a catalytic NH3 system featuring Fe and Co featuring an anionic PNP backbone (Figure 17, bottom) [144,145]. Catalysis is achieved using similar conditions to both Peters and the previous Mo system above. Another recent report shows that a previously-studied system, (dppe)2Fe0(N2) exclusively produces N2H4 from N2 catalytically, and not NH3 [146–148].

Figure 17. Catalytic activity of homogeneous Fe-based NH3.

Figure 18. Mechanism of ammonia production from the monometallic catalysts. M=Mo, Fe, Co.

Certain homogeneous systems have also been shown to catalytically convert N 2 into N(SiMe3)3. Since the SiMe3 group is, essentially, “a bulky proton”, the relevance to NH 3 is paramount, as are the mechanistic implications related to the design of future NH 3 catalysts. Some recent examples include a bimetallic Co system from C. Lu which produces N(SiMe3) catalytically from N2 and Me3SiCl and KC8 with a TON of 200 [149]. Included in this report is a mechanistic study with relevance to the distal protonation/reduction pathways observed for the previously mentioned Mo and Fe systems. Indeed, a related system to the (PNP)Mo system mentioned above has also been shown to generate N(SiMe3)3 as well as other silylated amines. Here, a disilane is used in addition to Me 3SiCl to generate tetramethylazadisilacyclopentane [150,151]. This result is noteworthy since R3Si-H represents a deviation from the previously applied method of protonation followed by reduction, instead resulting from formally oxidative addition of the SiH bond. Although the generation of the active catalyst, (PNP)Mo(N), proceeds via initial reduction of (PNP)MoCl3 (and subsequent N2 cleavage), no additional reducing equivalents are consumed in the reaction (Figure 19). This represents an important advancement towards to catalytic homogeneous fixation of dinitrogen, not only to catalytic ammonia production.

Figure 19. Catalytic Silylation of N2 by a (PPP)Mo catalyst.

The culmination of these studies shows the current TON/TOF values for homogeneous Fe nitrogen reduction catalysts to be SS>Ag>Fe>Cu>Al>Zn in glow discharge plasma. Shigeyuki et al. [201] reported that the iron wire gives higher ammonia concentration than the molybdenum wires in RF discharge and MW discharge. Dielectric barrier discharge plasma reactor is widely reported for screening of catalysts for ammonia synthesis. Bai et al. [210] smeared MgO on the electrode surface in DBD reactor and realized its improved performance. Mizushima et al. [211] employed catalytic membrane integrated in dielectric barrier discharge reactor, which gave catalytic activity in following order Ru>Ni>Pt>Fe>only alumina membrane. A localized production of ammonia assisted by plasma might lead to non-conventional applications such as in the NOx abatement and as energy storage or fuel [9,208].

4 1.

REFERENCES UNEP and WHRC (2007) Reactive Nitrogen in the Environment: Too Much or Too Little of a Good Thing. United Nations Environ. Program.

2.

Smil, V. (2002) Nitrogen and food production: proteins for human diets. Ambio, 31 (2), 126–131.

3.

Galloway, J.N., and Cowling, E.B. (2002) Reactive nitrogen and the world: 200 years of change.

Ambio, 31 (2), 64–71. 4.

Chanway, C.P.P., Anand, R., Yang, H., and Edited by Takuji Ohyama (2014) Nitrogen Fixation Outside and Inside Plant Tissues, in Advances in Biology and Ecology of Nitrogen Fixation, InTech, pp. 3–21.

5.

D.F.Bezdicek, and A.C.Kennedy (1998) Microorganisms in action, Blackwell Scientific Publications.

6.

Canfield, D.E., Glazer, A.N., and Falkowski, P.G. (2010) The evolution and future of Earth’s nitrogen cycle. Science (80-. )., 330 (6001), 192–6.

7.

Galloway, J.N., Townsend, A.R., Erisman, J.W., et al. (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science, 320 (5878), 889–892.

8.

Galloway, J.N. (1998) The global nitrogen cycle: changes and consequences. Environ. Pollut., 102 (1), 15–24.

9.

Patil, B.S., Wang, Q., Hessel, V., and Lang, J. (2015) Plasma N2-fixation: 1900–2014. Catal.

Today, 256, 49–66. 10.

Smil, V. (2004) Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World

Food Production, MIT Press. 11.

Modak, J.M. (2002) Haber Process for Ammonia Synthesis. Resonance, (August), 69–77.

12.

Nørskov, J., Contacts, B., Miranda, R., et al. (2016) Sustainable Ammonia Synthesis Exploring the scientific challenges associated with discovering alternative, sustainable processes for ammonia production DOE Roundtable Report SUSTAINABLE AMMONIA SYNTHESIS.

13.

Kessler, P.S., McLarnan, J., and Leigh, J.A. (1997) Nitrogenase phylogeny and the molybdenum dependence of nitrogen fixation in Methanococcus maripaludis. J. Bacteriol., 179 (2), 541–543.

14.

Boyd, E.S., and Peters, J.W. (2011) An alternative path for the evolution of biological nitrogen fixation. Front. Microbiol. Chem., 2, 205.

15.

Boyd, E.S., Anbar, A.D., Miller, S., et al. (2011) A late methanogen origin for molybdenumdependent nitrogenase. Geobiology, 9 (3), 221–232.

16.

Dos Santos, P.C., Fang, Z., Mason, S.W., et al. (2012) Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics, 13 (1), 162.

17.

Burgess, B.K., and Lowe, D.J. (1996) Mechanism of molybdenum nitrogenase. Chem. Rev., 96 (7), 2983–3012.

18.

Eady, R.R. (1996) Structure−function relationships of alternative nitrogenases. Chem. Rev., 96 (7), 3013–3030.

19.

Lee, C.C., Hu, Y., and Ribbe, M.W. (2009) Unique features of the nitrogenase VFe protein from

Azotobacter vinelandii. Proc. Natl. Acad. Sci. U. S. A., 106 (23), 9209–9214. 20.

Kim, J., and Rees, D.C. (1992) Structural models for the metal centers in the nitrogenase molybdenum-iron protein. Science (80-. )., 257 (5077), 1677–1682.

21.

Kim, J., and Rees, D.C. (1992) Crystallographic structure and functional implications of the nitrogenase molybdenum-iron protein from Azotobacter vinelandii. Nature, 360 (6404), 553–560.

22.

Chan, M.K., Kim, J., and Rees, D.C. (1993) The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 Å resolution structures. Science (80-. )., 260 (5109), 792–794.

23.

Shah, V.K., and Brill, W.J. (1977) Isolation of an iron-molybdenum cofactor from nitrogenase.

