Donald E. Canfield

The Evolution and Future of Earth's Nitrogen Cycle

Nitrogens Past and Future Microorganisms have been controlling Earths nitrogen cycle since life originated. With life evolving around it, nitrogen became both an essential nutrient and a major regulator of climate. Canfield et al. (p. 192) review the major changes in the nitrogen cycle throughout Earths history. Most of the time, perturbations typically coincided with the evolution of new metabolic pathways in various Bacteria or Archaea. The last century, however, has seen humans push the biological nitrogen cycle into a new stage altogether. The addition of large quantities of fixed nitrogen to crops in the form of fertilizer chokes out aquatic life that relies on runoff and adds significant amounts of N2O—a potent greenhouse gas—to the atmosphere. Although microorganisms may one day restore balance to the nitrogen cycle that they helped shape for billions of years, humans must modify their behavior or risk causing irreversible changes to life on Earth. Atmospheric reactions and slow geological processes controlled Earth’s earliest nitrogen cycle, and by ~2.7 billion years ago, a linked suite of microbial processes evolved to form the modern nitrogen cycle with robust natural feedbacks and controls. Over the past century, however, the development of new agricultural practices to satisfy a growing global demand for food has drastically disrupted the nitrogen cycle. This has led to extensive eutrophication of fresh waters and coastal zones as well as increased inventories of the potent greenhouse gas nitrous oxide (N2O). Microbial processes will ultimately restore balance to the nitrogen cycle, but the damage done by humans to the nitrogen economy of the planet will persist for decades, possibly centuries, if active intervention and careful management strategies are not initiated.

A new model for Proterozoic ocean chemistry

There was a significant oxidation of the Earths surface around 2 billion years ago (2 Gyr). Direct evidence for this oxidation comes, mostly, from geological records of the redox-sensitive elements Fe and U reflecting the conditions prevailing during weathering. The oxidation event was probably driven by an increased input of oxygen to the atmosphere arising from an increased sedimentary burial of organic matter between 2.3 and 2.0 Gyr. This episode was postdated by the final large precipitation of banded iron formations around 1.8 Gyr. It is generally believed that banded iron formations precipitated from an ocean whose bottom waters contained significant concentrations of dissolved ferrous iron, and that this sedimentation process terminated when aerobic bottom waters developed, oxidizing the iron and thus removing it from solution. In contrast, I argue here that anoxic bottom waters probably persisted until well after the deposition of banded iron formations ceased; I also propose that sulphide, rather than oxygen, was responsible for removing iron from deep ocean water. The sulphur-isotope record supports this hypothesis as it indicates increasing concentrations of oceanic sulphate, starting around 2.3 Gyr, leading to increasing rates of sulphide production by sulphate reduction. The increase in sulphide production became sufficient, around 1.8 Gyr, to precipitate the total flux of iron into the oceans. I suggest that aerobic deep-ocean waters did not develop until the Neoproterozoic era (1.0 to ∼0.54 Gyr), in association with a second large oxidation of the Earths surface. This new model is consistent with the emerging view of Precambrian sulphur geochemistry and the chemical events leading to the evolution of animals, and it is fully testable by detailed geochemical analyses of preserved deep-water marine sediments.

Reactive iron in marine sediments

A combined field/laboratory study has been undertaken to explore the mineralogy, concentrations and reactivity (towards sulfide) of iron in marine sediments. Also considered is the importance of bacterial Fe liberation in regulating pore-water chemistry. Two contrasting marine environments are included; one is the relatively Fe-poor FOAM site and the other is the Fe-rich sediments of the subaqueous Mississippi Delta. Results show that oxide minerals are the most important Fe phases in early diagenetic pyrite formation. However, viewed separately, lepidocrocite and ferrihydrite are more reactive towards sulfide than goethite and hematite. When Fe oxides are present in relatively high concentrations, dissolved sulfide is nearly absent from sediment pore waters (with concomitant high concentrations of dissolved Fe), even in the presence of active sulfide production by sulfate reduction. A combination of experimental results and diagenetic modelling shows that in some sediments pore water Fe finds it origin in the bacterial reduction of iron oxides. This seems the case even though greater amounts of Fe are reduced by reaction of sulfide with iron oxides. It appears that distinct microenvironments may exist in marine sediments, where, in one microenvironment, sulfide reacts with Fe oxides locally precipitating Fe sulfide minerals. In another, Fe reduced and solubilized by microorganisms migrates freely into solution.

