The ability of microorganisms to transfer electrons to and from metals was one of the recent major discoveries made by the Geomicrobiology field [4,5]. The importance of this finding is evident, having changed the way scientists nowadays apprehend metal cycles.
Metals are highly abundant on our planet. Hence, under certain environmental conditions, they play a key role in microbial metabolism as the dominant electron donor or terminal electron acceptor [1,2,4,5]. These metabolisms are thought to be among the most ancient, having probably driven the carbon cycle in the early Life stage and catalyzed the deposition of massive sedimentary ore deposits known as banded iron formations [6,7]. Today, these microbial metabolisms still remain widespread and ecologically influential, controlling the mobilization, distribution and speciation of many
metals (e.g. Fe, Mn, Cr, Hg, Au, Mo, Co, Pd, As, Se, U, Te and V) [1,2,4,5,8,9]. Furthermore, the establishment of these metal redox cycles in specific environmental niches contribute greatly to other biotic redox cycles and geochemically relevant abiotic redox conversions.
Because of the importance of microorganisms to both ancient and modern biogeochemical cycles and their potential usefulness in several biotechnologies (e.g. microbial fuel cells and bioremediation of environments contaminated by toxic heavy metals), an increase in scientific interest to study these organisms and their metabolisms arose.
Microbial influence on the iron redox cycle. Iron is the most “ironic” of
the elements. It is the fourth most abundant element in the Earth’s crust, and after oxygen, the most abundant redox-active element capable of sustaining Life via iron-coupled redox reactions. On the other hand, at circumneutral pH, oxygen promotes the rapid oxidation of soluble ferrous iron to insoluble ferric iron oxides, leaving the vast majority of the planet’s environment with vanishingly low iron concentrations that limits the existence of Life. As a result, only in oxygen-limited environments, such as oxic/anoxic interfaces of sediments, is iron abundant enough that microorganisms can use it as an electron donor or acceptor to sustain growth [10-13].
The elemental cycle of iron comprises complex abiotic and microbiological interactions (Figure 1.1). First thought to be only an abiotic phenomenon, the discovery of microorganisms capable of oxidizing iron raised the hypothesis of biotic involvement in the iron redox cycle [10-13].
Figure 1.1. Iron biogeochemical redox cycle. Adapted from [11].
Under circumneutral pH conditions the biogeochemical cycling of iron comprises oxic and anoxic habitats where iron is either occurring in its oxidized Fe(III) or reduced Fe(II) redox state, as precipitated or dissolved species. In oxic environments the oxidation of Fe(II) by molecular oxygen is the predominant iron converting process. Aerobic iron-oxidizing microorganisms (e.g. Gallionella, Leptothrix, Syderoxydans and Mariprofundus genera) are therefore restricted to micro-aerobic environments where the chemical oxidation rates are sufficiently slow to allow microorganisms to successfully compete with abiotic iron oxidation [11,14-16]. Biotic Fe(II) oxidation at 50 μM O2 was shown to contribute only 20 % to the iron oxidation, though decreasing O2 concentration to 15 μM its contribution increased to more than 80 % [14]. At more anoxic conditions, iron oxidation is dominated by anaerobic phototrophic (e.g. Rhodobacter, Rhodomicrobium, Chlorobium, Rhodovulum,
Thiodictyon and Rhodopseudomonas genera) [16,17] and nitrate-reducing iron- oxidizing microorganisms (e.g. Ferroglobus, Acidovorax and Aquabacterium)
relevant at elevated nitrite concentrations and in low pH environments [20]. These organisms do not compete with each other since they inhabit different niches and rely on different energy sources (chemical and light energy) or different electron acceptors (O2, NO3–).
Under acidic conditions, Fe(II) is more stable and persists for a longer period of time in the environment even in the presence of O2. This allows aerobic acidophilic Fe(II)-oxidizing bacteria (e.g. Acidithiobacillus; Acidiferrobacter and Ferrovum genera) to compete with the abiotic oxidation of
Fe(II) by O2 [16,21].
In all cases, microorganisms capable of iron oxidation have to cope with the issue of encrustation due to the formation of insoluble Fe(III) species [22]. The sole exception are the acidophilic Fe(II)-oxidizing bacteria, since Fe(III) is soluble at low pH values.
Iron-oxidation is only one-side of the coin. To close the biogeochemical iron cycle, Fe(III), which at circumneutral pH is mostly trapped in the form of insoluble iron oxides, has to be reduced in order to provide Fe(II) for re- oxidation. This Fe(III) can be either reduced biologically through microorganisms [10,13,23] or chemically by hydrogen sulfide, which is a common end product of microbial sulfur and sulfate reduction [24]. Insoluble Fe(III) species are reduced mostly in anaerobic conditions either by anaerobes (e.g. Geobacter and Geothrix genera) [25-27] or by facultative anaerobes (e.g.
Shewanella genus) [28,29]. These dissimilatory iron reducing bacteria are able to
perform the biochemically challenging electron transfer to the extracellular insoluble Fe(III) oxides and produce soluble Fe(II). Although there are Fe(III)- reducing bacteria which can couple the reduction of Fe(III) to the oxidation of complex organic compounds, it has been suggested that fermentative
microorganisms break down these compounds and Fe(III)-reducing bacteria use these fermentative end products as carbon sources [30]. Both, Geobacter and
Shewanella have become model organisms to study the biochemical
mechanisms of iron reduction and extracellular electron transfer in general [23,31].
Soluble Fe(II) can diffuse once again to the oxic/anoxic interface where it becomes re-oxidized to Fe(III), which precipitates in the form of ferric iron minerals, re-starting this remarkably dynamic and complex biogeochemical cycle. It has been estimated that in sediments each iron atom goes through approximately 100 cycles of oxidation/reduction prior to permanent incorporation [24].