Characterization of iron oxide nanoparticle films at the air–water interface in Arctic tundra waters
Graphical abstract
Introduction
Iron (Fe) oxides and oxyhydroxides are ubiquitous in nature and play an important role in the environmental cycling of carbon (C) and other nutrients (Cornell and Schwertmann, 2003). These minerals can be formed by both abiotic (Laurent et al., 2008) and biotic processes that produce a wide variety of both amorphous and crystalline iron oxides or oxyhydroxides. For instance, magnetotactic bacteria produce single magnetic domain nanoparticles for geolocation purposes (Blakemore, 1975; Frankel et al., 1979; Kolinko et al., 2014). Aerobic bacteria such as Leptothrix, Sphaerotilus, and Gallionella spp. (Corstjens et al., 1992) oxidize ferrous Fe(II), forming filamentous microbial mats (Emerson and Revsbech, 1994; Emerson et al., 2010; Angelova et al., 2015; Nedkov et al., 2016). Fe(II) can also react with molecular oxygen (O2) to produce hydroxyl radicals that oxidize dissolved organic carbon through abiotic processes (Trusiak et al., 2018). On the other hand, dissimilatory iron reducing bacteria couple the oxidation of organic C with the reduction of Fe(III) minerals or complexes, producing soluble Fe(II) or mixed-valence iron oxides such as magnetite (Fe2+Fe23+O4) (Lovley, 1997; Fredrickson et al., 1998). Mixed-valence iron oxide/oxyhydroxide minerals can influence the complex cycling of C and other nutrients, because these minerals can serve as both an electron source and sink for microbes, effectively acting as a biogeobattery, as recently demonstrated by Byrne et al. (2015). This cycle of continuous Fe reduction and oxidation across redox zones drives soil organic C degradation (Emerson et al., 2012).
Currently, there is a great interest in assessing and understanding the C cycle in Arctic ecosystems due to the potential release of greenhouse gases from frozen soil organic matter (permafrost) upon thaw and microbial degradation (Schuur et al., 2008, Schuur et al., 2009; Hinzman et al., 2013; Hugelius et al., 2014; Herndon et al., 2015; Schädel et al., 2016). The C and Fe cycles are intimately linked in these ecosystems through biologically mediated and hydrological processes. High concentrations of iron in many Arctic soils have prompted studies seeking to elucidate the role that Fe reducing and oxidizing bacteria play in degrading organic C stocks (Lipson et al., 2010, Lipson et al., 2013; Emerson et al., 2015; Miller et al., 2015). While initial studies have focused on mineral-microbial interactions for C degradation occurring in permafrost-affected soils or wet tundra systems (Herndon et al., 2015, Herndon et al., 2017; Yang et al., 2016), little attention has been given to processes occurring at the air-water interface for these ecosystems.
We have observed the ubiquitous presence of iridescent films on the surface of standing waters in small ponds and pools across field sites during multiple field campaigns on the Seward Peninsula in western Alaska. However, the nature and molecular composition for these films are largely unknown. We hypothesize that: (i) these films were formed at the natural redox transition zone represented by the air-water interface via microbially mediated Fe(II) oxidation, and (ii) they consist of phases that could act as electron acceptors and/or donors and thus contribute to organic matter degradation in these anoxic tundra environments. To our knowledge, there have been no reports on iron oxide/oxyhydroxide nanoparticle formation in Arctic surface waters at the air-water interface. Identifying the nature of Fe containing minerals produced in these systems could thus be important for understanding both C and Fe cycling when the oxides/oxyhydroxides sink into anoxic zones and are subsequently reduced.
The present research characterizes the organic and mineral composition of the films using a suite of microscopic and spectroscopic methods to determine their possible origins and biogeochemical significance. Here high-resolution transmission electron microscopy (in both scanning and conventional modes; STEM and TEM, respectively), energy dispersive X-ray spectroscopy (EDS), and electron energy loss spectroscopy (EELS) were used to determine the morphology, elemental composition, and mineralogy of the films. Surface enhanced Raman scattering (SERS) and Fourier transform infrared (FTIR) spectroscopy were used to characterize any associated organic phases, such as extracellular polymeric substances (EPS), and thus microbial roles in the formation of the Arctic surface films. Results detailing the chemical and structural characters for these surface water films are discussed in the context of understanding the potential roles that these films at the air-water interface play for the biogeochemical cycling of Fe and C within the Arctic tundra environment.
Section snippets
Site description and sample collection
Samples were collected from September 7 to 15, 2016 and August 8 to 12, 2017 at a field research site located ~27 miles outside of Nome, Alaska, along the Teller Road. The site, established by the Department of Energy Office of Science, Next-Generation Ecosystem Experiments (NGEE Arctic) project, is characterized by a watershed with a peat plateau underlain by permafrost at the top of the hillslope, willow shrubs, mosses, lichens and sedges on drier hillslopes, and a saturated, peaty lowland at
General water chemistry
Typical pH values for the surface waters collected in both years were ~5.5, lower than the median pH value of ~6.8 measured for waters from across the Teller site. Water chemistry data for both years are given in the Supporting information (see Table S1 and Fig. S1) where the observed concentrations for the major ions (e.g., Fe2+, Cl−, SO42−) present are similar. The waters contained relatively high levels of Fe(II), ~2.1 mg l−1 and ~4.9 mg l−1, in 2016 and 2017, respectively. Additionally,
Conclusions
The analytical results presented here indicate that the films observed in 2016 and 2017 at the air–water interface for Arctic tundra surface waters are comprised predominantly of a combination of extracellular polymeric substances and iron oxide/oxyhydroxide nanoparticle aggregates. For samples collected in 2016 magnetite phases were observed within these surface films. The presence of naturally occurring iron oxide/oxyhydroxide nanoparticle thin films in poorly drained tundra may have
Author contributions
AMJ, JRE, and BG designed the experiments; AMJ, JZ, MJP, DEG, SDW, and BG collected the film samples; AMJ performed FTIR and SERS analyses; JRE performed STEM/TEM, EDS, and EELS analyses, JZ and XY performed bulk water chemistry characterization, AMJ, JRE, EMP, and BG performed data analysis; all authors contributed to writing the manuscript.
Notes
The authors declare no competing financial interest.
Acknowledgements
This work was supported by the Office of Biological and Environmental Research in the United States Department of Energy (DOE) Office of Science, as part of the Next Generation Ecosystem Experiments (NGEE Arctic) project. We thank the Sitnasuak Native Corporation for issuing the land use permit that allows access to this research site along the Teller Road. The manuscript has been authored by Oak Ridge National Laboratory (ORNL), which is managed by UT-Battelle LLC for the DOE under Contract
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These authors contributed equally to this work.