Eukaryotic microbes store nitrate for “breathing” in anoxia

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Background

Dissimilatory nitrate reduction, a physiological mechanism to generate energy in the absence of oxygen, is an integral part of the microbial nitrogen cycle and best studied in prokaryotic microbes. In contrast, the list of eukaryotic microbes known to reduce nitrate dissimilatory is still short, but includes major global players such as diatoms, foraminifers, and fungi. In many eukaryotic microbes, the ability to reduce nitrate dissimilatory is coupled to the ability to store nitrate intracellularly. Nitrate is taken up from the surrounding water and stored inside the cell at concentrations by far exceeding ambient concentrations. The partitioning of this intracellular nitrate between dissimilation and assimilation remains unclear. When external electron acceptors (e.g. oxygen, nitrate) are short in supply, intracellular nitrate stores provide resource independence and metabolic flexibility. This might be especially important for motile organisms like benthic diatoms. They migrate up and down in sediments triggered by diurnal cycles or tides, and may take up nitrate in the upper, oxic sediment layers and use it for dissimilation in the deeper, anoxic layers. This life style exists in the only prokaryotic microbes that store nitrate intracellularly, the large sulfur bacteria, but remains to be demonstrated for eukaryotic microbes. It is also conceivable that the intracellular nitrate of eukaryotic microbes fuels dissimilatory nitrate reduction by prokaryotic endosymbionts. Thus, prokaryotic and/or eukaryotic genes might be involved in dissimilatory nitrate reduction that occurs inside eukaryotic microbes. So far, eukaryotic genes have only been identified in soil fungi, but in none of the aquatic representatives of eukaryotic nitrate reducers. Analyzing the genetic inventory of eukaryotic microbes that “breathe nitrate” will help to elucidate the evolutionary history of this metabolic trait. One obvious question is whether the great evolutionary success of e.g. diatoms and fungi is linked to the ability to reduce nitrate dissimilatory. Aside from these ecophysiological and evolutionary aspects, the environmental significance of the nitrogen turnover that accompanies eukaryotic nitrate respiration needs to be addressed. The products of the various pathways of dissimilatory nitrate reduction range from a harmless gas (i.e. dinitrogen) to a strong greenhouse gas (i.e. nitrous oxide). In particular, the ecological role of eukaryotic nitrate reducers in the spreading hypoxic and anoxic zones of the oceans must be described.
This Research Topic focuses on the intracellular storage of nitrate by microbial eukaryotes and its dissimilatory use for survival in oxygen-deficient zones of aquatic ecosystems. The aim is to summarize, collect, and discuss new findings on this understudied research topic. This includes studies on ecophysiology, functional gene inventory, and environmental impact, and a general discussion of open questions and modern tools that will inspire further research. This Research Topic is also meant to motivate researchers to test their pet eukaryote for intracellular nitrate storage because this might be the best hint for the capability to “breathe nitrate”.

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