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The appearance of NO on Earth and relationships with geological time. The Figure shows as a horizontal bar the division of time into the accepted eons (Hadean through to Phanerozoic). The units are in millions of years, and the scale ranges from 4.5 bya (4.5 × 109 years) to the present. Blue vertical arrows show accepted, but approximate, timings of the appearance or prevalence of the most significant biological events. Haemoglobins are considered to have emerged alongside the appearance of single-celled life, with an initial role in NO detoxification that later evolved and diversified (see text). At the top, NO is shown as being formed under the influence of lightning and coronal discharges in the Hadean atmosphere, subsequently generating various NOx, which served as early electron acceptors. NO reductase probably appeared before the related terminal oxidases, which appeared after the Great Oxidation Event. All timings are approximate and solely illustrative.
Other gasotransmitters that we now consider central to signalling in biology, i.e., primarily carbon monoxide (CO) and hydrogen sulfide (H2S), were also surely present in the prebiotic atmosphere; thus, life evolved with these gases . Nitrogen is cycled in our contemporary atmosphere by intimately interlinked biotic processes (see Section 3.1). However, before any organisms emerged, all nitrogen cycling must have been abiological; indeed, this cycling may have set the stage for the origin of life.
To understand how nitrogen cycling might proceed on terrestrial planets with comparable geodynamic activity to Earth, but on which life did not arise, Laneuville and coworkers  constructed a kinetic model of nitrogen cycling in its various major chemical forms (e.g., N2, reduced (NHx) and oxidized (NOx) species) between major planetary reservoirs (the atmosphere, oceans, crust and mantle) and included inputs from space. The model predicts a significant increase in oceanic nitrogen content over time, mostly as NHx, while atmospheric N2 content was lower than today. These distributions may have contributed to nitrogen assimilation and cycling over geological time scales.
With the Great Oxidation Event [19,20], which produced a rapid rise in the partial pressure of atmospheric O2 between 2.45 and 2.22 bya, cells began to utilize gases in a variety of physiological functions for signalling purposes . The presence of O2 would have enabled reactions with NO, as described in Section 1. Atmospheric O2 concentrations reached modern levels in the Devonian period as a result of photosynthesis , and with the consequent change in the oxidation state of the atmosphere, H2S was eliminated as a primary electron donor, and NO and CO became less advantageous as electron acceptors .
At some point in evolution, NO became an ancestral regulator of diverse metabolic processes. In particular, S-nitrosylation of protein cysteine residues emerged as a preeminent effector of NO bioactivity , but the evolutionary pressures that drove this are unknown, as is the timing of the appearance of cellular NO synthases (NOSs).
NO is generated from L-arginine that is produced from L-citrulline via the action of two of the five urea cycle enzymes. Briefly, argininosuccinate synthetase catalyses the rate-limiting step, converting L-citrulline to argininosuccinate, which is then converted to L-arginine by argininosuccinate lyase. The L-arginine so formed is then converted to NO and L-citrulline by the action of eNOS to complete the cycle .
Globins catalyse important reactions with nitrogen oxide species, such as NO dioxygenation and nitrite reduction. The formation of NO from nitrite is a reaction catalysed by globins that has received increasing attention due to its potential as a hypoxic NO signalling mechanism. NO dioxygenation is by far the most common reaction of NO with the haem group of globins in nature, and sometimes constitutes the main function of the protein, as in the case of flavohaemoglobins .
Among microorganisms, NOS enzymes have been found in many bacterial strains, including Nocardia , Lactobacillus fermentum , Staphylococcus aureus , Bacillus subtilis [54,55,56], B. cereus , B. anthracis , Deinococcus radiodurans , Sorangium cellulosum , Streptomyces turgidiscabies  and Geobacillus stearothermophilus , and in the haloalkaliphilic archaeon Natronomonas pharaonis  and the cyanobacterium Synechococcus PCC 7335 .