The anaerobic degradation of organic matter in Danish coastal sediments: Iron reduction, manganese reduction, and sulfate reduction

We used a combination of porewater and solid phase analysis, as well as a series of sediment incubations, to quantify organic carbon oxidation by dissimilatory Fe reduction, Mn reduction, and sulfate reduction, in sediments from the Skagerrak (located off the northeast coast of Jutland, Denmark). In the deep portion of the basin, surface Mn enrichments reached 3.5 wt%, and Mn reduction was the only important anaerobic carbon oxidation process in the upper 10 cm of the sediment. In the less Mn-rich sediments from intermediate depths in the basin, Fe reduction ranged from somewhat less, to far more important than sulfate reduction. Most of the Mn reduction in these sediments may have been coupled to the oxidation of acid volatile sulfides (AVS), rather than to dissimilatory reduction. High rates of metal oxide reduction at all sites were driven by active recycling of both Fe and Mn, encouraged by bioturbation. Recycling was so rapid that the residence time of Fe and Mn oxides, with respect to reduction, ranged from 70-250 days. These results require that, on average, an atom of Fe or Mn is oxidized and reduced between 100-300 times before ultimate burial into the sediment. We observed that dissolved Mn2+ was completely removed onto fully oxidized Mn oxides until the oxidation level of the oxides was reduced to about 3.8, presumably reflecting the saturation by Mn2+ of highly reactive surface adsorption sites. Fully oxidized Mn oxides in sediments, then, may act as a cap preventing Mn2+ escape. We speculate that in shallow sediments of the Skagerrak, surface Mn oxides are present in a somewhat reduced oxidation level (< 3.8) allowing Mn2+ to escape, and perhaps providing the Mn2+ which enriches sediments of the deep basin.

Pathways of organic carbon oxidation in three continental margin sediments

We have combined several different methodologies to quantify rates of organic carbon mineralization by the various electron acceptors in sediments from the coast of Denmark and Norway. Rates of NH4+ and Sigma CO2 liberation sediment incubations were used with O2 penetration depths to conclude that O2 respiration accounted for only between 3.6-17.4% of the total organic carbon oxidation. Dentrification was limited to a narrow zone just below the depth of O2 penetration, and was not a major carbon oxidation pathway. The processes of Fe reduction, Mn reduction and sulfate reduction dominated organic carbon mineralization, but their relative significance varied depending on the sediment. Where high concentrations of Mn-oxide were found (3-4 wt% Mn), only Mn reduction occurred. With lower Mn oxide concentrations more typical of coastal sediments, Fe reduction and sulfate reduction were most important and of a similar magnitude. Overall, most of the measured O2 flux into the sediment was used to oxidized reduced inorganic species and not organic carbon. We suspect that the importance of O2 respiration in many coastal sediments has been overestimated, whereas metal oxide reduction (both Fe and Mn reduction) has probably been well underestimated.

Comparative Earth History and Late Permian Mass Extinction

The repeated association during the late Neoproterozoic Era of large carbon-isotopic excursions, continental glaciation, and stratigraphically anomalous carbonate precipitation provides a framework for interpreting the reprise of these conditions on the Late Permian Earth. A paleoceanographic model that was developed to explain these stratigraphically linked phenomena suggests that the overturn of anoxic deep oceans during the Late Permian introduced high concentrations of carbon dioxide into surficial environments. The predicted physiological and climatic consequences for marine and terrestrial organisms are in good accord with the observed timing and selectivity of Late Permian mass extinction.

N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica.

In oxygen-depleted zones of the open ocean, and in anoxic basins and fjords, denitrification (the bacterial reduction of nitrate to give N2) is recognized as the only significant process converting fixed nitrogen to gaseous N2. Primary production in the oceans is often limited by the availability of fixed nitrogen such as ammonium or nitrate, and nitrogen-removal processes consequently affect both ecosystem function and global biogeochemical cycles. It was recently discovered that the anaerobic oxidation of ammonium with nitrite—the ‘anammox’ reaction, performed by bacteria—was responsible for a significant fraction of N2 production in some marine sediments. Here we show that this reaction is also important in the anoxic waters of Golfo Dulce, a 200-m-deep coastal bay in Costa Rica, where it accounts for 19–35% of the total N2 formation in the water column. The water-column chemistry in Golfo Dulce is very similar to that in oxygen-depleted zones of the oceans—in which one-half to one-third of the global nitrogen removal is believed to occur. We therefore expect the anammox reaction to be a globally significant sink for oceanic nitrogen.

