Nitrogen Fixation

BHASKAR S. PATIL,Micro Flow Chemistry and Process Technology, EindhovenUniversity of Technology, Eindhoven, The Netherlands

VOLKER HESSEL,Micro Flow Chemistry and Process Technology, EindhovenUniversity of Technology, Eindhoven, The Netherlands

LANCE C. SEEFELDT, Department of Chemistry and Biochemistry, Utah State University,Logan, UT, United States

DENNIS R. DEAN, Department of Biochemistry, Virginia Polytechnic Institute and StateUniversity, Blacksburg, VA, United States

BRIAN M. HOFFMAN, Department of Chemistry, Northwestern University, Evanston, IL,United States

BRIAN J. COOK, Center for Catalysis & Center for Heterocyclic Compounds,Department of Chemistry, University of Florida, Gainesville, Florida, United States

LESLIE J. MURRAY, Center for Catalysis & Center for Heterocyclic Compounds,Department of Chemistry, University of Florida, Gainesville, Florida, United States

1. Introduction . . . . . . . . . . . . . . . . . 12. Biological Nitrogen Fixation . . . . . . 22.1. Nitrogenases . . . . . . . . . . . . . . . . . 22.1.1. Mo-Nitrogenase . . . . . . . . . . . . . . . 32.1.2. Fe Protein Cycle . . . . . . . . . . . . . . . 32.1.3. MoFe Protein Cycle . . . . . . . . . . . . 43. Chemical Nitrogen Fixation . . . . . . 63.1. Industrial Processes for Nitrogen

Fixation . . . . . . . . . . . . . . . . . . . . 73.1.1. Plasma Assisted Nitrogen Fixation:

Birkeland–Eyde Arc Process. . . . . . . 73.1.2. Frank and Caro Cyanamide Process. . 9

3.1.3. Haber–Bosch Process (HBP): ACentury of Heterogeneous AmmoniaCatalysis . . . . . . . . . . . . . . . . . . . . 9

3.2. Lab-Scale Efforts for ChemicalNitrogen Fixation . . . . . . . . . . . . . 10

3.2.1. Electrocatalytic Nitrogen Fixation . . . 113.2.2. Photocatalytic Nitrogen Fixation . . . . 123.2.3. Homogeneous Catalytic Nitrogen

Reduction to Ammonia . . . . . . . . . . 123.2.4. Nonthermal Plasma (NTP) Assisted

Nitrogen Fixation . . . . . . . . . . . . . . 15References. . . . . . . . . . . . . . . . . . . 16

1. Introduction

Nitrogen (dinitrogen or N2), which makes up to∼78.08% of the Earth’s atmosphere, is an essen-tial element for sustaining all living organisms[1]. Nitrogen is found in nucleic acids, chloro-phyll, and amino acids, to name a few biologicalconstituents [2]. Even though dinitrogen isabundantly available, it is not directly accessibleto plants and animals. Dinitrogen can only beused in its “fixed” form, like ammonium NH4

� �

and nitrate NO3� �

. To become metabolicallyavailable, the NºN triple bond must be broken,and the resulting atomic nitrogen must be chem-ically bonded with other elements, such asoxygen and/or hydrogen through a process

called “nitrogen fixation” [3]. Atomic nitrogencan also be combined with carbon throughprocess known as “nitrogen assimilation” [3].Some prokaryotes are capable of directly fixingatmospheric dinitrogen and supplying it toplants in a process known as biological nitrogenfixation [4, 5], through which almost half of N2

is fixed on Earth. Biological fixation of dini-trogen takes places in the ocean and waterbodies, during farming, and in forest and non-agricultural land. The other important naturalsources for fixed nitrogen, which is nonbiolog-ical, are lightning that result from the electricdischarge between two clouds and combustionprocesses, where conditions are optimum forNOx formation [6]. The increasing food demand

2017 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim10.1002/14356007.a17_471.pub2

from the exploding global population necessi-tated intensified agricultural practices, whichmeant that biologically fixed nitrogen was nolonger sufficient and thus, chemical processes toartificially fix nitrogen were developed [7–9].Today almost all chemically fixed nitrogencomes from the Haber–Bosch process (dis-cussed in Section 3.1.3) [10]. The estimationof global nitrogen fixation quantities, asreported in 2010, are shown in Figure 1 [6].In this figure, the segments farming, ocean, andforest represent nitrogen fixation by nitrogenasein microorganisms present in those locales.

Besides using fixed nitrogen as a fertilizer inagriculture, chemically fixed nitrogen in the

form of ammonia is also used for large scaleapplications in chemical industry, e.g., pharma-ceuticals, explosives, and plastic manufacturing[9, 11] (See also → Ammonia, 2. ProductionProcesses). A complete picture of the range ofproducts derived from ammonia is presented inFigure 2.

The chemical process for nitrogen fixation isnotorious for high CO2 emission, energy con-sumption, and harsh operating conditions. Onthe other hand, biological nitrogen fixation takesplace at mild conditions, thus it gives hope fordevelopment of a new artificial nitrogen fixationprocess operating under mild operating condi-tions [9, 12]. This possibility has opened doorsfor different research areas in biological andchemical nitrogen fixation and have been thesubject of increasing efforts since 1960s.

Various approaches and key conceptsinvolved in biological and chemical nitrogenfixation processes are briefly discussed as wellas some commercially applied chemical pro-cesses for nitrogen fixation.

2. Biological Nitrogen Fixation

2.1. Nitrogenases

More than half of the N2 fixed on Earth isaccomplished by microorganisms through the

Figure 1. Estimation of quantities of fixed nitrogen in 106 t/ain 2010 [6]; the farming, ocean, and forest segments alldenote nitrogen fixation by nitrogenase in microorganismspresent in those locales, adapted from [9] with kindpermission of Elsevier B.V.