Proc. Natl. Acad. Sci. U. S. A., 74 (8), 3249–3253. 24.

Chan, J.M., Christiansen, J., Dean, D.R., and Seefeldt, L.C. (1999) Spectroscopic evidence for changes in the redox state of the nitrogenase P-cluster during turnover. Biochemistry, 38 (18), 5779–5785.

25.

Georgiadis, M.M., Komiya, H., Chakrabarti, P., et al. (1992) Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science (80-. )., 257 (5077), 1653–1659.

26.

Thorneley, R.N.F., and Lowe, D.J. (1985) Kinetics and mechanism of the nitrogenase enzyme, in

Molybdenum Enzymes, vol. 7, Wiley-Interscience Publications, New York, pp. 221–284. 27.

Hageman, R. V, and Burris, R.H. (1978) Nitrogenase and nitrogenase reductase associate and dissociate with each catalytic cycle. Proc. Natl. Acad. Sci. U. S. A., 75 (6), 2699–2702.

28.

Schindelin, H., Kisker, C., Schlessman, J.L., et al. (1997) Structure of ADP x AIF4(-)-stabilized nitrogenase complex and its implications for signal transduction. Nature, 387 (6631), 370–376.

29.

Chiu, H., Peters, J.W., Lanzilotta, W.N., et al. (2001) MgATP-Bound and nucleotide-free structures of a nitrogenase protein complex between the Leu 127 Delta-Fe-protein and the MoFe-protein.

Biochemistry, 40 (3), 641–650. 30.

Tezcan, F.A., Kaiser, J.T., Mustafi, D., et al. (2005) Nitrogenase complexes: multiple docking sites

for a nucleotide switch protein. Science, 309 (5739), 1377–1380. 31.

Duval, S., Danyal, K., Shaw, S., et al. (2013) Electron transfer precedes ATP hydrolysis during nitrogenase catalysis. Proc. Natl. Acad. Sci., 110, 16414–16419.

32.

Danyal, K., Dean, D.R., Hoffman, B.M., and Seefeldt, L.C. (2011) Electron transfer within nitrogenase: evidence for a deficit-spending mechanism. Biochemistry, 50 (43), 9255–9263.

33.

Danyal, K., Shaw, S., Page, T.R., et al. (2016) Negative cooperativity in the nitrogenase Fe protein electron delivery cycle. Proc. Natl. Acad. Sci., 113, E5783–E5791.

34.

Yang, Z.-Y., Ledbetter, R., Shaw, S., et al. (2016) Evidence that the Pi release event is the ratelimiting step in the nitrogenase catalytic cycle. Biochemistry, 55, 3625–3635.

35.

Rivera-Ortiz, J.M., and Burris, R.H. (1975) Interactions among substrates and inhibitors of nitrogenase. J. Bacteriol., 123 (2), 537–545.

36.

Hoffman, B.M., Lukoyanov, D., Yang, Z.-Y., et al. (2014) Mechanism of nitrogen fixation by nitrogenase: the next stage. Chem. Rev., 114 (8), 4041–4062.

37.

Hoffman, B.M., Lukoyanov, D., Dean, D.R., and Seefeldt, L.C. (2013) Nitrogenase: a draft mechanism. Acc. Chem. Res., 46 (2), 587–595.

38.

Hoffman, B.M., Dean, D.R., and Seefeldt, L.C. (2009) Climbing nitrogenase: toward a mechanism of enzymatic nitrogen fixation. Acc. Chem. Res., 42 (5), 609–619.

39.

Igarashi, R.Y., Laryukhin, M., Dos Santos, P.C., et al. (2005) Trapping H- bound to the nitrogenase FeMo-cofactor active site during H2 evolution: characterization by ENDOR spectroscopy. J. Am.

Chem. Soc., 127 (17), 6231–6241. 40.

Lukoyanov, D., Barney, B.M., Dean, D.R., et al. (2007) Connecting nitrogenase intermediates with the kinetic scheme for N2 reduction by a relaxation protocol and identification of the N2 binding state. Proc. Natl. Acad. Sci. U. S. A., 104 (5), 1451–1455.

41.

Barney, B.M., Lukoyanov, D., Igarashi, R.Y., et al. (2009) Trapping an intermediate of dinitrogen (N2) reduction on nitrogenase. Biochemistry, 48 (38), 9094–9102.

42.

Lukoyanov, D., Dikanov, S.A., Yang, Z.-Y., et al. (2011) ENDOR/HYSCORE studies of the common intermediate trapped during nitrogenase reduction of N2H2, CH3N2H, and N2H4 support an alternating reaction pathway for N2 reduction. J. Am. Chem. Soc., 133 (30), 11655–11664.

43.

Lukoyanov, D., Yang, Z.-Y., Barney, B.M., et al. (2012) Unification of reaction pathway and kinetic scheme for N2 reduction catalyzed by nitrogenase. Proc. Natl. Acad. Sci., 109, 5583–5587.

44.

Yang, Z.-Y., Khadka, N., Lukoyanov, D., et al. (2013) On reversible H2 loss upon N2 binding to

FeMo-cofactor of nitrogenase. Proc. Natl. Acad. Sci., 110, 16327–16332. 45.

Lukoyanov, D., Yang, Z.-Y., Duval, S., et al. (2014) A confirmation of the quench-cryoannealing relaxation protocol for identifying reduction states of freeze-trapped nitrogenase intermediates.

Inorg. Chem., 53, 3688–3693. 46.

Lukoyanov, D., Yang, Z.-Y., Khadka, N., et al. (2015) Identification of a key catalytic intermediate demonstrates that nitrogenase is activated by the reversible exchange of N 2 for H2. J. Am. Chem.

Soc., 137 (10), 3610–3615. 47.

Lukoyanov, D., Khadka, N., Yang, Z.-Y., et al. (2016) Reductive elimination of H2 activates nitrogenase to reduce the N≡N triple bond: characterization of the E4(4H) Janus intermediate in wild-type enzyme. J. Am. Chem. Soc., 138 (33), 10674–10683.

48.

Lukoyanov, D., Khadka, N., Yang, Z.-Y., et al. (2016) Reversible photoinduced reductive elimination of H2 from the nitrogenase dihydride state, the E4(4H) Janus intermediate. J. Am.

Chem. Soc., 138 (4), 1320–1327. 49.

Lukoyanov, D., Khadka, N., Dean, D.R., et al. (2017) Photoinduced reductive elimination of H 2 from the nitrogenase dihydride (Janus) state involves a FeMo-cofactor-H2 intermediate. Inorg.

