Abstract
Iron (Fe) is the fourth most abundant element in the Earth’s crust where ferrous Fe [Fe(II)] and ferric Fe [Fe(III)] can be used by archaea for energy conservation. In these archaea-Fe interactions, Fe(III) serves as terminal electron acceptor for anaerobic respiration by a variety of archaea, while Fe(II) serves as electron donor and/or energy sources for archaeal growth. As no Fe is incorporated into the archaeal cells, these redox reactions are referred to as dissimilatory Fe(III) reduction and Fe(II) oxidation, respectively. Dissimilatory Fe(III)-reducing archaea (FeRA) and Fe(II)-oxidizing archaea (FeOA) are widespread on Earth where they play crucial roles in biogeochemical cycling of not only Fe, but also carbon and sulfur. To reduce extracellular Fe(III) (oxyhydr)oxides, some FeRA transfer electrons directly to the Fe(III) (oxyhydr)oxides most likely via multiheme c-type cytochromes (c-Cyts). These multiheme c-Cyts may form the pathways similar to those found in bacteria for transferring electrons from the quinone/quinol pool in the cytoplasmic membrane to the Fe(III) (oxyhydr)oxides external to the archaeal cells. Use of multiheme c-Cyts for extracellular Fe(III) reduction by both Domains of Archaea and Bacteria emphasizes an ancient mechanism of extracellular electron transfer, which is well conserved. Other FeRA, however, reduce Fe(III) (oxyhydr)oxides indirectly via electron shuttles. Similarly, it is proposed that FeOA use pathways to oxidize Fe(II) on the surface of the cytoplasmic membrane and then to transfer the released electrons across the cytoplasmic membrane inward to the O2 and NAD+ in the cytoplasm. In this review, we focus on the latest understandings of the molecular mechanisms used by FeRA and FeOA for Fe(III) reduction and Fe(II) oxidation, respectively.
Highlights
By mass, iron (Fe) is the most abundant element on Earth and the fourth most abundant element in the Earth’s crust (Morgan and Anders, 1980)
Fe(III)-reducing archaea (FeRA) are found in different environmental settings, ranging from the sediment of freshwater lakes to deep sea hyperthermal vents, where they are involved in biogeochemical cycling of Fe, and carbon (C) (Slobodkina et al, 2009; Yamada et al, 2014; Weber et al, 2017)
This review focuses on our current understandings of the molecular mechanisms underlying the ability of FeRA and Fe(II)-oxidizing archaea (FeOA) to exchange electrons with Fe(III) and Fe(II), respectively
Summary
Iron (Fe) is the most abundant element on Earth and the fourth most abundant element in the Earth’s crust (Morgan and Anders, 1980). Some of these multiheme c-Cyt-encoding genes are acquired by the ANME from the Fe(III)-reducing bacteria via lateral gene transfer (Skennerton et al, 2017; Leu et al, 2020b) Their direct involvements in extracellular reduction of Fe(III) still remain to be demonstrated, the multiheme c-Cyts of these ANME may form the pathways similar to those found in the bacteria and that proposed in other FeRA (Figure 2A) to transfer electrons from the quinone/quinol pool in the cytoplasmic membrane, across the cell wall to the Fe(III) (oxyhydr)oxides or the bacterial cells contacted on the archaeal cell surface (Figure 2C; McGlynn et al, 2015; Shi et al, 2016; Jiang et al, 2019; Leu et al, 2020b). Given that they are different from those of bacteria (Bird et al, 2011; Bonnefoy and Holmes, 2012; Shi et al, 2012, 2016; Ilbert and Bonnefoy, 2013; Jiang et al, 2019), the molecular mechanisms for Fe(II) oxidation by FeOA must have evolved independently
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