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

2 Nitrogen Fixation

action of the enzyme nitrogenase [10]. Nitroge-nases are found in two of the three domains oflife, i.e., in bacteria and archaea [13–16]. Nitro-genases are found in a wide-array of thesemicrobes, which are often referred to as diazo-trophs. Nitrogenases have not been found in anyeukaryotes. Diazatrophs are found in most eco-systems, including aquatic (e.g., oceans) andterrestrial [16]. Three different nitrogenaseshave been identified, with some microbes con-taining all three. The most commonly foundand best studied nitrogenase is called Mo-nitrogenase, reflecting the presence of theelement molybdenumMo as part of the complexmetal cluster that forms the site of N2 bindingand reduction [17]. The other two nitrogenasetypes are often referred to as “alternative” nitro-genases, because they are not as often found andnot as well studied [18]. These alternative nitro-genases are called V-nitrogenase and Fe-onlynitrogenase, with the names reflecting thereplacement of Mo by the metals vanadiumand iron, in the active site metal cluster, respec-tively. The alternative nitrogenases are codedfor by unique gene clusters, so are distinctenzymes. However, the overall architecture ofthe protein complexes and metal clusters appearto be very similar to the Mo-nitrogenase. Forthis reason, and especially because of the prev-alence of the Mo-nitrogenase, this enzyme istaken as the paradigm for nitrogenases and isthe focus of this presentation. Reviews on thealternative nitrogenases can be found elsewhere[18, 19].

2.1.1. Mo-Nitrogenase

The Mo-nitrogenase is composed of two proteincomplexes, referred to as MoFe protein (alsocalled dinitrogenase or component I) and Feprotein (also referred to as dinitrogenase reduc-tase or component II) [17]. The MoFe protein isan α2β2 heterotetramer, with each αβ dimerconstituting a minimal catalytic unit [20, 21].Each αβ dimer contains an 8Fe-7S cluster calledP cluster and an 7Fe-9S-Mo-C-homocitratecluster called FeMo-cofactor [22]. The FeMo-cofactor (also termed FeMo-co) is the site ofsubstrate binding and reduction [23]. The Pcluster is proposed to serve as an electronshuttle, delivering electrons to FeMo-co [24].The Fe protein component is an α2 homodimer,

having a single 4Fe-4S cluster that bridges thetwo subunits [25]. Each subunit of the Fe pro-tein contains an ATP binding site. During catal-ysis, the Fe protein transiently associates withthe MoFe protein, during which an electron istransferred from the Fe protein to the MoFeprotein and the two ATP molecules are hydro-lyzed to two ADP and two inorganic phosphate(Pi) [26]. The complete catalytic cycle of nitro-genase involves a number of steps in eachprotein component. The steps in each proteincomponent are intertwined; for convenience theevents associated with the Fe protein delivery ofelectrons are often called the Fe protein cycle,whereas the events associated with the MoFeprotein are called the MoFe protein cycle. Keysteps in each of these cycles are summarized inFigure 3.

2.1.2. Fe Protein Cycle

The Fe protein functions to deliver electrons tothe MoFe protein during the transient associa-tion of the two proteins [27]. The Fe proteincycle is initiated when the Fe protein, with areduced [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 dockedto the MoFe protein have shown that the Feprotein binds to the surface of the MoFe proteindirectly over a P cluster [28–30]. Kinetic studiesshow the association of the Fe protein with theMoFe protein to be fast relative to other keysteps [26]. Following association of the Fe

Figure 3. A) Schematic representation of the MoFe proteinand Fe protein components of nitrogenase; only one half ofthe MoFe protein is shown with a symmetrical αβ half notshown. The Fe protein contains one 4Fe-4S cluster and twoATP binding sites. Each αβ half of the MoFe proteincontains an 8Fe-7S cluster (called the P cluster) and aFeMo-cofactor (called FeMo-co or M cluster); B) Structuresof the metal clusters; Fe is shown in rust, S in yellow, C ingrey, O in red, and Mo in magenta

Nitrogen Fixation 3

protein with the MoFe protein, a sequence ofsteps happens rapidly (Fig. 4). A pre-steadystate study revealed that electron transfer (ET)from the Fe protein to the MoFe protein is thefirst step after protein association, with a pseudofirst order rate constant of 140 s�1 [31]. Thiselectron transfer event has been shown to beconformationally gated, with large scale proteinchanges in the structure of the complex preced-ing and controlling electron transfer [32]. Theinvolvement of the P cluster in the ET events hasbeen established [24], with available evidencesuggesting a deficit spending order of ET steps[32]. Following protein–protein association, theP cluster transfers one electron to the FeMo-coin a gated step, which is followed by fast ETfrom the Fe protein to the oxidized P cluster.The net result of the ET events is oxidation ofthe reduced Fe protein and the transfer of anelectron to FeMo-cofactor. This ET process inthe Fe protein cycle is followed by ATP hydrol-ysis with a first order rate constant of about 40s�1 [31, 33]. This step is then followed by Pirelease with a rate constant of about 20 s�1.Finally, the oxidized Fe protein, presumablywith two bound ADP, dissociates from theMoFe protein. Earlier studies using the non-physiological reductant dithionite as the elec-tron source for the reduction of Fe proteinsuggested that this dissociation step had a rateconstant of 6 s�1 and thus was the rate-limitingstep [26]. However, a study from 2016 usingreduced flavodoxin, one of the natural reduc-tants in the cell, revealed that the dissociationstep was fast with this reductant, indicating thatevents associated with the Pi release step are

rate-limiting for the Fe protein cycle [34]. Oncedissociated, the Fe protein is reduced (physio-logically by flavodoxin or ferredoxin) and theADP is replaced by ATP to recharge the Feprotein and complete the Fe protein cycle.

2.1.3. MoFe Protein Cycle

Electrons received by theMoFe protein from theFe protein are ultimately accumulated on FeMo-cofactor. A kinetic scheme representing theaccumulation of electrons into the MoFe proteinwas put forward by LOWE and THORNELEY [26]from a series of kinetic and spectroscopic stud-ies. In a modified and simplified Lowe andThorneley (LT) scheme, the E0 state representsthe resting state before any electrons are accu-mulated, with the number of electrons trans-ferred to MoFe protein indicated with an nsubscript (En) as shown in Figure 5. Since theelectrons are ultimately accumulated on FeMo-cofactor, the En state can be taken as the number

Figure 4. Schematic presentation of the Fe protein cycle. One αβ unit of the MoFe protein is shown on top containing a Pcluster (P) and FeMo-cofactor in the resting (M) or one electron reduced (Mr) state. The α2 dimer Fe protein is shown on thebottom 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 rep-resents the MoFe protein that has accumulated n electronsfrom the Fe protein cycle.