Chem., 56 (4), 2233–2240. 50.

Rittle, J., and Peters, J.C. (2016) An Fe-N2 complex that generates hydrazine and ammonia via Fe=NNH2: Demonstrating a hybrid distal-to-alternating pathway for N2 reduction. J. Am. Chem.

Soc., 138, 4243–4248. 51.

Anderson, J.S., Cutsail III, G.E., Rittle, J., et al. (2015) Characterization of an Fe≡N-NH2 Intermediate Relevant to Catalytic N2 Reduction to NH3. J. Am. Chem. Soc., 137, 7803–7809.

52.

Jensen, B.B., and Burris, R.H. (1985) Effect of high pN2 and high pD2 on NH3 production, H2 evolution, and HD formation by nitrogenases. Biochemistry, 24 (5), 1141–1147.

53.

Guth, J.H., and Burris, R.H. (1983) Inhibition of nitrogenase-catalyzed NH3 formation by H2.

Biochemistry, 22 (22), 5111–5122. 54.

Perutz, R.N., and Procacci, B. (2016) Photochemistry of transition metal hydrides. Chem. Rev., 116 (15), 8506–8544.

55.

Frost, D.C., and McDowell, C.A. (1956) The dissociation energy of the nitrogen moolecule. R. Soc.

London. Math. Phys. Sci., A, 278–284. 56.

Ernst, F.A. (1928) Fixation of atmospheric nitrogen. Ind. Chem. Monogr., (USA).

57.

Egeland, A., and Burke, W.J. (2005) Kristian Birkeland the first space scientist , Springer,

Dordrecht, The Netherlands. 58.

Birkeland, K.R. (1906) ON THE OXIDATION OF ATMOSPHERIC NITROGEN IN ELECTRIC ARCS .

Trans. Faraday Soc., 2, 98–116. 59.

Maxwell, G.R. (2004) Synthetic Nitrogen Products- A Practical Guide to the Products and

Processes, Kluwer Academic Publishers, New York. 60.

Travis, A.S. (2015) The Synthetic Nitrogen Industry in World War I: Its Emergence and Expansion , Springer, Fargo, North Dakota, USA.

61.

Appl, M. (2012) Ammonia, 2. Production Processes. Ullmann’s Encycl. Ind. Chem., 139–225.

62.

Appl, M. (1997) The Haber-Bosch Heritage: The Ammonia Production Technology. 50th Anniv. IFA

Tech. Conf., 25. 63. 64.

(2005) Ammonia Safety Symposium : Ammonia Timeline. Chem. Eng. Prog., (June), 57–62. Krebs, R.E. (2006) The History and Use of Our Earth’s Chemical Elements: A Reference Guide, Greenwood Press, Westport.

65.

Leigh, G.J. (2002) Nitrogen Fixation at the Millennium, Elsevier Science.

66.

International Energy Agency-IEA (2013) Technology Roadmap: Energy and GHG Reductions in the Chemical Industry via Catalytic Processes.

67.

Thiemann, M., Scheibler, E., and Wiegand, K.W. (2000) Nitric Acid, Nitrous Acid, and Nitrogen Oxides, in Ullmann’s Encyclopedia of Industrial Chemistry, Wiley-VCH Verlag GmbH & Co. KGaA.

68.

Smil, V. (1997) Global Population and the Nitrogen Cycle. Sci. Am., (July), 76–81.

69.

Smil, V. (1999) Detonator of the population explosion. Nature, 400 (6743), 415.

70.

2017, U.S.G.S. (2017) Mineral commodity summaries 2017. U.S. Geol. Surv., 202.

71.

Smith, V. (2004) Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World Food Production. MIT Press.

72.

Liu, H. (2014) Ammonia synthesis catalyst 100 years: Practice, enlightenment and challenge.

Chinese J. Catal., 35 (10), 1619–1640. 73.

Schlögl, R. (2003) Catalytic Synthesis of Ammonia—A “Never-Ending Story”? Angew. Chemie Int.

Ed., 42 (18), 2004–2008. 74.

Shannon, I.R. (1978) The synthesis of ammonia and related reactions. 2, 28–45.

75.

Zheng Xiaoling, W.K. (2001) The Second Generation Catalysis System for Ammonia Synthesis¡a¡aRuthenium-based Ammonia Synthesis Catalyst and Its Industrial Application. Prog.

Chem., 13 (6), 473–480. 76.

Rodriguez, M.M., Bill, E., Brennessel, W.W., and Holland, P.L. (2011) . Science (80-. )., 334 (6057), 780–783.

77.

Asatryan, R., Bozzelli, J.W., Silva, G. da, et al. (2010) Formation and Decomposition of Chemically Activated and Stabilized Hydrazine. J. Phys. Chem. A, 114 (21), 6235–6249.

78.

Hellman, A., Baerends, E.J., Biczysko, M., et al. (2006) Predicting Catalysis:  Understanding Ammonia Synthesis from First-Principles Calculations. J. Phys. Chem. B, 110 (36), 17719–17735.

79.

Bielawa, H., Hinrichsen, O., Birkner, A., and Muhler, M. (2001) The Ammonia-Synthesis Catalyst of the Next Generation: Barium-Promoted Oxide-Supported Ruthenium. Angew. Chemie Int. Ed., 40 (6), 1061–1063.

80.

Jacobsen, C.J.H., Dahl, S., Hansen, P.L., et al. (2000) Structure sensitivity of supported ruthenium catalysts for ammonia synthesis. J. Mol. Catal. A Chem., 163, 19–26.

81.

Dahl, S., Sehested, J., Jacobsen, C.J.H., et al. (2000) Surface science based microkinetic analysis of ammonia synthesis over ruthenium catalysts. J. Catal., 192 (2), 391–399.

82.

Dahl, S., Taylor, P.A., Törnqvist, E., and Chorkendorff, I. (1998) The Synthesis of Ammonia over a Ruthenium Single Crystal. J. Catal., 178 (2), 679–686.

83.

Dahl, S., Tornqvist, E., and Chorkendoff, I. (2000) Dissociative Adsorption of N2 on Ru (0001): A Surface Reaction Totally Dominated by Steps. J. Catal., 390 (192), 381–390.

84.

Dahl, S., Logadottir, A., Egeberg, R.C., et al. (1999) Role of Steps in ${\mathrm{N}}_{2}$ Activation on Ru(0001). Phys. Rev. Lett., 83 (9), 1814–1817.

85.

Aika, K. (1986) Heterogeneous Catalysis of Ammonia Synthesis at Room Temperature and Atmospheric Pressure. Angew. Chemie Int. Ed. English, 25 (6), 558–559.

