Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction

The oxidation of ammonium is a key step in the nitrogen cycle, regulating the production of nitrate, nitrous oxide and dinitrogen. In marine and freshwater ecosystems, anaerobic ammonium oxidation coupled to nitrite reduction, termed anammox, accounts for up to 67% of dinitrogen production1–3. Dinitrogen production through anaerobic ammonium oxidation has not been observed in terrestrial ecosystems, but the anaerobic oxidation of ammonium to nitrite has been observed in wetland soils under iron-reducing conditions4,5. Here, we incubate tropical upland soil slurries with isotopically labelled ammonium and iron(III) to assess the potential for anaerobic ammonium oxidation coupled to iron(III) reduction, otherwise known as Feammox6, in these soils. We show that Feammox can produce dinitrogen, nitrite or nitrate in tropical upland soils. Direct dinitrogen production was the dominant Feammox pathway, short-circuiting the nitrogen cycle and resulting in ecosystem nitrogen losses. Rates were comparable to aerobic nitrification7,8 and to denitrification9, the latter being the only other process known to produce dinitrogen in terrestrial ecosystems. We suggest that Feammox could fuel nitrogen losses in ecosystems rich in poorly crystalline iron minerals, with low or fluctuating redox conditions. Terrestrial net primary productivity is often limited by the availability of fixed nitrogen (N) owing in large part to the mobility of N across ecosystem boundaries, particularly through denitrification10. Denitrification is dominantly a microbial process that converts nitrate (NO3−) to nitrous oxide (N2O) and dinitrogen (N2) gases. In terrestrial ecosystems, denitrification is thought to be the only process by which fixed N is converted to N2, thereby completing the nitrogen cycle. In aquatic systems, anammox bypasses the potential for N2O production as well as decreasing internal N cycling. Bacteria capable of anammox have been detected in soil11,12, but the occurrence of anammox has not been demonstrated in terrestrial ecosystems13. The reduction of ferric iron (Fe(iii)) can be coupled to anaerobic ammonium (NH4+) oxidation to produce N2 (ref. 14), NO3−(ref. 14), or NO2− (refs 4–6). This process is termed Feammox6 and theoretically could occur abiotically or be microbially mediated. There is some evidence of Feammox to NO2− in wetland soils4,5, but Feammox to N2 has not been previously described nor has Feammox been measured in upland soils. Feammox to N2 is energetically more favourable than Feammox to NO2− or NO3− and is favourable over a wider range of conditions. Environments rich in poorly crystalline Fe minerals, such as highly weathered soils, have the potential to support Feammox. Under conditions typically found in soil, Feammox to N2 using ferrihydrite, a common poorly crystalline Fe oxide, yields