4 Nitrogen Fixation

of electrons accumulated in FeMo-cofactor orone of its bound, semireduced intermediates.Each electron accumulated on FeMo-cofactor islikely balanced by the accumulation of a proton,in proton coupled electron transfer. The accu-mulated protons also are indicated in the schemeof Figure 5. Several aspects of this kineticscheme are noteworthy. First, the E2(2H),E3(3H), and E4(4H) states can “relax” by for-mation of H2 back to lower E states. This reflectsthe long-known fact that nitrogenase can evolveH2 in the absence of any other substrate [35]. Itwas also established from early kinetic studiesthat N2 does not bind until at least three or fourelectrons/protons are accumulated on FeMo-cofactor (shown binding to the E4 state inFig. 5) [26]. The mechanistic reason for theneed to accumulate four electrons/protons onFeMo-cofactor before N2 can bind remained amystery for decades. Even more so, the incor-poration of a stoichiometric release of one H2

for each N2 bound, with a resulting stoichio-metric requirement of 8 e�/H+ to form twoNH3, remained a mystery, and indeed was noteven universally accepted [17]. Studies of themid-2000s have validated this stoichiometryand revealed the mechanistic reason for thesephenomenon [36–38].

A key breakthrough in understanding themechanism of N2 binding came from the trap-ping of a catalytically central intermediate usinga combination of substitution of amino acidsnear the active site and freeze quenching sam-ples during turnover [39–49]. Spectroscopic andkinetic examination of the trapped state usingFeMo-cofactor 57Fe, 95Mo, 1H, and 2H iso-topomers led to two important conclusionsabout this intermediate: (i) The state isE4(4H), which has accumulated 4[e�/H+] andis activated to bind N2 for reduction with H2

release (denoted the Janus intermediate); (ii) theE4(4H) state contains two bridging Fe–H–Fehydrides (Fig. 6) [36–38]. The observation ofthe two hydrides indicates that the metal corehad not changed formal oxidation state eventhough four electrons had been transferred andexplains how FeMo-cofactor can accumulatefour electrons at the constant potential of theFe protein: The electrons are “parked” as metalhydrides.

The presence of metal hydrides in the E4(4H)state allowed consideration of several different

models for how N2 would bind and why H2

would be evolved. Each model was compared toa series of earlier observations that providedconstraints on the mechanism of the nitrogenasereaction, ruling out all but one model [36–38].Only a reductive elimination (RE) model wasconsistent with these observations (Fig. 7A). Inthis model, the two hydrides combine to formH2, leaving behind a doubly reduced metalcluster [36–38]. N2 binding during this processis accompanied by the prompt addition of thetwo electrons and remaining two protons, yield-ing a cluster bound diazenido-level intermedi-ate. This first step in the reduction of N2,cleavage of the NºN triple bond and the

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

Figure 7. Reversible N2 and H2 binding to E4. A) Proposedreductive elimination (RE)-oxidative addition (OA) forreversible N2 binding and H2 release at the E4(4H) stateof FeMo-cofactor; the RE and OA step at the E4 state areshown. B) Proposed mechanism for the reversible RE/OA ofN2 and H2 at the E4 state of FeMo-cofactor (The exact orderof N2 binding and H2 loss is unknown).

Nitrogen Fixation 5

2 e�/H+ conversion to a cluster bound diaze-nido-intermediate, is by far the thermo-dynamically most difficult step of N2 fixationand is thermodynamically driven by the reduc-tion of two protons and hydrolysis of four ATP,which leads to H2 release [36]. Studies of thenative MoFe show that the Janus intermediate inthe modified and native MoFe are identical andthat the process in Figure 7A is indeed a kineti-cally reversible and essentially thermoneutralequilibrium, driving the cleavage of the NºNtriple bond, whereas direct reduction of N2 todiazene is extremely endergonic [47–49]. Sub-sequent addition of protons and electrons ulti-mately lead to the formation of two ammonia(NH3) molecules. There are two alternatives asto when the first NH3 is released, after deliveryof 5 e�/H+ to FeMo-cofactor, or after 7 e�/H+,with the preponderance of the evidence favoringthe latter [36, 50, 51].

If N2 binding and reduction truly involvesRE and is a readily reversible equilibrium, thenin the presence of added H2 the equilibrium canbe reversed, with oxidative addition (OA) of H2

to E4(2N2H) generating the bridging hydridesand releasing N2 to form the E4(4H) state. Sucha reaction would explain the observation thatdeuterium (D2) is converted to two HD whennitrogenase is turned over under D2 and N2 [17,52, 53]. In this case, the D2 undergoes OA toload two Fe–D–Fe bridging deuterides [36].These deuterides, not being exchangeablewith solvent, can be protonated by the sulfur-bound protons derived from solvent, yieldingtwo HD, corresponding to the relaxation steps ofFigure 3. This proposed explanation for the HDformation associated with the RE mechanismfor N2 activation was tested and confirmed bythe demonstration that when the known sub-strate acetylene (C2H2) was added along withN2 and D2, the acetylene intercepted the [Fe–D–Fe]-containing states, resulting in the reductionof acetylene to ethylenes with one or two D(C2DH3 and C2D2H2) [44]. In the absence of N2,deutero-acetylenes are not formed, because thebridging deuterides only form through RE/OAat the E4(4H) state.