Isotopic evidence for microbial sulphate reduction in the early Archaean era.

Sulphate-reducing microbes affect the modern sulphur cycle, and may be quite ancient, though when they evolved is uncertain. These organisms produce sulphide while oxidizing organic matter or hydrogen with sulphate. At sulphate concentrations greater than 1 mM, the sulphides are isotopically fractionated (depleted in 34S) by 10–40‰ compared to the sulphate, with fractionations decreasing to near 0‰ at lower concentrations. The isotope record of sedimentary sulphides shows large fractionations relative to seawater sulphate by 2.7 Gyr ago, indicating microbial sulphate reduction. In older rocks, however, much smaller fractionations are of equivocal origin, possibly biogenic but also possibly volcanogenic. Here we report microscopic sulphides in ∼3.47-Gyr-old barites from North Pole, Australia, with maximum fractionations of 21.1‰, about a mean of 11.6‰, clearly indicating microbial sulphate reduction. Our results extend the geological record of microbial sulphate reduction back more than 750 million years, and represent direct evidence of an early specific metabolic pathway—allowing time calibration of a deep node on the tree of life.

Ferruginous Conditions Dominated Later Neoproterozoic Deep-Water Chemistry

Earths surface chemical environment has evolved from an early anoxic condition to the oxic state we have today. Transitional between an earlier Proterozoic world with widespread deep-water anoxia and a Phanerozoic world with large oxygen-utilizing animals, the Neoproterozoic Era [1000 to 542 million years ago (Ma)] plays a key role in this history. The details of Neoproterozoic Earth surface oxygenation, however, remain unclear. We report that through much of the later Neoproterozoic (<742 ± 6 Ma), anoxia remained widespread beneath the mixed layer of the oceans; deeper water masses were sometimes sulfidic but were mainly Fe2+-enriched. These ferruginous conditions marked a return to ocean chemistry not seen for more than one billion years of Earth history.

Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes

Geochemical data suggest that oxygenation of the Earth’s atmosphere occurred in two broad steps. The first rise in atmospheric oxygen is thought to have occurred between ∼2.45 and 2.2 Gyr ago, leading to a significant increase in atmospheric oxygen concentrations and concomitant oxygenation of the shallow surface ocean. The second increase in atmospheric oxygen appears to have taken place in distinct stages during the late Neoproterozoic era (∼800–542 Myr ago), ultimately leading to oxygenation of the deep ocean ∼580 Myr ago, but details of the evolution of atmospheric oxygenation remain uncertain. Here we use chromium (Cr) stable isotopes from banded iron formations (BIFs) to track the presence of Cr(VI) in Precambrian oceans, providing a time-resolved picture of the oxygenation history of the Earth’s atmosphere–hydrosphere system. The geochemical behaviour of Cr is highly sensitive to the redox state of the surface environment because oxidative weathering processes produce the oxidized hexavalent [Cr(VI)] form. Oxidation of reduced trivalent [Cr(III)] chromium on land is accompanied by an isotopic fractionation, leading to enrichment of the mobile hexavalent form in the heavier isotope. Our fractionated Cr isotope data indicate the accumulation of Cr(VI) in ocean surface waters ∼2.8 to 2.6 Gyr ago and a likely transient elevation in atmospheric and surface ocean oxygenation before the first great rise of oxygen 2.45–2.2 Gyr ago (the Great Oxidation Event). In ∼1.88-Gyr-old BIFs we find that Cr isotopes are not fractionated, indicating a decline in atmospheric oxygen. Our findings suggest that the Great Oxidation Event did not lead to a unidirectional stepwise increase in atmospheric oxygen. In the late Neoproterozoic, we observe strong positive fractionations in Cr isotopes (δ53Cr up to +4.9‰), providing independent support for increased surface oxygenation at that time, which may have stimulated rapid evolution of macroscopic multicellular life.