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      Editorial: Eukaryotic Microbes Store Nitrate for “Breathing” in Anoxia

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          Abstract

          The microbial nitrogen cycle is one of the most complex and environmentally important element cycles on Earth, but most studies focus exclusively on the direct involvement of prokaryotes. Therefore, this Research Topic was launched to attract more attention to the role of eukaryotic microbes in the nitrogen cycle. In seven contributions, new findings on intracellular storage and the dissimilatory and assimilatory use of nitrate by eukaryotic microbes are summarized and discussed. The Research Topic was inaugurated with a Review Article that provides an overview of the ecophysiology of nitrate storage and dissimilatory nitrate reduction by diverse marine eukaryotes (Kamp et al.). The review emphasizes that eukaryotic nitrate storage and dissimilatory nitrate reduction are far more widespread than previously envisioned. Even though this field of research is still in its infancies, recent advances further strengthen the ecological significance of this metabolic trait. Dissimilatory nitrate reduction has now been confirmed in various species, which are so far covering four out of eight major lineages in the eukaryotic tree of life, i.e., foraminifers, diatoms, fungi, and ciliates. Nitrate storage has been found in even six out of the eight lineages, i.e., foraminifers, gromiids, diatoms, fungi, dinoflagellates, haptophytes, and chlorophytes. A compilation of intracellular nitrate inventories in various sediments indicates that the eukaryotic intracellular nitrate pools vastly exceed porewater nitrate pools. Quantitative estimates on the phylogenetic partitioning of dissimilatory nitrate reduction suggest that eukaryotes may even rival prokaryotes in certain sediments. The Review Article was followed by six Original Research Articles. Two of them focus on nitrate storage and nitrogen turnover in sinking diatom-bacteria aggregates (Kamp et al.; Stief et al.). Depending on their size and respiration activity, diatom-bacteria aggregates can develop an anoxic center even at relatively high oxygen concentrations in the surrounding water. Aggregates sinking through oxygenated waters might thus be important hot spots for anaerobic nitrogen conversions, including denitrification and thus fixed-nitrogen loss. Anoxia inside the aggregates enables nitrate-storing and aggregate-forming diatoms, such as Skeletonema marinoi, to perform Dissimilatory Nitrate Reduction to Ammonium (DNRA). Interestingly though, the nitrate initially stored by diatoms also becomes available to the bacterial community of the aggregate during its descent. This partially uncouples the denitrification activity by aggregate-associated bacteria from ambient nitrogen supplies. It was also speculated that intracellular nitrate not converted before the aggregates have settled onto the seafloor might fuel benthic nitrogen transformations (Marzocchi et al., 2017). Two articles of this Research Topic deal with foraminifers, which were the first marine eukaryotes, found to perform denitrification on intracellular nitrate in anoxic conditions (Risgaard-Petersen et al., 2006). This groundbreaking finding has since stimulated research on denitrification by foraminifera and their endobionts (e.g., Piña-Ochoa et al., 2010; Bernhard et al., 2012). Here, additional research activities centering on foraminifera exposed to anoxic conditions are presented. Nitrate incorporation and subsequent assimilation by foraminifera, or possibly by their endobionts, in dysoxic or anoxic conditions has been studied by Nomaki et al. An important conclusion was that foraminiferal (intracellular) nitrate is not solely used for denitrification, but can also fuel nitrogen assimilation, even in oxygen-depleted environments. Along these lines, the in situ experiments with 13C- and 15N-labeled phytodetritus by Enge et al. provide insights into organic C and N uptake by calcareous foraminifera that were studied along a depth transect in sediments of the Oxygen Minimum Zone of the Arabian Sea. The study revealed that the cellular C/N uptake-ratio is lower, if foraminifers are exposed to lower oxygen concentrations. The authors discuss that the low C/N uptake-ratio is due to a greater demand or storage of organic (i.e., food-based) nitrogen in anoxic conditions and that it is potentially used (as nitrate) for denitrification and thus for energy conservation. Gromiids are rather large, nitrate-storing protists that, similar to diatom-bacteria aggregates, may turn anoxic internally due to their own respiration activity. Sources and sinks of intracellular nitrate in gromiids and the potential role of their bacterial endobionts in the ensuing nitrate dynamics were studied by Høgslund et al. Tracer experiments with 15N revealed that intracellular nitrate is both taken up from the environment and produced internally, probably by bacterial endobionts performing nitrification. Anoxia triggers denitrification activity that is apparently mediated by bacterial endobionts since it can be inhibited by antibiotics. The article by Garcia-Robledo et al. addresses the spatial-temporal dynamics of inorganic nutrients in the sediment of an intertidal mudflat with previously unseen comprehensiveness. The magnitude and relative importance of porewater, intracellular, and exchangeable pools of nitrate, ammonium, and phosphate were correlated with the seasonal dynamics in abundance and photosynthetic activity of benthic microalgae. Interestingly, exchangeable nitrate, i.e., nitrate ionically adsorbed to organic matter or clay particles, accounted for the largest fraction of the total sedimentary nitrate pool, a phenomenon so far only described for ammonium and phosphate. These results suggest that anoxic sediment layers may actually harbor two sources of nitrate, i.e., intracellular and exchangeable nitrate, which might supply electron acceptors to the microbial community. In summary, this Research Topic reports novel findings on nitrate storage and use across a broad phylogeny reaching from diatoms (and other microalgae) to foraminifers and gromiids. The included studies address the ecophysiology of the organisms and their environmental impact on pelagic and benthic habitats as well as in anoxic micro-niches, such as diatom-bacteria aggregates or even inside of gromiids. Further, the metabolic fate of assimilated nitrogen and the biogeochemical role of intracellular vs. adsorbed nitrogen compounds in sediments were revealed. The new perspectives provided here are expected to stimulate more research on the eukaryotic players in the nitrogen cycle, especially since their ecological significance is becoming increasingly clear. Author contributions All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. Conflict of interest statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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          Evidence for complete denitrification in a benthic foraminifer.