86.

Kotarba, A., Dmytrzyk, J., Raróg-Pilecka, W., and Kowalczyk, Z. (2003) Surface heterogeneity and ionization of Cs promoter in carbon-based ruthenium catalyst for ammonia synthesis. Appl. Surf.

Sci., 207 (1–4), 327–333. 87.

Choe, J.S., and Kellogg, L.J. (1995) Membrane-assisted process to produce ammonia.

88.

Michalsky, R., Avram, A.M., Peterson, B.A., et al. (2015) Chemical looping of metal nitride catalysts: low-pressure ammonia synthesis for energy storage. Chem. Sci., 6 (7), 3965–3974.

89.

Vojvodic, A., Medford, A.J., Studt, F., et al. (2014) Exploring the limits: A low-pressure, lowtemperature Haber–Bosch process. Chem. Phys. Lett., 598, 108–112.

90.

Li, X.-F., Li, Q.-K., Cheng, J., et al. (2016) Conversion of Dinitrogen to Ammonia by FeN3Embedded Graphene. J. Am. Chem. Soc., 138 (28), 8706–8709.

91.

Norskov Jingguang; Miranda, Raul; Singh, Aayuash; Rohr, Brian; Goldstein, Julia, J.C. (2016) Sustainable Ammonia Synthesis, DOE Roundtable Report. U.S. Dep. Energy, Off. Sci., 1–21.

92.

Erisman, J.W., Sutton, M.A., Galloway, J., et al. (2008) How a century of ammonia synthesis changed the world. Nat. Geosci., 1, 636–9.

93.

Patil, B.S., Wang, Q., Hessel, V., and Lang, J. (2016) Plasma Assisted Nitrogen Fixation Reactions, in Alternative Energy Sources For Green Chemistry (eds.Stefanidis, G.D., and Stankiewicz, A.), Royal Society of Chemistry, Cambridge, UK.

94.

Becker, J.Y., and Posin, B. (1988) Nitrogen fixation. J. Electroanal. Chem. Interfacial Electrochem., 250 (2), 385–397.

95.

Rosca, V., Duca, M., de Groot, M.T., and Koper, M.T.M. (2009) Nitrogen Cycle Electrocatalysis.

Chem. Rev., 109 (6), 2209–2244. 96.

van der Ham, C.J.M., Koper, M.T.M., and Hetterscheid, D.G.H. (2014) Challenges in reduction of dinitrogen by proton and electron transfer. Chem. Soc. Rev., 43 (15), 5183–5191.

97.

Giddey, S., Badwal, S.P.S., and Kulkarni, A. (2013) Review of electrochemical ammonia production technologies and materials. Int. J. Hydrogen Energy, 38 (34), 14576–14594.

98.

Kordali, V., Kyriacou, G., and Lambrou, C. (2000) Electrochemical synthesis of ammonia at atmospheric pressure and low temperature in a solid polymer electrolyte cell. Chem. Commun., (17), 1673–1674.

99.

Lan, R., Irvine, J.T.S., and Tao, S. (2012) Ammonia and related chemicals as potential indirect hydrogen storage materials. Int. J. Hydrogen Energy, 37 (2), 1482–1494.

100.

Lan, R., Irvine, J.T.S., and Tao, S. (2013) Synthesis of ammonia directly from air and water at ambient temperature and pressure. Sci. Rep., 3, 1145.

101.

Lan, R., Alkhazmi, K.A., Amar, I.A., and Tao, S. (2014) Synthesis of ammonia directly from wet air at intermediate temperature. Appl. Catal. B Environ., 152–153, 212–217.

102.

Marnellos, G., and Stoukides, M. (1998) Ammonia Synthesis at Atmospheric Pressure. Science (80-

. )., 282 (5386), 98–100. 103.

Amar, I.A., Petit, C.T.G., Zhang, L., et al. (2011) Electrochemical synthesis of ammonia based on doped-ceria-carbonate composite electrolyte and perovskite cathode. Solid State Ionics, 201 (1), 94–100.

104.

Murakami, T., Nohira, T., Goto, T., et al. (2005) Electrolytic ammonia synthesis from water and nitrogen gas in molten salt under atmospheric pressure. Electrochim. Acta, 50 (27), 5423–5426.

105.

Köleli, F., and Röpke, T. (2006) Electrochemical hydrogenation of dinitrogen to ammonia on a polyaniline electrode. Appl. Catal. B Environ., 62 (3–4), 306–310.

106.

Pospíšil, L., Hromadová, M., Gál, M., et al. (2008) Electrochemical impedance of nitrogen fixation mediated by fullerene–cyclodextrin complex. Electrochim. Acta, 53 (25), 7445–7450.

107.

Pospisil, L., Bulickova, J., Hromadova, M., et al. (2007) Electrochemical conversion of dinitrogen to ammonia mediated by a complex of fullerene C60 and [gamma]-cyclodextrin. Chem. Commun., (22), 2270–2272.

108.

Skodra, A., and Stoukides, M. (2009) Electrocatalytic synthesis of ammonia from steam and nitrogen at atmospheric pressure. Solid State Ionics, 180 (23–25), 1332–1336.

109.

Hong, J., Prawer, S., and Murphy, A.B. (2014) Production of Ammonia by Heterogeneous Catalysis in a Packed-Bed Dielectric-Barrier Discharge : Influence of Argon Addition and Voltage. IEEE

Trans. PLASMA Sci., 42 (10), 2338–2339. 110.

Kitano, M., Inoue, Y., Yamazaki, Y., et al. (2012) Ammonia synthesis using a stable electride as an electron donor and reversible hydrogen store. Nat. Chem., 4 (11), 934–40.

111.

Pickett, C.J., and Talarmin, J. (1985) Electrosynthesis of ammonia. Nature, 317 (6038), 652–653.

112.

Fenwick, A.Q., Gregoire, J.M., and Luca, O.R. (2015) Electrocatalytic Reduction of Nitrogen and Carbon Dioxide to Chemical Fuels: Challenges and Opportunities for a Solar Fuel Device. J.

Photochem. Photobiol. B Biol., 152, Part A, 47–57. 113.

Bickley, R.I., and Vishwanathan, V. (1979) Photocatalytically induced fixation of molecular nitrogen by near UV radiation. Nature, 280 (5720), 306–308.

114.

Schrauzer, G.N., Strampach, N., Hui, L.N., et al. (1983) Nitrogen photoreduction on desert sands under sterile conditions. Proc. Natl. Acad. Sci., 80 (12), 3873–3876.