The photolysis of transition metal dihydridecomplexes commonly results in the reductiveelimination of H2 [54], and it has beenobserved that cryogenic irradiation of nitroge-nase E4(4H) with visible light likewise results

in the photoinduced RE of a H2 [46–49]. Whenthe photolyzed sample was warmed to 217 K,the process was reversed, with OA of thereleased H2 to reform the E4(4H) state. Kineticanalysis of the rates of loss of the E4(4H) stateand the formation of the E4(2H)

∗ state haveuncovered the existence of an intermediatebetween these two state, which has beenassigned to a H2 bound state (Fig. 7) [49].The analysis further suggested that this H2

functions as an intermediate in the thermalRE of H2 that activates FeMo-co to breakthe NºN triple bond during catalysis. Whilethe order of H2 release and N2 binding has notbeen experimentally established, it is neces-sary that N2 bind before H2 is released. Loss ofH2 first essentially results in an E2(2H) state,which is not expected to bind N2. This suggeststhat N2 would at least associate with the H2

bound state (Fig. 7).With these studies, the central elements of

the nitrogenase mechanism have becomeclear. Similar studies are needed to fill outthe full reaction pathway for N2 reduction.This includes a deepened understanding ofhow electrons/protons are accumulated in theearly E states and how the FeMo-co bounddiazene is stepwise reduced to two ammoniamolecules.

Many challenges remain to fully understandhow nitrogenase catalyzes the reduction of N2 toammonia under mild conditions, but extensivestudies since the 1960s have disclosed manyaspects of this fascinating and complex molec-ular machine, while studies since 2007 revealthe heart of its catalytic mechanism.

3. Chemical Nitrogen Fixation

The NºN triple bond is one of the strongest,which needs 9.77 eV (941 kJ/mol) of energy todissociate and has an ionization potential of 15.6eV [55]. This indicates the extremely highenergy required for cleaving or oxidation ofthe dinitrogen molecule. Moreover, dinitrogencan only be reduced by highly electropositivemetals, such as lithium (with electronegativityof 0.98). Thus, breaking the NºN triple bond isoften the rate-limiting step in the nitrogen fixa-tion process and is the subject of considerableresearch [12].

6 Nitrogen Fixation

3.1. Industrial Processes for NitrogenFixation

Up to the beginning of the 19th century, thefixed nitrogen stockpiled in the form of organicor inorganic materials over millions of yearswas enough to sustain the demands of theEarth’s population [9]. An explosive growthof population, with increasing sizes of cities,demanded ways to provide more nitrogenthrough nitrogen fixation. Starting early in the20th century, nitrogen obtained from artificialprocesses overtook the nitrogen obtained fromnatural organic and inorganic sources [56]. Thechemical nitrogen fixation processes could onlybe developed on industrial scale, includingreactions for the production of nitric oxide(NO), ammonia (NH3), hydrogen cyanide(HCN) and nitric acid (HNO3); all these effortscould be combined into the following threemain approaches with the corresponding indus-trial process as an example:

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

∙ Use of compounds capable of fixing nitro-gen in their structure: e.g., cyanamide(Frank-Caro) process [56, 59, 60]

∙ Combining atmospheric nitrogen withhydrogen to form ammonia: e.g.,Haber–Bosch process [61] (→ Ammonia,2. Production Processes)

These processes are discussed below.Figure 8 outlines the most significant eventsin the industrialized nitrogen fixation processdevelopment [56, 62, 63].

Both, Birkeland–Eyde and Frank–Caro pro-cesses were very energy intensive [64] andeventually taken over by the Haber–Bosch pro-cess from 1930s [10, 60, 61]. Comparativelylower energy consumption and higher volumesof ammonia produced by Haber–Bosch processwere the main reasons. The chronological prog-ress is shown in Figure 9, which emphasizes thedramatic reduction in energy consumption fornitrogen fixation [65]. Significant developmentin technology since the 1950s has made itpossible to reduce the energy consumption ofthe Haber–Bosch nitrogen fixation process byalmost three times to reach the energy consump-tion of 28–36 GJ/t N-fixed (→ Ammonia, 2.Production Processes).

3.1.1. Plasma Assisted Nitrogen Fixation:Birkeland–Eyde Arc Process

Nitrogen fixation was first realized through anelectric arc process, known as Birkeland–Eydeor Norwegian Arc Process, which was devel-oped by CHRISTIAN BIRKELAND and SAMUEL EYDE

in 1903 [57]. In fact, the Birkeland–Eyde pro-cess is also the first plasma process ever realizedsuccessfully on the industrial scale. This processemploys the most fundamental means of chem-ically fixing dinitrogen by direct reaction with

Figure 8. Major milestones in chemical nitrogen fixation process development [56, 62, 63]

Nitrogen Fixation 7

oxygen under plasma conditions to producenitrogen oxides. The nitric oxide productionis favored by high temperature processingwith minimum thermodynamic energy require-ment of 6.4 GJ/t of nitrogen (→ NitricAcid, Nitrous Acid, and Nitrogen Oxides) andhas a positive standard Gibbs free energy of86.55 kJ/mol.

N2 � O2↔2 NO ΔH � 90 kJ=mol � 1 eV �1�

2 NO � O2↔2 NO2 �2�

2 NO2 � H2O↔HNO2 HNO3 �3�

The typical process flow scheme for theindustrial Birkeland–Eyde process is shown inFigure 10. The Birkeland and Eyde furnace wasbased on the phenomena of deflection of anelectric arc by a magnetic field. This helped to

spread the electric arc through the gas. First, airwas rapidly passed through a zone of exceed-ingly high temperature in an electric arc furnace,producing∼1–2 vol% nitric oxide (Eq. 1). In thesecond step, nitric oxide was oxidized to nitro-gen dioxide (Eq. 2). Finally, nitrogen dioxidewas then absorbed in water to produce dilutenitric acid (30%) in a train of absorption col-umns (Eq. 3), including alkaline absorptioncolumns for recovering unabsorbed NOx. Theexperiments were first carried out using a 2.24kW power supply in 1903. In the next step, acommercial plant working on 111.8 kW wasinstalled, whose successful operation led toinstallation of a 745.7 kW plant near Arendal,Norway. This successful demonstration resultedin a number of new plasma furnace installations,the biggest of which was a 238.6 MW plasmafurnace, fixing 3.8× 104 t of nitrogen in total peryear (in 1928) [56, 60].

