The past, present and future of nitrogenous compounds in the atmosphere, and their interactions with plants

Abstract

Ammonia was necessary for the origin of life. However, NH₃ would not have been a significant component of the neutral or mildly reducing (N₂, CO₂, H₂O) atmosphere which characterized the Hadean earth (>3·8 Gyr ago), especially in view of the u.v. lability of NH₃, the greater u.v. output of the young sun than pertains today, and the absence of an atmospheric u.v. screen. Heterogeneous phase reactions, following atmospheric chemistry, have been proposed as a prebiotic NH₃ source. Lightning, or bolides (meteorites and comets), generated NO_x^., and Fe²⁺ in the sea could have reduced NO₂⁻ resulting from the NO_x^. to NH₄⁺; this disequilibrium NH₄⁺ level could have supported the production of the nitrogenous organic building blocks of life. NO_x^. and NH_y thus could both have had important roles in the origin and evolution of life. Burgeoning biota could soon have depleted abiotically generated NH₄⁺, and biological N₂ fixation could have evolved in its present Fe-demanding, O₂-sensitive forms in the Archaean O₂-free, Fe²⁺-rich environment. Organic matter could have driven biological denitrification reactions based on NO₂⁻ and NO₃⁻ generated abiologically using some redox components which evolved in earlier chemolithotrophs and photolithotrophs, regenerating atmospheric NO_x^. and producing N₂O. Any atmospheric NH₃ leaking from oceanic biology would have been subject to u.v. breakdown and rain-out. Although O₂-evolving photosynthesis probably began in the Archean some 3·5 Gyr ago, any O₂ accumulation was local until 2·0 Gyr ago (Proterozoic) due to consumption by oxidation of Fe²⁺ and S²⁻. However, localized O₂ accumulation before 2·0 Gyr ago could account for the observed early evolution of cytochrome oxidase and the possibility of O₂-consuming chemolithotrophic and chemoorganotrophic nitrification, with further possibilities of NO_x^. production. Oxygen accumulation globally from 2·0 Gyr onwards coincided approximately with the evolution of eukaryotes, which contributed phagotrophy to the reactions of the N cycle as well as the nutrification-like aerobic production of NO^. by nitric oxide synthetase, while lightning and bolides could now generate NO^. from N₂ and O₂.

Evidence for terrestrial ecosystems is found from 1·0 Gyr onwards; NO_x^. and NH₃ generated by terrestrial biota stands a greater chance of escaping to the atmosphere than do these compounds generated in the sea where recycling within the water body is likely. As CO₂ levels fell and O₂ levels rose, NH₃ cycling in the photorespiratory carbon oxidation cycle might have been evident as early as 1 Gyr ago, although this does not seem to be a major contributor to atmospheric NH₃ today. Embryophyte evolution on land 450 Myr ago, together with symbionts and biophages, increased primary productivity and N cycling on land, with greater quantitative possibilities for NO_x^. and NH₃ escape to the atmosphere. The evolution of lignin (and related phenylpropanoids) at least 400 Myr ago, with associated NH₃ recycling in vascular land plant, does not seem (on present evidence) to increase NH₃ loss to the atmosphere significantly. Biomass burning occurred at least 350 Myr ago with lightning as the likely ignition source; such burning yielded NO^., NH₃, N₂O and N₂ from organic N. As in earlier times, the existence of terrestrial embryophyte vegetation has been punctuated by major bolide impacts, with the Cretaceous-Tertiary boundary impact generating perhaps 10⁴ as much NO^. as a year's thunderstorms do today, although the toxicity of NO_x^.per se to vegetation might not have been the major effect of the NO_x^. on biota. Terrestrial plants suffered fewer extinctions at this time than did many other major taxa. Despite such very significant generators of atmospheric combined N as major bolide impacts, the mean levels of NH_y, NO_x^. and N₂O (and O₃) in the atmosphere during the 450 Myr existence of embryophyte vegetation was lower than the current, globally averaged, anthropogenically influenced values. Current globally averaged levels of atmospheric combined N are thus not without precedent in the history of life, globally for NO_x^., and locally for NH_y, so vegetation has had evolutionary experience of high atmospheric combined N. However, this should not make us complacent about the impact of current wide-spread and continuing anthropogenic inputs of combined N, in view of the rate and extent of the inputs, and their combination with other aspects of local anthropogenic influence (e.g. SO₂ from burning of high-S coal), stratospheric O₃ depletion, and global environmental change (increasing CO₂, temperature and sea-level).