115.

Schrauzer, G.N., and Guth, T.D. (1977) Photocatalytic reactions. 1. Photolysis of water and photoreduction of nitrogen on titanium dioxide. J. Am. Chem. Soc., 99 (22), 7189–7193.

116.

Ranjit, K.T., Varadarajan, T.K., and Viswanathan, B. (1996) Photocatalytic reduction of dinitrogen to ammonia over noble-metal-loaded TiO2. J. Photochem. Photobiol. A Chem., 96 (1), 181–185.

117.

Miyama, H., Fujii, N., and Nagae, Y. (1980) Heterogeneous photocatalytic synthesis of ammonia from water and nitrogen. Chem. Phys. Lett., 74 (3), 523–524.

118.

Zheng, Y., Jensen, A.D., Glarborg, P., et al. (2009) Heterogeneous fixation of N2: Investigation of

a novel mechanism for formation of NO. Proc. Combust. Inst., 32 (2), 1973–1980. 119.

Janet, C.M., Navaladian, S., Viswanathan, B., et al. (2010) Heterogeneous Wet Chemical Synthesis of Superlattice-Type Hierarchical ZnO Architectures for Concurrent H2 Production and N2 Reduction. J. Phys. Chem. C, 114 (6), 2622–2632.

120.

Bai, Y., Ye, L., Chen, T., et al. (2016) Facet-Dependent Photocatalytic N2 Fixation of Bismuth-Rich Bi5O7I Nanosheets. ACS Appl. Mater. Interfaces, 8 (41), 27661–27668.

121.

Zhu, D., Zhang, L., Ruther, R.E., and Hamers, R.J. (2013) Photo-illuminated diamond as a solidstate source of solvated electrons in water for nitrogen reduction. Nat Mater, 12 (9), 836–841.

122.

Lu, Y., Yang, Y., Zhang, T., et al. (2016) Photoprompted Hot Electrons from Bulk Cross-Linked Graphene Materials and Their Efficient Catalysis for Atmospheric Ammonia Synthesis. ACS Nano, 10 (11), 10507–10515.

123.

Jia, H.-P., and Quadrelli, E.A. (2014) Mechanistic aspects of dinitrogen cleavage and hydrogenation to produce ammonia in catalysis and organometallic chemistry: relevance of metal hydride bonds and dihydrogen. Chem. Soc. Rev., 43 (2), 547–564.

124.

Li, Y., Li, Y., Wang, B., et al. (2013) Ammonia formation by a thiolate-bridged diiron amide complex as a nitrogenase mimic. Nat Chem, 5 (4), 320–326.

125.

Liu, J., Kelley, M.S., Wu, W., et al. (2016) Nitrogenase-mimic iron-containing chalcogels for photochemical reduction of dinitrogen to ammonia. Proc. Natl. Acad. Sci., 113 (20), 5530–5535.

126.

Čorić, I., and Holland, P.L. (2016) Insight into the Iron–Molybdenum Cofactor of Nitrogenase from Synthetic Iron Complexes with Sulfur, Carbon, and Hydride Ligands. J. Am. Chem. Soc., 138 (23), 7200–7211.

127.

Sivasankar, C., Baskaran, S., Tamizmani, M., and Ramakrishna, K. (2014) Lessons learned and lessons to be learned for developing homogeneous transition metal complexes catalyzed reduction of N2 to ammonia. J. Organomet. Chem., 752, 44–58.

128.

Tanabe, Y., and Nishibayashi, Y. (2013) Developing more sustainable processes for ammonia synthesis. Coord. Chem. Rev., 257 (17–18), 2551–2564.

129.

Fryzuk, M.D. (2009) Side-on End-on Bound Dinitrogen: An Activated Bonding Mode That Facilitates Functionalizing Molecular Nitrogen. Acc. Chem. Res., 42 (1), 127–133.

130.

Bazhenova, T.A., and Shilov, A.E. (1995) Nitrogen fixation in solution. Coord. Chem. Rev., 144, 69–145.

131.

Chatt, J., Dilworth, J.R., and Richards, R.L. (1978) Recent advances in the chemistry of nitrogen

fixation. Chem. Rev., 78 (6), 589–625. 132.

Yandulov, D. V, and Schrock, R.R. (2003) Catalytic reduction of dinitrogen to ammonia at a single molybdenum center. Science, 301 (5629), 76–8.

133.

Schenk, S., Le Guennic, B., Kirchner, B., and Reiher, M. (2008) First-Principles Investigation of the Schrock Mechanism of Dinitrogen Reduction Employing the Full HIPTN3N Ligand. Inorg. Chem., 47 (9), 3634–3650.

134.

Thimm, W., Gradert, C., Broda, H., et al. (2015) Free Reaction Enthalpy Profile of the Schrock Cycle Derived from Density Functional Theory Calculations on the Full [MoHIPTN3N] Catalyst.

Inorg. Chem., 54 (19), 9248–9255. 135.

Schrock, R.R. (2008) Catalytic Reduction of Dinitrogen to Ammonia by Molybdenum: Theory versus Experiment. Angew. Chemie Int. Ed., 47 (30), 5512–5522.

136.

Arashiba, K., Miyake, Y., and Nishibayashi, Y. (2011) A molybdenum complex bearing PNP-type pincer ligands leads to the catalytic reduction of dinitrogen into ammonia. Nat Chem, 3 (2), 120– 125.

137.

Kuriyama, S., Arashiba, K., Nakajima, K., et al. (2014) Catalytic Formation of Ammonia from Molecular Dinitrogen by Use of Dinitrogen-Bridged Dimolybdenum–Dinitrogen Complexes Bearing PNP-Pincer Ligands: Remarkable Effect of Substituent at PNP-Pincer Ligand. J. Am. Chem. Soc., 136 (27), 9719–9731.

138.

Connelly, N.G., and Geiger, W.E. (1996) Chemical Redox Agents for Organometallic Chemistry.

Chem. Rev., 96 (2), 877–910. 139.

Arashiba, K., Kinoshita, E., Kuriyama, S., et al. (2015) Catalytic Reduction of Dinitrogen to Ammonia by Use of Molybdenum–Nitride Complexes Bearing a Tridentate Triphosphine as Catalysts. J. Am. Chem. Soc., 137 (17), 5666–5669.

140.

Anderson, J.S., Rittle, J., and Peters, J.C. (2013) Catalytic conversion of nitrogen to ammonia by an iron model complex. Nature, 501 (7465), 84–87.

141.