For this process, the raw material (air) isavailable abundantly and almost for free. How-ever, less than 3% of the supplied energy wasutilized for the reaction, while the rest of thesupplied energy (97%) was wasted in establish-ing conditions suitable for the reaction to takeplace, e.g., to obtain 1 t of fixed nitrogen it wasrequired to process 175 t of air. Even thoughequipment had been built to rapidly cool theproduct gas to avoid decomposition of nitricoxide, it was believed that a large amount ofnitric oxide decomposition actually took place[9, 56].

Various efforts were attempted to improvethe performance of the Birkeland–Eyde process,but this thermal plasma assisted nitrogen fixa-tion process was found difficult to realize withsufficient product yield at affordable energy

Figure 9. Comparison of energy consumption of ammoniafor three N-fixation processes [65]

Figure 10. Industrial scale model of Birkeland–Eyde nitrogen-fixation process, reproduced with kind permission of SpringerScience and Business Media [57]a) Power station; b) Electric arc furnace; c) Cooling section; d–f) NO absorption and alkaline absorber section; g) Final fertilizerproduct

8 Nitrogen Fixation

input. Because of the poor energy efficiency andhigh mechanical maintenance requirement, itwas eventually abandoned as an industrial pro-cess [56, 66].

3.1.2. Frank and Caro Cyanamide Process(→ Cyanamides)

German scientists FRANK and CARO developedthe cyanamide process in 1895–1898 to fixatmospheric dinitrogen and commercialized itaround the same time as the Birkeland–Eydeprocess. The Frank–Caro process needs lime-stone and carbon as the main reactants, both ofthem solids, to produce nitrogen-containingcalcium cyanamide as a solid product. In thisprocess, first limestone is heated to produce limeand carbon dioxide (Eq. 4), which then reactswith carbon to give out calcium carbide (Eq. 5).In the final step, dinitrogen was fixed in the formof calcium cyanamide by its reaction with cal-cium carbide at ∼1000°C (Eq. 6). The finalproduct, calcium cyanamide, was applied asfertilizer, which, after reaction with water,hydrolyzes to calcium carbonate and ammonia(which is then used by plants) via reaction(Eq. 7) [59, 60].

CaCO3���!heat CaO � CO2 �4�

CaO3 � 3 C���!heat CaC2 � CO �5�

CaC2 � N2���������!∼1000°C CaCN2 � C �6�

CaCN2 � 3 H2O→CaCO3 � 2 NH3 �7�

The cyanamide process grew rapidly, reach-ing its peak in 1918, with 35 plants and totalrated capacity of fixing 3.5 × 105 t of nitrogenper year [56], mainly because of its 70–80%lower energy requirement than the Birkeland–Eyde process. However, this process had lowerfixed nitrogen content in its final product, cyan-amide. Moreover, the solid reactants and prod-ucts made process operation and handlingdifficult. Eventually, the cyanamide processalso phased out.

3.1.3. Haber–Bosch Process (HBP): A Cen-tury of Heterogeneous Ammonia Catalysis

The Birkeland–Eyde and the Frank–Caroprocess were eventually displaced by the

Haber–Bosch process (HBP), developed byFRITZ HABER in 1908 and commercialized byCARL BOSCH (and later ALWIN MITTASCH) in 1913[10, 60, 61]. Comparatively lower energy con-sumption and higher volumes of ammonia pro-duced by the Haber–Bosch process were themain reasons. After 1941, industrial (di)nitrogenfixation was exclusively carried out by theHaber–Bosch ammonia synthesis process (→Ammonia, 2. Production Processes). This nitro-gen fixation to ammonia (NH3) [3] processremains one of the most industrially importanttransformations for human civilization [67]. Ona global scale, ammonia is produced at a rate of1.4 × 108 t/a [68]. The catalytic production ofNH3 was first discovered to proceed by com-bining the respective elements as their diatomicgases at high temperature and pressure (300°C,100 MPa) over a Fe catalyst, which was fusedtogether with trace amounts of alumina, calciumoxide, and potassium oxide [11]. This mixture issuch an effective NH3 production catalyst that itis still used [69]. The Fe catalyst is composi-tionally similar to that of magnetite (Fe3O4), andfuture generations of Fe-based NH3 productioncatalysts have utilized this iron oxide instead ofelemental Fe. For 70 years after the discovery ofthe HBP, little progress was made in Fe-basedNH3 production catalysts until the discovery ofFe1�xO (wüstite) as a replacement of elementalFe in 1986, again calcined with the same addi-tives as in the original composition [70]. Thiscomposition (Fe1�xO, Al2O3, CaO, K2O) is themost active Fe-based catalyst used in the HBP[71]. Significant research interest [72] wasdevoted to the development of rare metal-basedcatalysts to replace Fe, and were first introducedindustrially at British Petroleum in the late1970s. These barium-promoted Ru catalystsare comprised of Ru and Ba supported onMgO [73]. A large majority of industriallyactive NH3 generation plants consist of eitherFe3O4/Fe1�xO based catalysts (one-bed reactor)or Ba-Ru/MgO (two-bed) reactors [71].Although the reaction conditions are not asharsh or energetically costly as the initial dis-covery, NH3 production continues to be anenergy-intensive process and a challenge forthe research community.

The mechanism of nitrogen fixation at thecatalyst surface in the HBP remains an activeresearch area. The mechanism is proposed to

Nitrogen Fixation 9

proceed through a related step-wise pathway asshown in Figure 11 [75]. Here, local Fe centersare generated at high pressure and temperatureon the surface of the Fe-based catalyst. Theselocal Fe centers facilitate the cleavage of theN–N triple bond (bond dissociation energy =945 kJ/mol) to yield N adatoms on the catalystsurface, likely localized as Fe3N units. Additionof one equivalent of H2 affords a bound Fe-NH2,with a subsequent equivalent of H2 resulting inNH3 release and catalyst regeneration [76]. TheRu-based catalysts are thought to proceedthrough a similar mechanism, with five Ruatoms in a B5-type site activating one moleculeof N2 [77–82].

