Characterization of iron oxide nanoparticle films at the air–water interface in Arctic tundra waters

Highlights

• Biofilms from Arctic tundra air/water interfaces collected over 2 years were analyzed.

• Biofilms consist of EPS-coated iron (oxyhydr)oxide nanoparticle aggregates.

• Mineral phases of the iron (oxyhydr)oxide nanoparticles varied between years.

• Iron (oxyhydr)oxide biofilms may play an important role in Arctic carbon and iron cycles.

Abstract

Massive amounts of organic carbon have accumulated in Arctic permafrost and soils due to anoxic and low temperature conditions that limit aerobic microbial respiration. Alternative electron acceptors are thus required for microbes to degrade organic carbon in these soils. Iron or iron oxides have been recognized to play an important role in carbon cycle processes in Arctic soils, although the exact form and role as an electron acceptor or donor remain poorly understood. Here, Arctic biofilms collected during the summers of 2016 and 2017 from tundra surface waters on the Seward Peninsula of western Alaska were characterized with a suite of microscopic and spectroscopic methods. We hypothesized that these films contain redox-active minerals bound to biological polymers. The major components of the films were found to be iron oxide nanoparticle aggregates associated with extracellular polymeric substances. The observed mineral phases varied between films collected in different years with magnetite (Fe²⁺Fe₂³⁺O₄) nanoparticles (<5 nm) predominantly identified in the 2016 films, while for films collected in 2017 ferrihydrite-like amorphous iron oxyhydroxides were found. While the exact formation mechanism of these Artic iron oxide films remains to be explored, the presence of magnetite and other iron oxide/oxyhydroxide nanoparticles at the air–water interface may represent a previously unknown source of electron acceptors for continual anaerobic microbial respiration of organic carbon within poorly drained Arctic tundra.

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.