Del Castillo, T.J., Thompson, N.B., Suess, D.L.M., et al. (2015) Evaluating Molecular Cobalt Complexes for the Conversion of N2 to NH3. Inorg. Chem., 54 (19), 9256–9262.

142.

Ung, G., and Peters, J.C. (2015) Low-Temperature N2 Binding to Two-Coordinate L2Fe0 Enables Reductive Trapping of L2FeN2− and NH3 Generation. Angew. Chemie, 127 (2), 542–545.

143.

Creutz, S.E., and Peters, J.C. (2017) Exploring secondary-sphere interactions in Fe-NxHy complexes relevant to N2 fixation. Chem. Sci.

144.

Kuriyama, S., Arashiba, K., Tanaka, H., et al. (2016) Direct Transformation of Molecular Dinitrogen into Ammonia Catalyzed by Cobalt Dinitrogen Complexes Bearing Anionic PNP Pincer Ligands.

Angew. Chemie Int. Ed., 55 (46), 14291–14295. 145.

Kuriyama, S., Arashiba, K., Nakajima, K., et al. (2016) Catalytic transformation of dinitrogen into ammonia and hydrazine by iron-dinitrogen complexes bearing pincer ligand. Nat. Commun., 7, 12181.

146.

Komiya, S., Akita, M., Yoza, A., et al. (1993) Isolation of a zerovalent iron dinitrogen complex with 1,2-bis(diethylphosphino)ethane ligands. J. Chem. Soc. Chem. Commun., (9), 787–788.

147.

Yelle, R.B., Crossland, J.L., Szymczak, N.K., and Tyler, D.R. (2009) Theoretical Studies of N2 Reduction to Ammonia in Fe(dmpe)2N2. Inorg. Chem., 48 (3), 861–871.

148.

Doyle, L.R., Hill, P.J., Wildgoose, G.G., and Ashley, A.E. (2016) Teaching old compounds new tricks: efficient N2 fixation by simple Fe(N2)(diphosphine)2 complexes. Dalt. Trans., 45 (18), 7550–7554.

149.

Siedschlag, R.B., Bernales, V., Vogiatzis, K.D., et al. (2015) Catalytic Silylation of Dinitrogen with a Dicobalt Complex. J. Am. Chem. Soc., 137 (14), 4638–4641.

150.

Liao, Q., Saffon-Merceron, N., and Mézailles, N. (2015) N2 Reduction into Silylamine at Tridentate Phosphine/Mo Center: Catalysis and Mechanistic Study. ACS Catal., 5 (11), 6902–6906.

151.

Liao, Q., Cavaillé, A., Saffon-Merceron, N., and Mézailles, N. (2016) Direct Synthesis of Silylamine from N2 and a Silane: Mediated by a Tridentate Phosphine Molybdenum Fragment. Angew.

Chemie Int. Ed., 55 (37), 11212–11216. 152.

Samukawa, S., Hori, M., Rauf, S., et al. (2012) The 2012 Plasma Roadmap. J. Phys. D. Appl.

Phys., 45 (25), 253001. 153.

Ingels, R., Graves, D., Anderson, S., and Koller, R. (2015) Modern Plasma Technology for Nitrogen Fixation: New Opportunities? Int. Fertil. Soc., (771), 1–27.

154.

Cherkasov, N., Ibhadon, A.O., and Fitzpatrick, P. (2015) A review of the existing and alternative methods for greener nitrogen fixation. Chem. Eng. Process. Process Intensif., 90, 24–33.

155.

Hessel, V., Cravotto, G., Fitzpatrick, P., et al. (2013) Industrial applications of plasma , microwave and ultrasound techniques : Nitrogen-fixation and hydrogenation reactions. Chem. Eng. Process.

Process Intensif., 71, 19–30. 156.

Patil, B.S. (2017) Plasma (Catalyst) – Assisted Nitrogen Fixation : Reactor Development for Nitric Oxide and Ammonia Production.

157.

Hessel, V., Anastasopoulou, a., Wang, Q., et al. (2013) Energy, catalyst and reactor considerations for (near)-industrial plasma processing and learning for nitrogen-fixation reactions.

Catal. Today, 211, 9–28. 158.

Anastasopoulou, A., Butala, S., Lang, J., et al. (2016) Life Cycle Assessment of the Nitrogen Fixation Process Assisted by Plasma Technology and Incorporating Renewable Energy. Ind. Eng.

Chem. Res., 55 (29), 8141–8153. 159.

Anastasopoulou, A., Butala, S., Patil, B.S., et al. (2016) Techno-economic feasibility study of renewable power systems for a small scale plasma-assisted nitric acid plant in Kenya. Processes, 4 (4) (54).

160.

Fauchais, P., and Rakowitz, J. (1979) Physics on plasma chemistry. J. Phys., 40 (C7), C7-289-C7312.

161.

Neyts, E.C., and Bogaerts, a (2014) Understanding plasma catalysis through modelling and simulation—a review. J. Phys. D. Appl. Phys., 47 (22), 224010.

162.

Whitehead, J.C. (2016) Chapter 3 – The Chemistry of Cold Plasma, Elsevier Inc.

163.

Pollo, I., Hoffmann-Fedenczuk, K., and Fedenczuk, L. (1981) The influence of gas-inlet and quenching systems on the nitrogen oxides production in air plasmas. Int. Symp. Plasma Chem., 2, 756–760.

164.

Krop, J., and Pollo, I. (1980) Chemical reactors for synthesis of nitrogen oxide in low temperature of air plasma jet. II. Efficiency of nitrogen oxide synthesis in reactors with rotating disk. Chemia, 633 (92), 25–33.

165.

Namihira, T., Tsukamoto, S., Wang, D., et al. (1999) Production of nitric monoxide in dry air using pulsed discharge. 12th IEEE Int. Pulsed Power Conf. (Cat. No.99CH36358), 2, 1313–1316.

166.

Namihira, T., Katsuki, S., Hackam, R., et al. (2002) Production of nitric oxide using a pulsed arc discharge. Plasma Sci. IEEE Trans., 30 (5), 1993–1998.

167.

Patil, B.S., Rovira Palau, J., Hessel, V., et al. (2016) Plasma Nitrogen Oxides Synthesis in a MilliScale Gliding Arc Reactor: Investigating the Electrical and Process Prameters. Plasma Chemsiry

Plasma Process., 36, 241–257. 168.

Patil, B.S., Peeters, F.J.J., A., M.J., et al. (2017) Plasma nitrogen oxide production from air at atmospheric pressure using a pulse powered milli-scale gliding arc reactor. Submitt. to AIChEJ.

169.