Due to the high energetic requirements ofHBP, there has been rich active research indeveloping new heterogeneous nitrogen fixationsystems. Many of these systems are still basedon the time-tested thermochemical approachthat HBP employs. Ru has been reported numer-ous times with alternative additives than BaO/MgO, with K [83] and Cs [84] used as promot-ers on carbon surfaces. Additional efforts havebeen made to reduce the energetic cost ofproducing NH3 by recycling the steam usedin the reactor towards more NH3 production[85]. In 2015, chemical looping involvingreduction of Mn6N2.58 to Mn4N was used todrive the hydrogenation of Ca3N2, Sr2N andSrH2 and produce NH3 catalytically from H2Ounder ambient sunlight as the heat source [86].Finally, numerous computational studies havefocused on developing new NH3 generationcatalysts [87], highlighted by the design of anFeN3-embedded graphene catalyst which is pre-dicted to operate at room temperature [88].

The Haber–Bosch process sustains 40% ofthe global population and has doubled the num-ber of humans supported per hectare of arableland [66, 90], therefore it is considered as themost important discovery of the 20th century[61]. After the invention of this process, theglobal population started growing rapidly. Theincrease in global population and the nitrogen

fertilizer consumption follow a very similartrend as shown in Figure 12 [6].

3.2. Lab-Scale Efforts for ChemicalNitrogen Fixation

Several alternative approaches have been devel-oped for sustainable nitrogen fixation at mildoperating conditions, based on the biologicalone, such as electron driven electrocatalysis andphotocatalysis, homogeneous and enzyme catal-ysis [12]. It is highly unlikely that these alter-native processes would be more energy efficientthan the extraordinarily well optimized Haber–Bosch process. However, the emphasis shouldbe to minimize the substantial carbon footprintof nitrogen fixation by employing energy fromsustainable sources, such as wind, solar, orbiomass. Furthermore, it would be desirableto focus on the localized, at the point of use,fixation of nitrogen. This approach is expectedto solve the problems associated with the trans-portation and empower the famers working atremote places, such as in Africa.

Figure 11. Proposed mechanism for Fe-based Haber–Bosch catalysis, adapted from [74]

Figure 12. Global population increase and the nitrogenfertilizer consumption trends [3]a) Nitrogen is discovered; b) N is nutrient; c) Biologicalfixation; d) Haber–Bosch process

10 Nitrogen Fixation

3.2.1. Electrocatalytic Nitrogen Fixation

Although HBPmakes use of dihydrogen as boththe reducing agent and proton source for nitro-gen fixation to ammonia (see Fig. 13), an alter-native approach is to use an electrode to provideelectrons [91] coupled to an exogenous protonsource [92]. The overall thermodynamics ofdinitrogen reduction are more favorable if elec-trochemical reduction and protonation are con-certed or tightly-coupled (viz. proton-coupledelectron-transfer or PCET) [93]. However,adventitious production of H2 is often competi-tive with NH3 formation in these systems,decreasing the Faradaic efficiency (mol NH3/mol e� passed) [94]. To date, few systems havebeen shown to generate NH3 electrocatalyti-cally. LAMBROU reported a Ru cathode on acarbon felt in a three-electrode system thatoperated at elevated temperature and standardpressure; the highest Faradaic efficiency of0.92% was achieved at 0.06 V and 90 °C[95]. In 2013, TAO showed catalytic NH3 pro-duction at a Pt cathode and anode, in

combination with an acidic Nafion 211 mem-brane [96–98]. Using air as their dinitrogensource, a maximum production rate of 3.5 ×109 mol s�1 cm�2 was obtained and the faradaicefficiency of this system was 0.7%, whichimproved to 2% when air is replaced by N2.Other more elaborate electrochemical setupshave also been reported; these systems, how-ever, require elevated temperatures to produceNH3. Examples include a double Pd electrodecell separated by SrCe0.95Yb0.05O3 (78%)[99], a petrovskite La0.6Sr0.4Fe0.8 with aCe0.8Sm0.2O2-δ LSFCu-SDC composite elec-trode [100], and the use of molten salts as anelectroactive surface (23%) [101].

Other noteworthy ammonia synthesis andcatalysis results include: Dinitrogen hydro-genation on a polyaniline electrode [102],NH3 generation mediated by a complex offullerene C60 and γ-cyclodextrin [103, 104],catalytic NH3 synthesis from steam and nitro-gen at atmospheric pressure [105], catalyticproduction using of a dielectric-barrier dis-charge [106], the use of a stable electride in

Figure 13. Energy-flow diagram of the Haber–Bosch process, initially producing H2 to feed into a NH3 production reactor,adapted from [89]a) Catalyst, 700–1000°C, 3 × 105–2.5 × 105 Pa; b) Catalyst, 800–900°C; c) Catalyst, 500°C; d) Fe catalyst, 450°C, 3 × 107 Pa

Nitrogen Fixation 11

solution as the electron source [107], andthe electrosynthesis of NH3 using Chatt-likeW(Ph2PC2H4PPh2)2 complexes (see below) atvitreous carbon electrodes [108].

3.2.2. Photocatalytic Nitrogen Fixation

One area of increasingly active research inheterogeneous nitrogen fixation utilizes photo-catalytic methods [109], in which incident pho-tons (hν) provide the required energy fordinitrogen reduction to ammonia. Since thelate 1970s [110], numerous heterogeneous sys-tems were reported to produce ammonia fromdinitrogen and sacrificial reductants using activephotocatalysts, such as TiO2 doped with knownnitrogen fixation-active metals, such as Fe andRu [111–113]. Here, TiO2 splits H2O photo-catalytically [114] generating H2 and O2, theformer of which goes directly into NH3 andN2H4 production see figure 14. However, some(di)nitrogen oxidation is unavoidable and NxHy

products are also observed [115]:Alcohols are also commonly employed as

sacrificial reductants in addition to H2O [113].Indeed, photolysis in the presence of H2O2

was found to lead to NO production, not NH3.Impressively, many of these systems showsignificant NH3 generation under ambientsunlight, highlighting the utility of this meth-odology [111]. Other photocatalytic systemsemploy semiconductors (i.e., ZnO, SrTiO3,CdS, and GaP) in lieu of TiO2 [116]. CHEN

et al. reported photocatalytic ammonia pro-duction using Bi5O7I nanosheets [117]. Othernotable results include using solvated elec-trons and water to reduce nitrogen to ammo-nia on a photo-illuminated diamond surface[118], as well as photocatalytic production of

NH3 by Fe-oxide adsorbed to cross-linkedgraphene via photo-prompted hot electrons[119]. Despite significant progress, however,the rate of ammonia produced and the scal-ability from reported photocatalytic methodsfail to compare favorably with that fromHaber–Bosch methods.