As in the NOS of higher organisms, bacterial NOS (bNOS) enzymes catalyse the oxidation of arginine to citrulline and NO in the presence of BH4 or tetrahydrofolate (H4F)  as cofactors. The oxygenase domain of bNOS shares 45% amino acid sequence identity with the oxygenase domain of mNOS . However, bNOS is smaller than its mammalian counterparts, lacking the N-terminal domain, the CaM-binding site and the reductase domain, the last being essential for electron transfer during NO biosynthesis. However, bNOS is able to generate NO in vivo using available cellular reductases . One exception is the bNOS from the Gram-negative S. cellulosum, which contains both a reductase and an oxygenase domain in the same polypeptide chain, with a 2Fe-2S ferredoxin subdomain involved in electron transfer from NADPH to haem .
bNOS enzymes seem to have different functions from those of mNOSs, including cytoprotection against oxidative stress , nitration of different metabolites , recovery from exposure to UV light  and modulation of aerobic respiratory metabolism . bNOS may also be considered as a therapeutic target, and bNOS inhibitors may be used to potentiate the activity of some traditional antibiotics , although the interplay between NO and antibiotic efficacy is complex, and examples of both inhibition and potentiation of antibiotic lethality exist (see Section 7 below).
Core structures of O2-binding cytochrome aa3 and NO-binding cNOR complex. The protein backbones for the core catalytic subunits for cytochrome aa3 from P. denitrificans (pdbID = 3HB3, ) and the cNOR NO reductase from P. aeruginosa (pdbID = 3O0R, ) were superposed (RMSD = 2.88 Å). The central haem cofactors and the catalytic copper (Cu) and iron (Fe) centres are shown along with the sidechains that coordinate these metals. Peripheral subunits, cofactors and solutes have been omitted for clarity.
Globins such as haemoglobin and myoglobin are also well-known to ligate NO via the haem iron O2-binding site and can both scavenge NO by oxidizing it to nitrate and generate NO in vivo via the reduction of nitrite ions by the ferrous haem cofactor , in addition to their primary roles as O2 carriers. However, perhaps more relevant in terms of NO binding are the specialist NO-detoxifying globins of microorganisms , with Hmp representing the archetypal example . The b-type haem cofactor of Hmp upon first inspection is a five-coordinate species similar to myoglobin, although a hydrogen-bonding network in the proximal pocket and charged residues in the distal cleft [77,78] confer properties more suitable to NO detoxification and O2 chemistry instead of O2 transport.
There is plenty of evidence to support the emergence of NOR complexes before oxygenic photosynthesis, so it is of interest to consider the availability of NO in an O2-depleted early atmosphere for use as a respiratory electron acceptor (as is the case for contemporary NO reductases). Prior to the emergence of oxygenic photosynthesis, it is thought that the oceans and atmosphere of Earth were reducing, suggesting that multivalent metals would exist mainly in their lower redox states, making them poor candidates as dissimilative electron acceptors. Hence, the availability of alternative electron acceptors is likely to have been less diverse than today, making NO a more attractive electron acceptor in the absence of more modern competition (e.g., O2, ferric iron) [99,100]. These primordial reducing conditions may also have presented a hurdle for the incorporation of copper ions (but not ferrous iron) into NO-binding sites due to the propensity of reduced cuprous Cu+ ions to disproportionate, although it has been suggested that coordination of Cu+ by appropriate ligands (e.g., thiolates) can stabilize this ionic state . Furthermore, the presence of NO-binding copper centres in obligate anaerobes (e.g., HCOs) demonstrates that copper is available for incorporation in anoxic environments. Hence, these observations support the idea that, prior to the Great Oxidation Event, NO was present alongside the suitable metallic precursors to generate simple NO-binding centres. It has been hypothesized that, following the increase in atmospheric O2, copper O2 proteins (COPs) with simple copper centres (e.g., the phenoloxidase tyrosinase) evolved to remove atmospheric O2 [102,103], and it is intriguing, yet perhaps unsurprising, that these protein family members can also bind NO . 2b1af7f3a8