Patil, B.S., Peeters, F.J.J., A., M.J., et al. (2017) Fertilizing With the Wind: Unravelling the Pulse Powered 2D Gliding Arc Reactor for Atmospheric Pressure Plasma Nitrogen Oxides Production in Containerized Fertilizer Plant. Submitt. to Energy Environ. Sci.

170.

Wang, W., Patil, B.S., Heijkers, S., et al. (2017) Nitrogen fixation by gliding arc plasma: Better insight by chemical kinetics modeling. ChemSusChem, 10, 1–14.

171.

Rapakoulias, D., Cavadias, S., and Amouroux, J. (1980) Processus catalytiques dans un réacteur à plasma hors d’équilibre II. Fixation de l’azote dans le système N2-O2. Rev. Phys. Appl., 15 (7), 1261–1265.

172.

Rapakoulias, D., and Amouroux, J. (1979) Réacteur de synthèse et de trempe dans un plasma hors d’équilibre : application à la synthèse de C2H2 et HCN. Rev. Phys. Appl., 14 (12), 961–968.

173.

Amouroux, J., Cavadias, S., and Rapakoulias, D. (1979) Réacteur de synthèse et de trempe dans un plasma hors d’équilibre : application à la synthèse des oxydes d’azote. Rev. Phys. Appl., 14, 969–976.

174.

Mutel, B., Dessaux, O., and Goudmand, P. (1984) Energy Cost Improvement of The Nitrogen Oxides Synthesis in a Low Pressure Plasma. Rev. Phys. Appl., 19, 461–464.

175.

Patil, B.S., Cherkasov, N., Lang, J., et al. (2016) Low temperature plasma-catalytic NOx synthesis in a packed DBD reactor: Effect of support materials and supported active metal oxides. Appl.

Catal. B Environ., 194, 123–133. 176.

Pollo, I., and Banasik, S. (1979) Some problems of energy utilization in a plasma reactor with a direct current argon plasma generator. Chemia, 631 (91), 377–8.

177.

Pollo, I., and Banasik, S. (1978) Experiments on the synthesis of nitric oxide in an argon plasma.

Chem. Plazmy, 259–270. 178.

Bequin, C.P., Ezell, J.B., Salvemini, A., et al. (1967) The application of plasma to chemical

synthesis, MIT Press, Cambridge, Massachussetts. 179.

LaRoche, M.J. (1955) La Chimie des hautes temperatures, CNRS, Paris.

180.

Jackson, K., and Bloom, M.S. (1963) British Patent. BP 915771, issued 1963.

181.

Partridge, W.S., Parlin, R.B., and Zwolinski, B.J. (1954) Fixation of Nitrogen in a Crossed Discharge. Ind. Eng. Chem., 46 (7), 1468–1471.

182.

Grosse, A.V., Stokes, C.S., Cahill, J.A., and Correa, J.J. (1961) Final Annual Report.

183.

Timmins, R., and Amman, P. (1970) Plasma Applications in Chemical Processes, Mir (World), Moscow.

184.

Coudert, J.F., Baronnet, J.M., Rakowitz, J., and Fauchais, P. (1977) Synthesis of nitrogen oxides in a plasma produced by a jet arc generator. Symp. Int. Chim. Plasmas, 1.

185.

Baronnet, J.M., Coudert, J.F., Rakowitz, J., et al. (1979) Nitrogen Oxides Synthesis In a D.C.

Plasma Jet. 4th Int. Symp. plasma Chem. 186.

Rahman, M., and Cooray, V. (2003) NOx generation in laser-produced plasma in air as a function of dissipated energy. Opt. Laser Technol., 35 (7), 543–546.

187.

Conrad, R.W. (1979) Nitrogen fixation with a high energy laser. US 4167463, issued 1979.

188.

Polak, L.S., Ovsiannikov, A.A., Slovetsky, D.I., and Vurzel, F.B. (1975) Theoretical and Applied

Plasma Chemistry, Nauka (Science), Moscow. 189.

Matsuuchi, H. (2013) System and method for generating high concentration NO2. US8425852, issued 2013.

190.

Asisov, R.I., Givotov, V.K., Rusanov, V.D., and Fridman, A. (1980) High Energy Chemistry (Khimia Vysokikh Energij). Sov. Phys., 14, 366.

191.

Belova, V.M., Eremin, E.N., and Maltsev, A.N. (1978) Heterogeneous catalytic oxidation of nitrogen in a glow discharge II 1:1 nitrogen-oxygen mixture. Russ. J. Phys. Chem., 52 (7), 968– 970.

192.

Sun, Q., Zhu, A., Yang, X., et al. (2003) Formation of NOx from N2 and O2 in catalyst-pellet filled dielectric barrier discharges at atmospheric pressure. Chem. Commun., 5 (12), 1418–9.

193.

O’Hare, L.R. (1984) Nitrogen fixation by plasma and catalyst. US 4451436, issued 1984.

194.

O’Hare, L.R. (1989) Nitrogen fixation by electric arc and catalyst. US4877589, issued 1989.

195.

Amouroux, J., Rapakoulias, D., and Cavadias, S. (1984) Method and device for preparation of nitric oxides. CH 645321 A5, issued 1984.

196.

Schaub, G., and Turek, T. (2011) Energy Flows, Material Cycles and Global Development: A

Process Engineering Approach to the Earth System. 197.

Sugiyama, K., Akazawa, K., Oshima, M., et al. (1986) Ammonia Synthesis by Means of Plasma over MgO Catalyst. Plasma Chem. Plasma Process., 6 (2), 179–193.

198.

Yin, K.S., and Venugopalan, M. (1983) Plasma chemical Synthesis. I. Effect of Electrode Material on the Synthesis of Ammonia. Plasma Chem. Plasma Process., 3 (3), 343–350.

199.

Uyama, H., and Matsumoto, O. (1989) Synthesis of ammonia in high-frequency discharges.

Plasma Chem. Plasma Process., 9 (1), 13–24. 200.

Uyama, H., and Matsumoto, O. (1989) Synthesis of Ammonia in High-Frequency Discharges. II. Synthesis of Ammonia in a Microwave Discharge Under Various Conditions. Chem. Plasma Process.

Plasma, 9 (3), 421–432.

201.

Tanaka, S., Uyama, H., Matsumoto, and O., and Matsumoto, O. (1994) Synergistic Effects of Catalysts and Plasmas on the Synthesis of Ammonia and Hydrazine. Chem. Plasma Process.

Plasma, 14 (4), 491–504. 202.

Nakajima, J., and Sekiguchi, H. (2008) Synthesis of ammonia using microwave discharge at atmospheric pressure. Thin Solid Films, 516 (13), 4446–4451.

