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Impact of Reactive Surfaces on the Abiotic Reaction Between Nitrite and Ferrous Iron and Associated Nitrogen and Oxygen Isotope Dynamics

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Impact of Reactive Surfaces on the Abiotic Reaction Between Nitrite and Ferrous Iron and Associated Nitrogen and Oxygen Isotope Dynamics Biogeosciences, 17, 4355–4374, 2020 https://doi.org/10.5194/bg-17-4355-2020 © Author(s) 2020. This work is distributed under the Creative Commons Attribution 4.0 License. Impact of reactive surfaces on the abiotic reaction between nitrite and ferrous iron and associated nitrogen and oxygen isotope dynamics Anna-Neva Visser1,4, Scott D. Wankel2, Pascal A. Niklaus3, James M. Byrne4, Andreas A. Kappler4, and Moritz F. Lehmann1 1Department of Environmental Sciences, Basel University, Bernoullistrasse 30, 4056 Basel, Switzerland 2Woods Hole Oceanographic Institution, Woods Hole, 360 Woods Hole Rd, MA 02543, USA 3Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland 4Department of Geosciences, Tübingen University, Hölderlinstrasse 12, 72074 Tübingen, Germany Correspondence: Anna-Neva Visser ([email protected]) Received: 28 February 2020 – Discussion started: 17 March 2020 Revised: 14 July 2020 – Accepted: 16 July 2020 – Published: 28 August 2020 Abstract. Anaerobic nitrate-dependent Fe(II) oxidation tions, suggesting an overall lower reactivity of the mineral- − (NDFeO) is widespread in various aquatic environments only set-up. Similarly, the average NO2 reduction rate in and plays a major role in iron and nitrogen redox dynam- the mineral-only experiments (0:004±0:003 mmol L−1 d−1) ics. However, evidence for truly enzymatic, autotrophic ND- was much lower than in the experiments with both min- −1 −1 FeO remains limited, with alternative explanations involv- eral and DB (0:053 ± 0:013 mmol L d ), as was N2O −1 −1 ing the coupling of heterotrophic denitrification with the abi- production (204:02 ± 60:29 nmol L d ). The N2O yield − otic oxidation of structurally bound or aqueous Fe(II) by re- per mole NO2 reduced was higher in the mineral-only set- active intermediate nitrogen (N) species (chemodenitrifica- ups (4 %) than in the experiments with DB (1 %), suggest- tion). The extent to which chemodenitrification is caused (or ing the catalysis-dependent differential formation of NO. N- − enhanced) by ex vivo surface catalytic effects has not been NO2 isotope ratio measurements indicated a clear differ- directly tested to date. To determine whether the presence ence between both experimental conditions: in contrast to the 15 − of either an Fe(II)-bearing mineral or dead biomass (DB) marked N isotope enrichment during active NO2 reduc- 15 catalyses chemodenitrification, two different sets of anoxic tion ( "NO DC10:3 ‰) observed in the presence of DB, − 2 batch experiments were conducted: 2 mM Fe(II) was added NO2 loss in the mineral-only experiments exhibited only a C − to a low-phosphate medium, resulting in the precipitation small N isotope effect (< 1 ‰). The NO2 -O isotope ef- − 18 of vivianite (Fe3.PO4/2), to which 2 mM nitrite (NO2 ) was fect was very low in both set-ups ( "NO2 <1 ‰), which was later added, with or without an autoclaved cell suspension most likely due to substantial O isotope exchange with am- (∼ 1:96 × 108 cells mL−1) of Shewanella oneidensis MR-1. bient water. Moreover, under low-turnover conditions (i.e. in − Concentrations of nitrite (NO2 ), nitrous oxide (N2O), and the mineral-only experiments as well as initially in experi- 2C − iron (Fe , Fetot) were monitored over time in both set-ups ments with DB), the observed NO2 isotope systematics sug- to assess the impact of Fe(II) minerals and/or DB as catalysts gest, transiently, a small inverse isotope effect (i.e. decreas- − 15 18 of chemodenitrification. In addition, the natural-abundance ing NO2 δ N and δ O with decreasing concentrations), − 15 18 isotope ratios of NO2 and N2O(δ N and δ O) were anal- which was possibly related to transitory surface complexa- ysed to constrain the associated isotope effects. Up to 90 % of tion mechanisms. Site preference (SP) of the 15N isotopes the Fe(II) was oxidized in the presence of DB, whereas only in the linear N2O molecule for both set-ups ranged between ∼ 65 % of the Fe(II) was oxidized under mineral-only condi- 0 ‰ and 14 ‰, which was notably lower than the values pre- Published by Copernicus Publications on behalf of the European Geosciences Union. 4356 A.