          Benthic foraminifera are unicellular eukaryotes found abundantly in many types of marine sediments. Many species survive and possibly reproduce in anoxic habitats, 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 environments, 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.
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            Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida.

            Benthic foraminifers inhabit a wide range of aquatic environments including open marine, brackish, and freshwater environments. Here we show that several different and diverse foraminiferal groups (miliolids, rotaliids, textulariids) and Gromia, another taxon also belonging to Rhizaria, accumulate and respire nitrates through denitrification. The widespread occurrence among distantly related organisms suggests an ancient origin of the trait. The diverse metabolic capacity of these organisms, which enables them to respire with oxygen and nitrate and to sustain respiratory activity even when electron acceptors are absent from the environment, may be one of the reasons for their successful colonization of diverse marine sediment environments. The contribution of eukaryotes to the removal of fixed nitrogen by respiration may equal the importance of bacterial denitrification in ocean sediments.
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              Denitrification likely catalyzed by endobionts in an allogromiid foraminifer.

              Nitrogen can be a limiting macronutrient for carbon uptake by the marine biosphere. The process of denitrification (conversion of nitrate to gaseous compounds, including N(2) (nitrogen gas)) removes bioavailable nitrogen, particularly in marine sediments, making it a key factor in the marine nitrogen budget. Benthic foraminifera reportedly perform complete denitrification, a process previously considered nearly exclusively performed by bacteria and archaea. If the ability to denitrify is widespread among these diverse and abundant protists, a paradigm shift is required for biogeochemistry and marine microbial ecology. However, to date, the mechanisms of foraminiferal denitrification are unclear, and it is possible that the ability to perform complete denitrification is because of the symbiont metabolism in some foraminiferal species. Using sequence analysis and GeneFISH, we show that for a symbiont-bearing foraminifer, the potential for denitrification resides in the endobionts. Results also identify the endobionts as denitrifying pseudomonads and show that the allogromiid accumulates nitrate intracellularly, presumably for use in denitrification. Endobionts have been observed within many foraminiferal species, and in the case of associations with denitrifying bacteria, may provide fitness for survival in anoxic conditions. These associations may have been a driving force for early foraminiferal diversification, which is thought to have occurred in the Neoproterozoic era when anoxia was widespread.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                07 December 2017
                2017
                : 8
                : 2439
                Affiliations
                [1] 1AIAS, Aarhus Institute of Advanced Studies, Aarhus University , Aarhus, Denmark
                [2] 2Nordcee, Department of Biology, University of Southern Denmark , Odense, Denmark
                Author notes

                Edited by: Hongyue Dang, Xiamen University, China

                Reviewed by: Frank Schreiber, Bundesanstalt für Materialforschung und Prüfung (BAM), Germany; Dirk De Beer, Max Planck Society (MPG), Germany

                *Correspondence: Peter Stief peterstief@ 123456biology.sdu.dk

                This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.02439
                5770622
                234c3ebe-4b8e-4cb2-ba57-fa7bdb7cd04e
                Copyright © 2017 Kamp and Stief.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 20 October 2017
                : 24 November 2017
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 4, Pages: 2, Words: 1401
                Funding
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Award ID: KA3187/2-1
                Categories
                Microbiology
                Editorial

                Microbiology & Virology
                nitrogen-cycle,diatoms,foraminifers,gromiids,endobionts,marine snow,intracellular nitrate,low-oxygen environments

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