203.

Uyama, H., Nakamura, T., Tanaka, S., and Matsumoto, O. (1993) Catalytic effect of iron wires on the syntheses of ammonia and hydrazine in a radio-frequency discharge. Plasma Chem. Plasma

Process., 13 (1), 117–131. 204.

Kiyooka, H., and Matsumoto, O. (1996) Reaction Scheme of Ammonia Synthesis in the ECR Plasmas. Plasma Chem. Plasma Process., 16 (4), 547–562.

205.

Bai, M., Zhang, Z., Bai, X., et al. (2003) Plasma synthesis of ammonia with a microgap dielectric barrier discharge at ambient pressure. IEEE Trans. Plasma Sci., 31 (6), 1285–1291.

206.

Bai, M., Zhang, Z., Bai, M., et al. (2008) Synthesis of Ammonia Using CH4/N2 Plasmas Based on Micro-Gap Discharge under Environmentally Friendly Condition. Plasma Chem. Plasma Process., 28 (4), 405–414.

207.

Mizushima, T., Matsumoto, K., Sugoh, J., et al. (2004) Tubular membrane-like catalyst for reactor with dielectric-barrier-discharge plasma and its performance in ammonia synthesis. Appl. Catal. A

Gen., 265 (1), 53–59. 208.

Patil, B.S., Peeters, F.J.J., Kaathoven, A.S.R. van, et al. (2017) Deciphering the Plasma-Catalyst Support Interaction for Plasma Assisted Ammonia Synthesis in a Packed DBD Reactor. Submitt. to

Ind. Eng. Chemstry Res. 209.

van Helden, J.H., Wagemans, W., Yagci, G., et al. (2007) Detailed study of the plasma-activated catalytic generation of ammonia in N[sub 2]-H[sub 2] plasmas. J. Appl. Phys., 101 (4), 43305.

210.

Mingdong, B., Xiyao, B., and Zhitao, Z. (2000) Synthesis of Ammonia in a Strong Electric Field Discharge at Ambient Pressure. Plasma Chem. Plasma Process., 20 (4), 511–520.

211.

Mizushima, T., Matsumoto, K., Ohkita, H., and Kakuta, N. (2006) Catalytic Effects of Metal-loaded Membrane-like Alumina Tubes on Ammonia Synthesis in Atmospheric Pressure Plasma by Dielectric Barrier Discharge. Plasma Chem. Plasma Process., 27 (1), 1–11.

FIGURES

Estimation of global nitrogen fixation quantities (Million tonn/year) Farming, 47, 10%

Haber-Bosch process

Haber-Bosch process, 136, 29%

Combustion Lightning

Ocean and water body, 140, 30%

Combustion, 26, 5%

Forest and non agricultural land, 111, 24%

Lightning, 11, 2%

Forest and non agricultural land Ocean and water body Farming

Figure 1. Estimation of quantities of fixed nitrogen in million metric tons per year in 2010 [6]. The farming, ocean, and forest segments all represent nitrogen fixation by nitrogenase in microorganisms present in those locales. reprinted from [9] with kind permission of Elsevier B.V.

Figure 2. Range of applications of chemically fixed nitrogen in the form of ammonia, reprinted from [9] with kind permission of Elsevier B.V.

Figure 3. Mo-Nitrogenase. Schematic representation of the MoFe protein and Fe protein components of nitrogenase (top). Only one half of the MoFe protein is shown with a symmetrical ab half not shown. The Fe protein contains one 4Fe-4S cluster and two ATP binding sites. Each ab half of the MoFe protein contains an 8Fe-7S cluster (called the P cluster) and a FeMo-cofactor (called FeMo-co or M cluster). Structures of the metal clusters are shown (below). Fe is shown in rust, S in yellow, C in gray, O in red, and Mo in magenta.

Figure 4. Schematic of the Fe protein cycle. One αβ unit of the MoFe protein is shown on top containing a P cluster (P) and FeMocofactor in the resting (M) or one electron reduced (Mr) state. The α2 dimer Fe protein is shown on the bottom with a 4Fe-4S cluster (box) in the reduced (R) or oxidized (ox) state. The rate constants for each step are shown.

Figure 5. Simplified Lowe and Thorneley Scheme. E represents the MoFe protein that has accumulated n electrons from the Fe protein cycle.

Figure 6. Structure of FeMo-co and the E4(4H) state. Shown is the structure of the E4(4H) state with one FeS face highlighted with a red box (top) and one Fe-S face with two bridging Fe-H-Fe (bottom). The exact location of binding of the bridging hydrides is not known.

Figure 7. Proposed reductive elimination (RE)-oxidative addition (OA) mechanism for reversible N2 binding and H2 release at the E4(4H) state of FeMo-co.

Figure 8. Reversible N2 and H2 binding to E4. The RE and OA step at the E4 state is shown (top). Proposed mechanism for the reversible RE/OA of N2 and H2 at the E4 state of FeMo-cofactor (bottom). The exact order of N2 binding and H2 loss is unknown.

Figure 9. Major milestones in chemical nitrogen fixation process development [56,63,64].

450

GJ/t of ammonia

400

Birkeland-Eyde Process

350 300 250 200

Cyanamide Process

Haber-Bosch Process

150 100

Steam Reforming and Optimization

50 0 1900 1920 1940 1960 1980 2000 2020

Year Figure 10. Comparison of energy consumption for three N-fixation processes [66].

Figure 11. The industrial scale model of Birkeland-Eyde nitrogen-fixation process; from the power station on the left of the figure to the final fertilizer product to the right. With kind permission from [57] Springer Science and Business Media.

Figure 12. Proposed mechanism for Fe-based Haber Bosch catalysis [76].

7

140

6

120

5

100

4

80

3

60

2 1 0

H-B Process N is Nutrient N is discovered Biological N-fixation

1750 1800 1850 1900 1950 2000

Year

40 20 0

NH3 Production (Million tons/year)

Population (Billion)

Figure 13. Energy-flow diagram of the Haber-Bosch process, initially producing H2 to feed into a NH3 production reactor [91].

Figure 14. Global population increase and the nitrogen fertilizer consumption trends [3].

Figure 15. Photolytic production of H2 from H2O and Generation of NxHy Products

Figure 16. Mo-based NH3 generation catalysts

Figure 17. Catalytic activity of homogeneous Fe-based NH3.

Figure 18. Mechanism of ammonia production from the monometallic catalysts. M=Mo, Fe, Co.

Figure 1920. Catalytic Silylation of N2 by a (PPP)Mo catalyst.