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3 The Role of Microorganisms in Iron Reduction in Marine Sediments

       Carolina Reyes1 and Patrick Meister2

       1 Department of Environmental Geosciences, University of Vienna, Centre for Microbiology and Environmental Systems Science, Althanstrasse 14, 1090, Vienna, Austria

       2 Department of Geodynamics and Sedimentology, University of Vienna, Faculty of Earth Sciences, Geography and Astronomy, Althanstrasse 14, 1090, Vienna, Austria https://orcid.org0000‐0002‐7413‐607X

       Corresponding Author: Carolina Reyes ([email protected]), Patrick Meister ([email protected]) ORCiD code: 0000‐0003‐3623‐6456

      ABSTRACT

      Iron‐reducing microbial activity may occur in marine sediments in zones where it is not outcompeted by abiotic reaction of three‐valent (ferric) iron with sulfide. Because near neutral pH ferric iron prevails in solid form, microorganisms have developed different strategies for extracellular electron transfer. Microbial pili, nanowires, and electron shuttles have been observed in two microorganisms, Shewanella and Geobacter, to transfer electrons to iron oxide mineral surfaces. Alternatively, iron may be chelated and transported into the cell. However, other than in these two model microorganisms, the pathways of electron transfer are poorly understood. Previous diversity studies showed that a number of phylogenetic groups of both Bacteria and Archaea, capable of using iron as an electron acceptor, occur in marine sediments, some of which are versatile, capable of reducing various electron acceptors. These groups seem to be associated with zones of iron reduction, such as suboxic zones and sulfide‐free methanogenic zones, but their pathways of iron reduction are largely unknown. We highlight the necessity to further elucidate electron transport pathways including extracellular systems, using molecular genetic studies, to understand their ecological role in natural systems such as in marine sediments.

3.1. INTRODUCTION

      Iron is often reduced and oxidized within closely spaced zones in the marine sedimentary biome (Froelich et al. 1979), and iron oxides often represent the most abundant solid phase electron acceptor. Although three‐valent iron [iron(III)] does not spontaneously react with organic electron donors, such reactions may be mediated by microbial enzymatic pathways, providing a source of energy to the respective organisms residing in a particular location in a redox gradient. In contrast, iron(III) is abiotically reduced by sulfide. Under anoxic marine conditions, various reduced sulfur species may be available to react with iron (Canfield 1989; Rickard and Luther III, 2007). It is often difficult to assess whether iron cycling is driven by abiotic reaction with sulfide in a prevailing redox gradient, or whether it is the result of a microbial process. Nevertheless, evidence in a number of studies reviewed herein show that bacteria in marine environments are indeed using iron as electron acceptor in their metabolic pathways.

Microbially driven iron reduction most likely occurs in locations where reactions are not outcompeted by abiotic reduction of iron. Ocean margins, including shoreline, continental shelf, and slope regions, are abundant in terrigenous‐clastic sediments, which are generally iron‐rich but also rich in organic matter. In contrast, open‐ocean sediments generally receive limited iron from the continent but large amounts of iron are delivered from mid‐ocean ridge hydrothermal activity (not further discussed here). Sedimentary organic matter can be delivered from land to the ocean by river discharge or become deposited from marine primary production (de Haas et al. 2002). As a result, coastal upwelling zones, estuaries, and stagnant shelf basins may show anoxic conditions in bottom water, further enhancing the preservation of organic matter, giving rise to predominantly sulfidic conditions in the sediment. In turn, in shallow coastal areas water energy is often high (above the wave base), resulting in better ventilated, more oxic conditions at the sediment surface and suboxic conditions within the sediment, supporting iron cycling. Deep‐sea sediments also show suboxic conditions in some areas (e.g. Meister et al., 2009). Overall, different environmental factors support microbial iron cycling, but may also support reactions via competing pathways. It is still not entirely clear which factors control microbial iron reduction in marine sediments and, therefore, it is difficult to assess which pathways the organisms use to access this source of electron acceptors.

      The metabolic pathways involved in iron reduction are explored in detail in only two model organisms, Shewanella and Geobacter, but only the latter was suggested to be responsible for iron reduction in marine sediments. However, as shown by Reyes et al. (2016), several representatives of other phylogenetic groups with members capable of performing iron reduction were detected in Baltic Sea sediments, using DNA sequencing. Among these organisms, several groups are sulfate reducers or versatiles, possibly switching to iron reduction if the conditions are favorable. Furthermore, as iron itself plays a fundamental role as a reactive center in many electron‐transporting enzymes and cofactors, the availability of iron at trace amounts is a requirement for all organisms. Thus, understanding which organism can reduce iron and what strategies they use to access solid‐phase iron(III) would be fundamental to understanding the ecological role of iron cycling in marine systems.

      While current literature on this topic is rather limited, this chapter will provide a brief overview of current knowledge and highlight the role of iron‐reducing organisms in marine sediments. This chapter focuses on the question of where in the sediment iron reduction occurs and what microbial pathways are potentially involved. It then discusses which microorganisms are involved and how diverse these communities are. In addition, a compilation and a phylogenetic tree of known iron‐reducing microorganisms in the marine environment is presented and their functional diversity is discussed.

3.2. THE REDOX ZONES IN SHALLOW MARINE SEDIMENTS

      Dissolved iron(III) [Fe³⁺] under neutral to slightly alkaline pH prevailing in ocean margin sediments has a redox potential around 0 V, which enables this ion to serve as an electron acceptor for most anaerobic metabolic pathways, except for the oxidation of Mn(II) to Mn(IV) and NH₄ ⁺ to NO₃ ^– (Schulz and Zabel, 2006, p. 187). Accordingly, an iron reduction zone commonly occurs below the oxic/anoxic boundary, starting at the depth where nitrate and dissolved iron overlap (Froelich et al. 1979; König et al. 1999; Meister et al. 2014). The iron zone is also limited by the presence of dissolved sulfide, which reacts spontaneously with ferric iron to form insoluble iron sulfides (Schulz and Zabel, 2006, p. 247). In fact, the iron zone may be missing in cases where the iron content is low and sulfide production is overwhelming the production of dissolved iron(II) [Fe²⁺], which is generally the case in organic carbon‐rich sediments showing strong reducing conditions. In these cases, sulfide may even reach the seafloor, as shown, for example, by Calvert and Karlin (1991), or may be linked to nitrate reduction by Thioploca (Otte et al. 1999, pp. 3148–3157).

      The depth of the iron zone in the sequence of downward decreasing electron potential is, however, not just the result of spontaneous interaction of the ions. Froelich et al. (1979) demonstrated that a redox zonation arises due to a competitive advantage of the organisms capable of using a stronger

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