Nitrogen is an essential component of all living organisms and the main nutrient limiting life on our planet By far, the largest inventory of freely accessible nitrogen is atmospheric dinitrogen, but most organisms rely on more bioavailable forms of nitrogen, such as ammonium and nitrate, for growth The availability of these substrates depends on diverse nitrogen-transforming reactions that are carried out by complex networks of metabolically versatile microorganisms In this Review, we summarize our current understanding of the microbial nitrogen-cycling network, including novel processes, their underlying biochemical pathways, the involved microorganisms, their environmental importance and industrial applications

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The microbial nitrogen-cycling network

Microbial activities drive the global nitrogen cycle, and in the past few years, our understanding of nitrogen cycling processes and the micro-organisms that mediate them has changed dramatically. During this time, the processes of anaerobic ammonium oxidation (anammox), and ammonia oxidation within the domain Archaea, have been recognized as two new links in the global nitrogen cycle. All available evidence indicates that these processes and organisms are critically important in the environment, and particularly in the ocean. Here we review what is currently known about the microbial ecology of anaerobic and archaeal ammonia oxidation, highlight relevant unknowns and discuss the implications of these discoveries for the global nitrogen and carbon cycles.

https://faculty.ucmerced.edu/mbeman/Publications_files/FRANCIS07_ISMEJ.pdf

New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation.

Major insights into the phylogenetic distribution, biochemistry, and evolutionary significance of organelles involved in ATP synthesis (energy metabolism) in eukaryotes that thrive in anaerobic environments for all or part of their life cycles have accrued in recent years. All known eukaryotic groups possess an organelle of mitochondrial origin, mapping the origin of mitochondria to the eukaryotic common ancestor, and genome sequence data are rapidly accumulating for eukaryotes that possess anaerobic mitochondria, hydrogenosomes, or mitosomes. Here we review the available biochemical data on the enzymes and pathways that eukaryotes use in anaerobic energy metabolism and summarize the metabolic end products that they generate in their anaerobic habitats, focusing on the biochemical roles that their mitochondria play in anaerobic ATP synthesis. We present metabolic maps of compartmentalized energy metabolism for 16 well-studied species. There are currently no enzymes of core anaerobic energy metabolism that are specific to any of the six eukaryotic supergroup lineages; genes present in one supergroup are also found in at least one other supergroup. The gene distribution across lineages thus reflects the presence of anaerobic energy metabolism in the eukaryote common ancestor and differential loss during the specialization of some lineages to oxic niches, just as oxphos capabilities have been differentially lost in specialization to anoxic niches and the parasitic life-style. Some facultative anaerobes have retained both aerobic and anaerobic pathways. Diversified eukaryotic lineages have retained the same enzymes of anaerobic ATP synthesis, in line with geochemical data indicating low environmental oxygen levels while eukaryotes arose and diversified.

Biochemistry and Evolution of Anaerobic Energy Metabolism in Eukaryotes

Summary The widespread occurrence and diversity of ammonia oxidizing Archaea suggests their contribution to the nitrogen cycle is of global significance. Their dis- tribution appeared limited to low- and moderate- temperature environments until the recent finding of a diagnostic membrane lipid, crenarchaeol, in terres- trial hot springs. We report here the cultivation of a thermophilic nitrifier ('Candidatus Nitrosocaldus yel- lowstonii'), an autotrophic crenarchaeote growing up to 74°C by aerobic ammonia oxidation. The major core lipid of this archaeon growing at 72°C is crenar- chaeol, providing the first direct evidence for its syn- thesis by a thermophile. These findings greatly extend the upper temperature limit of nitrification and document that the capacity for ammonia oxidation is broadly distributed among the Crenarchaeota.

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Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol.

. Coastal hypoxia (defined here as Hypoxia alters both the structure and function of benthic communities, but effects may differ with regional hypoxia history. Human-caused hypoxia is generally linked to eutrophication, and occurs adjacent to watersheds with large populations or agricultural activities. Many occurrences are seasonal, within estuaries, fjords or enclosed seas of the North Atlantic and the NW Pacific Oceans. Benthic faunal responses, elicited at oxygen levels below 2 ml L−1, typically involve avoidance or mortality of large species and elevated abundances of enrichment opportunists, sometimes prior to population crashes. Areas of low oxygen persist seasonally or continuously beneath upwelling regions, associated with the upper parts of oxygen minimum zones (SE Pacific, W Africa, N Indian Ocean). These have a distribution largely distinct from eutrophic areas and support a resident fauna that is adapted to survive and reproduce at oxygen concentrations

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Effects of natural and human-induced hypoxia on coastal benthos

Several foraminiferal protozoa species grow in anoxic zones in marine sediment, but the type of anaerobic respiration that sustains them was not known. These organisms have now been found to accumulate nitrate intracellularly at concentrations more than 500 times the environmental values. The nitrate substitutes for oxygen in these anoxic habitats. The large amounts of nitrate that accumulate may even allow them to 'hold their breath' for more than a month. Denitrification, the biological conversion of nitrate to nitrogen, was believed to be restricted to bacteria and archaea. It has now been shown that highly abundant benthic foraminifers are also capable of denitrification, suggesting that much remains to be learned about the global nitrogen cycle. Benthic foraminifera are unicellular eukaryotes found abundantly in many types of marine sediments. Many species survive and possibly reproduce in anoxic habitats1, but sustainable anaerobic metabolism has not been previously described. Here we demonstrate that the foraminifer Globobulimina pseudospinescens accumulates intracellular nitrate stores and that these can be respired to dinitrogen gas. The amounts of nitrate detected are estimated to be sufficient to support respiration for over a month. In a Swedish fjord sediment where G. pseudospinescens is the dominant foraminifer, the intracellular nitrate pool in this species accounted for 20% of the large, cell-bound, nitrate pool present in an oxygen-free zone. Similarly high nitrate concentrations were also detected in foraminifera Nonionella cf. stella and a Stainforthia species, the two dominant benthic taxa occurring within the oxygen minimum zone of the continental shelf off Chile. Given the high abundance of foraminifera in anoxic marine environments1,2,3, these new findings suggest that foraminifera may play an important role in global nitrogen cycling and indicate that our understanding of the complexity of the marine nitrogen cycle is far from complete.

Signe Ingvardsen

Papers

Evidence for complete denitrification in a benthic foraminifer