Abstract
The cyclic nature of specific conversions in the nitrogen cycle imposes strict limitations to the conversions observed in nature and explains for example why anaerobic ammonium oxidation (anammox) bacteria can only use nitrite – and not nitrate – as electron acceptor in catabolism, and why nitrite is required as additional electron donor for inorganic carbon fixation in anabolism. Furthermore, the biochemistry involved in nitrite-dependent anaerobic methane oxidation excludes the feasibility of using nitrate as electron acceptor. Based on the cyclic nature of these nitrogen conversions, we propose two scenarios that may explain the ecological role of recently discovered complete ammonia-oxidizing (comammox) Nitrospira spp., some of which were initially found in a strongly oxygen limited environment: (i) comammox Nitrospira spp. may actually catalyze an anammox-like metabolism using a biochemistry similar to intra-oxic nitrite-dependent methane oxidation, or (ii) scavenge all available oxygen for ammonia activation and use nitrate as terminal electron acceptor. Both scenarios require the presence of the biochemical machinery for ammonia oxidation to nitrate, potentially explaining a specific ecological niche for the occurrence of comammox bacteria in nature.
Highlights
Catabolic processes in chemotrophic microorganisms either rely on substrate fermentations or on oxidation of an electron donor with an external electron acceptor
Why anammox has been found only with nitrite as electron acceptor and not nitrate can readily be explained by the biochemistry of the anammox catabolism
Why anammox uses nitrite as electron donor in anabolism for carbon dioxide reduction to biomass is a direct resultant from the cyclic nature of anammox catabolism
Summary
Catabolic processes in chemotrophic microorganisms either rely on (organic) substrate fermentations or on oxidation of an electron donor with an external electron acceptor. As opposed to anaerobic methane oxidation, the catabolic reaction shown in Figure 3 concerns a perfect cyclic conversion since two of the electrons gained upon oxidation of ammonia to nitrite (6 emol/mol NH+4 ) are required to reduce two nitrite to nitric oxide, with subsequent dismutation to dinitrogen gas and molecular oxygen, while the remaining four electrons would be required for the reduction of O2 at the ammonia monooxygenase. Under aerobic conditions the electrons will be accepted by oxygen, but we propose that in case of oxygen limitation nitrate may serve as alternative electron acceptor, with the concomitant formation of nitrite: Overall, this results in the conversion of ammonia with oxygen and nitrate, forming two nitrite in a so-called nitrite comproportionation reaction (Figure 4):. As described for the nitric oxide dismutase-based anammoxlike pathway, the formation of 30N2 from 15N labeled ammonium as reported by van Kessel et al (2015) can readily be explained by this pathway, as here the 15N-labeled nitrite formed by comammox Nitrospira will serve as substrate for anammox
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