-N. Visser et al.: Impact of reactive surfaces on the abiotic reaction viously reported for chemodenitrification. Our results imply Acidovorax delafieldii strain 2AN and Pseudogulbenkiania that chemodenitrification is dependent on the available reac- ferrooxidans strain 2002 (Chakraborty et al., 2011; Weber et − tive surfaces and that the NO2 (rather than the N2O) iso- al., 2009), is still not fully understood. It has been suggested tope signatures may be useful for distinguishing between that extracellular electron transfer (EET) might play a ma- chemodenitrification catalysed by minerals, chemodenitrifi- jor role in NDFeO, particularly in the presence of high lev- cation catalysed by dead microbial biomass, and possibly els of extracellular polymeric substances (EPS; Klueglein et true enzymatic NDFeO. al., 2014; Liu et al., 2018; Zeitvogel et al., 2017). EPS have been demonstrated to act as electron shuttles; hence, EET may indeed provide a plausible explanation for the observed Fe(II) oxidation in these cultures (Liu et al., 2018). The exis- 1 Introduction tence of such an electron transfer would imply that NDFeO is not necessarily a completely enzymatically catalysed reac- Iron (Fe) is essential for all living beings, and its biogeo- tion. Considering that all putative NDFeO strains were grown − chemical cycling has been studied extensively (Expert, 2012; under high (up to 10 mM) nitrate (NO3 ) and Fe(II) concen- Lovley, 1997). Although Fe is ubiquitous in most environ- trations and accumulated up to several millimoles of nitrite − − ments, it is not always bioavailable (Andrews et al., 2003; (NO2 ) from enzymatic NO3 reduction, other studies sug- Ilbert and Bonnefoy, 2013), and microorganisms must of- gested that the observed Fe(II) oxidation in these pure cul- ten cope with Fe limitation in their respective environments tures may be due to the abiotic side reaction between the − (Braun and Hantke, 2013; Ilbert and Bonnefoy, 2013). This generated NO2 and Fe(II) (Buchwald et al., 2016; Dhakal, is especially true at circumneutral pH and oxic conditions, 2013; Klueglein et al., 2014). This abiotic reaction between − where Fe(II) is quickly oxidized by O2 and, thus, only NO2 and Fe(II) is known as chemodenitrification (Eq. 1) and present as poorly soluble Fe(III)(oxyhydr)oxides (Cornell is proposed to lead to an enhanced production of N2O (An- and Schwertmann, 2003; Stumm and Sulzberger, 1992). In derson and Levine, 1986; Buchwald et al., 2016; Zhu-Barker contrast, under anoxic conditions, Fe is mainly present as ei- et al., 2015). ther dissolved Fe2C or as mineral-bound Fe(II) in Fe phos- 2C C − C ! C phates or carbonates (Charlet et al., 1990; Luna-Zaragoza et 4Fe 2NO2 5H2O 4FeOOH N2O al., 2009). Here, microbes use electron acceptors other than C 6HC1G◦ D −128:5kJmol−1 (1) O2 for respiration (He et al., 2016b; Lovley, 2012; Straub et al., 1996). One redox pair that has been proposed to be ex- Several studies have noted that the presence of reactive ploited by microbes under anoxic conditions through a mech- surfaces may enhance the abiotic reaction (Heil et al., 2016; anism known as nitrate-dependent Fe(II) oxidation (NDFeO) Sorensen and Thorling, 1991). For example, Klueglein and is NO−=Fe2C (Ilbert and Bonnefoy, 2013; Straub et al., Kappler (2013) tested the impact of goethite on Fe-coupled 3 − 1996). To date, genetic evidence that clearly supports this chemodenitrification in the presence of high Fe(II) and NO2 metabolic capacity of the studied microorganisms remains concentrations, and they confirmed the concentration de- lacking (Price et al., 2018), and biogeochemical evidence is pendency of this reaction with regard to both species (Van rare and putative. The latter is mostly based on experiments Cleemput and Samater, 1995). Possible catalytic effects (e.g. with the chemolithoautotrophic culture KS, which is a con- by reactive surfaces and/or organic matter) were not tested sortium of four different strains, including a relative of the specifically in these studies. However, multiple factors have − microaerophilic Sideroxydans/Gallionella. This enrichment been shown to affect the abiotic reaction between NO2 and culture has been shown to oxidize Fe(II) without the addition Fe(II) and may need to be considered, i.e. pH, temperature, of any organic co-substrates (Tominski et al., 2018). Tian et Fe2C concentrations, solubility of Fe(III)(oxyhydr)oxides, al. (2020) confirmed that Gallionellaceae are able to perform crystallinity of Fe(II) minerals, other metal ion concentra- autotrophic Fe(II)-dependent denitrification. Another more tions, and catalytic effects (Van Cleemput and Samater, 1995; indirect line of evidence includes results from slurry micro- Klueglein and Kappler, 2013; Ottley et al., 1997). In addition, cosm experiments with marine coastal sediments. In these the presence of organic compounds can lead to the abiotic − experiments, Fe(II) oxidation was still detected even after reduction of NO2 to NO (Van Cleemput and Samater, 1995; all bioavailable organics of the sediments were consumed McKnight et al., 1997; Pereira et al., 2013). − and only NO3 was left (Laufer et al., 2016). With regard Given the complex controls and potential interaction be- to other studies where NDFeO was initially thought to be tween Fe(II) and various nitrogenous compounds, including performed by autotrophs (Chakraborty et al., 2011; Weber intermediates, it may be an oversimplification to state that et al., 2009), it was subsequently shown that the microbes Fe(II) oxidation observed in previous laboratory set-ups is − rely on an organic co-substrate and must in fact be con- solely caused by the abiotic reaction with NO2 and not, for sidered mixotrophic (Klueglein et al., 2014; Muehe et al., example, stimulated by reactive surfaces (minerals, organic- 2009).
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