Invited commentary: lubricating the rusty wheel, new insights into iron oxidizing bacteria through comparative genomics

Iron is the fourth most abundant mineral in the Earth’s lithosphere (Weber et al., 2006; Emerson et al., 2013), where it is present at a mean concentration of 5% (Hedrich et al., 2011). Iron can exist in two oxidation stages as ferrous (Fe(II)) and ferric (Fe(III)) iron and some bacteria and archaea have evolved to use iron as an obligate or facultative energy source, giving them the name “Iron Oxidizing Bacteria” (FeOB) and “Iron Oxidizing Archaea” (FeOA), respectively (Figure 1). The oxidation from Fe(II) to Fe(III) can occur under both oxic and anoxic conditions within a pH range between 0.5 to 8.4 (Edwards et al., 2000; Weber et al., 2006; Hedrich et al., 2011). Here, the microbially mediated oxidation of iron under (micro-)aerobic circum-neutral conditions will be discussed. The biogeochemistry of iron poses several challenges to iron oxidizing microbes (for a detailed review see Weber et al., 2006). In circum-neutral environments and in the presence of oxygen, rapid abiotic oxidation of Fe(II) occurs, with half-life times of less than 60 s (Emerson et al., 2010). This abiotic oxidation to poorly soluble iron-oxyhydroxides reduces the availability of Fe(II) for biological process significantly. Microbial oxidation of Fe(II) therefore generally occurs in microaerophilic environments, which extend the half-life time of ferrous iron while at the same time increasing the amount of soluble Fe(II) (Bonnefoy and Holmes, 2012). Further, the oxidation from ferrous to ferric iron under low oxygen partial pressure increases the Gibbs free energy yield from 29 to −90 kJ mol−1 Fe(II) (Emerson et al., 2010). Iron oxidizing bacteria and archaea have contributed on a global scale to shape the lithosphere (Emerson and Moyer, 2002; Weber et al., 2006). Evidence of their impact on the global iron cycle has been dated back to Pre-Cambrian age where they are thought to have potentially aided in the deposition of banded iron formations (Hedrich et al., 2011). Even today they have a major impact on terrestrial and aquatic systems. FeOB and FeOA can be found in habitats ranging from deep sea vents to freshwater systems and the rhizosphere and can form thick mats and deposits from a few millimeters to tens of centimeters thick. More recently, these microbes have made their appearance in man-made environments and industrial processes (Valdes et al., 2008). Most commonly knownmay be their contribution to biofouling and corrosion where the buildup of ferric iron can lead to a reduction in the water flow rates and water quality (Hedrich et al., 2011; Mcbeth et al., 2011). Iron oxidizing microbes and their geological significance were first described in the 19th century (Ehrenberg, 1837; Harder, 1919). They are of key importance to global biogeochemical processes and more recently have gained interest for their impact on man-made environments (Hedrich et al., 2011). Yet, progress in understanding the ecology, physiology and genetic analysis of iron oxidizing microbes has been slow (Weber et al., 2006). Although iron oxidizing microbes can be readily observed in nature due to their striking morphology (such as the iconic stalk-forming Gallionella) and ability to form large microbial mats, they have proven elusive to cultivation under laboratory conditions. This elusiveness has caused confusion in the past, where taxonomy was inferred exclusively by morphological and ecological characteristics (Emerson et al., 2010). Recent advances in culturing techniques (Fabisch et al., 2013; Tischler et al., 2013) and culture-independent high-throughput DNA sequencing methods are providing a clearer phylogenetic picture of these bacteria (Emerson et al., 2010). The recent availability of metagenomic data in particular has greatly accelerated our understanding of iron oxidizing microbes (Wang et al., 2011; Yelton et al., 2013). Only 54 bacterial and 13 archaeal genomes of FeOB are publicly accessible to date (Weber et al., 2006; Cardenas et al., 2010; Emerson et al., 2010; Hedrich et al., 2011), on which the emerging sequencebased taxonomic framework is built upon