3.2.3. Homogeneous Catalytic NitrogenReduction to Ammonia

Ammonia production using homogeneous cata-lysts offers numerous advantages to that ofheterogeneous systems. Chief among these ben-efits are uniform reaction conditions, favorablekinetics (and thus high turnover frequency), aswell the ability to study by using spectroscopicmethods [120]. The latter in principle allows foran iterative approach to improving catalystdesign. Inspired by the iron-molybdenumcofactor (FeMo-co) from the molybdenum-dependent nitrogenases [36, 121–123], twomajor homogeneous catalytic systems havebeen developed thus far, i.e., those based onMo and Fe [124, 125]. Many low-valent transi-tion metal complexes are known to bind andactivate N2 and subsequently liberate NH3 uponprotonation; however, the vast majority of thesesystems only offer stoichiometric or sub-stoi-chiometric conversion [126, 127]. The discus-sion here focuses on Group 6 and 8 transitionmetal complexes that are catalytic for dinitrogento ammonia conversion.

Catalytic Homogeneous Systems with Group 6Transition Metals. Major advancementstowards homogeneous ammonia productionwere made in the 1960s with the synthesis ofGroup 6 dinitrogen complexes featuring biden-tate phosphines ligands pioneered by JOSEPHCHATT, among others, who showed synthesisof ammonia from nitrogen, albeit not catalyti-cally [128]. Reduction of nitrogen to ammoniawas first achieved in a catalytic fashion in theseminal report from YANDULOV and SCHROCK in2003, with the development of a monometallicMo complex featuring a trisamidate ligand withbulky hexaisopropylterphenyl (HIPT) groups(1) [129] (Fig. 15).

The conversion to ammonia was accom-plished catalytically by the controlled stepwise

Figure 14. Photolytic water splitting by TiO2 and its use innitrogen fixation

12 Nitrogen Fixation

addition of protons and electrons rather thanmolecular hydrogen, although H2 is produced asa by product. The use of protons and electrons asopposed to molecular hydrogen was unique andset the standard for future dinitrogen reductioncatalytic systems. Subsequent structural andcomputational studies support a monometallicmechanism involving distal protonation of aterminal N2 ligand, followed by N–N bondscission to release one equivalent of NH3 anda Mo(VI) nitrido species [130–132]; the pro-posed mechanism is as follows: Figure 16.

SCHROCK’s success using Mo was followedby other reports, most notably those publishedby NISHIBAYASHI et al. in 2011 [133]. Thissystem utilized a low-valent Mo(0) center sup-ported by a PNP pincer ligand, in contrast to thehigher valent Mo intermediates observed for the

Schrock system. The Nishibiyashi system gen-erates more equivalents of NH3/Mo before cat-alyst death; however, the mechanism remainsunclear as only the structure of the resting stateafter initial reduction of the (PNP)MoCl3 start-ing material (2) is known [134]. The combina-tion of protons and electrons rather thanmolecular hydrogen is used here as in theSchrock system with the source of acid andelectrons similar to previous reports. Of note,the Nishibayashi system utilizes a milder reduc-tant (Cp2Co, E = �1.33 V vs. Fc/Fc+) [135]than the Schrock system (Na/Hg, E = –2.36 Vvs. Fc/Fc+). A subsequent report using a cat-ionic MoVºN supported by a PPP version ofthis ligand shows a maximum turnover number(TON) of 63 eq. NH3/Mo [136].

Catalytic Homogeneous Systems with Group 8Transition Metals. Nearly 100 years after thedevelopment of the Haber–Bosch process, cat-alytic ammonia production from homogeneousFe systems was finally achieved by J. PETERSet al. in 2013 featuring low-valent Fe centersupported by a trisphosphine donor ligandwith an apical heteroatom, X (X = B, Si, C, N)[137, 138] (Fig. 17).

The structural and vibrational data on theisolated formally Fe(0) and Fe(-I) terminal N2

complexes evidence significant activation of theN2 triple bond. Catalytic NH3 production isachieved for these systems at �78°C usingstrong reductants and acids, KC8 and[H(Et2O)2]BArF4, respectively. Expectedly,dihydrogen is an adventitious by product ofthis reaction; however, the relative rate of N2

reduction is competitive with H2 formation.Subsequent studies support a mechanism thatproceeds through a primarily monometallic dis-tal pathway with protonation occurring at the

Figure 15. Schrock–Yandulov Mo catalyst for nitrogenfixation to ammonia [127–130].

Figure 16. (PNP)Mo system developed by NISHIBAYASHI

et. al. [131, 132].

Figure 17. Peters XP3M nitrogen reduction system[135, 136]

Nitrogen Fixation 13

β-N of bound N2 where M = Mo, Fe, Co[51, 139, 140]:

NISHIBAYASHI et al. have also developed acatalytic NH3 system featuring Fe and Co fea-turing an anionic PNP backbone [141, 142](Fig. 18).

Catalysis is achieved using similar condi-tions to both PETERS and the previous Mo systemabove. Another report shows that a previously-studied system, (dppe)2Fe

0(N2) exclusively pro-duces N2H4 from N2 catalytically, and not NH3

[143–145].Certain homogeneous systems have also

been shown to catalytically convert N2 intoN(SiMe3)3. Since the SiMe3 group is, essen-tially, “a bulky proton”, the relevance to NH3

is paramount, as are the mechanistic implica-tions related to the design of future NH3 cata-lysts. Some examples include a bimetallic Cosystem which produces N(SiMe3) catalyticallyfrom N2 and Me3SiCl and KC8 with a TON of200 [146]. Included in this report is a mecha-nistic study with relevance to the distal proto-nation/reduction pathways observed for thepreviously mentioned Mo and Fe systems.Indeed, a related system to the (PNP)Mo sys-tem mentioned above has also been shown togenerate N(SiMe3)3 as well as other silylatedamines. Recently, a disilane is used in additionto Me3SiCl to generate tetramethylazadisilacy-clopentane [147, 148] (see Fig. 19). This resultis noteworthy since R3Si-H represents a devi-ation from the previously applied method ofprotonation followed by reduction, instead

resulting from formally oxidative addition ofthe Si–H bond. Although the generation of theactive catalyst, (PNP)Mo(ºN), proceeds viainitial reduction of (PNP)MoCl3 (and subse-quent N2 cleavage), no additional reducingequivalents are consumed in the reaction(Fig. 19).

This represents an important advancementtowards to catalytic homogeneous fixation ofdinitrogen, not only to catalytic ammoniaproduction.

The culmination of these studies shows thecurrent TON/turnover frequency (TOF) valuesfor homogeneous Fe nitrogen reduction cata-lysts to be < 15 eq. NH3/mol Fe, far inferior tothat achieved via current industrial Haber–Bosch methods. The silver-lining for designand implementation of homogeneous ammoniaproduction catalysts is, with every generation ofcatalyst produced, TON increases. The currentresearch climate for NH3 production catalysts isstrong, so there remains a great deal of optimismfor the development of a NH3 catalyst that caneventually usurp the Haber–Bosch method forindustrial production.

Figure 18. Fe/Co PNP pyrrolide system developed byNISHIBAYASHI, [139, 140]

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

14 Nitrogen Fixation

3.2.4. Nonthermal Plasma (NTP) AssistedNitrogen Fixation

Renewable energy driven nonthermal plasma(NTP) is considered to be a very attractivealternative to develop a small scale and local-ized nitrogen fixation process [9, 149–152].Moreover, only NTP can effectively activatethe nitrogen and oxygen molecules to yieldnitric oxide with energy consumption lowerthan that of the Haber–Bosch process [151,153]. Since a dramatic decrease in the cost ratioof electricity to natural gas has been witnessed,it is encouraging to revisit the NTP assistednitrogen fixation processes. Thus, NTP alsogives an opportunity to use sustainable energyproduced from solar, wind, or biomass [151].NTP can easily be combined with heteroge-neous catalysts, often yielding a synergeticeffect. These plasma assisted processes aremore attractive on a smaller scale, thereforefocus has been on the containerized or modularplant [9, 149, 152, 154–156]. Besides, plasmareactor process offers advantages, such as sim-ple one step processes, can be operated andstopped instantaneously, provides high energydensity for very fast reactions resulting insmaller units, and is generally nonpolluting[157]. An extensive analysis of the literaturereported for NTP assisted nitrogen oxideand ammonia synthesis is reported in reviews[9, 152, 158] and book chapters [159, 160].

NTP Assisted Nitric Oxide Synthesis. Themotivation to revisit NTP assisted nitric oxidestems from the fact that the minimum thermo-dynamic energy required for nitric oxide forma-tion is 3.5 times lower than that of ammonia[153]. Moreover, nitric oxide can be producedfrom cheap and abundant raw material and doesnot need hydrogen. NTP assisted atmosphericnitrogen fixation into nitric oxide has beenstudied and reported for lab scale processesusing air plasma [161–168], from N2–O2 mix-ture [169–173], and in argon, argon–nitrogenplasma [166, 172, 174, 175]. The main NTPdischarges that were investigated are the radiofrequency discharges [176–179], DC discharges[180–183], lasers [184, 185], microwave dis-charges [186, 187], microwave with electroncyclone resonance discharges [188], gliding arcdischarges [165–168], glow discharges [189],

dielectric discharges [173, 190], inductivelycoupled HF discharges [169, 171], and pulsedarc discharges [163, 164]. The use of a catalystin the plasma reactor for the synthesis of nitricoxide has not been investigated widely due toinherent difficulty with nitrogen oxidationreaction [169, 172, 189, 191–193].

NTP Assisted Ammonia Synthesis. The NTPassisted ammonia synthesis is not as attractiveas nitric oxide synthesis, because it needs tocompete directly with the catalytic route ofHaber–Bosch process, which is far superior interms of energy consumption and the produc-tivity. Moreover, NTP assisted ammonia syn-thesis relies on energy expensive hydrogen,besides readily available nitrogen, which makesplasma assisted ammonia synthesis less attract-ive unless hydrogen is produced using renew-able energy. For ammonia formation, theminimum thermodynamic energy required is22.6 GJ/t of nitrogen, due to the energy expen-sive hydrogen production process [194].

Despite apparent high energy demand ofammonia synthesis process, nonequilibriumplasmas that operate at ambient temperatureare widely investigated. Synthesis of ammoniahas been reported for glow discharge plasmas[195, 196], microwave plasma [197–200], radiofrequency plasma [197, 201], electron cycloneresonance [202], dielectric barrier dischargeplasma [203–206] and expanding plasma[207]. These NTP’s are often combined withheterogeneous catalysts. Magnesium and cal-cium oxides showed a catalytic effect in theammonia synthesis when the reaction is carriedout in the presence of H2–N2 plasma, althoughthey are catalytically inactive in the thermalammonia synthesis [195]. In 1983, YIN andVENUGOPALAN found the order of catalytic activ-ity as Pt > SS > Ag > Fe > Cu > Al > Zn inglow discharge plasma. SHIGEYUKI et al. [199]reported that the iron wire gives higher ammo-nia concentration than the molybdenum wires inRF discharge and MW discharge. Dielectricbarrier discharge plasma reactor is widelyreported for screening of catalysts for ammoniasynthesis. BAI et al. [208] smeared MgO on theelectrode surface in DBD reactor and realized itsimproved performance. MIZUSHIMA et al. [209]employed catalytic membrane integrated indielectric barrier discharge reactor, which

Nitrogen Fixation 15

gave catalytic activity in following orderRu > Ni > Pt > Fe > only alumina membrane.A localized production of ammonia assisted byplasma might lead to nonconventional applica-tions, such as in the NOx abatement and asenergy storage or fuel [9, 206].

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