Figure 3.6 Phylogenetic tree of iron‐reducing bacteria and archaea isolated from marine sediments. The unrooted phylogenetic tree was adapted from Weber (2006) and was based on nearly full‐length 16S ribosomal DNA sequences compiled from the National Center for Biotechnology Information database. Sequences were aligned using Clustal Omega 1.2.4.1 and curated using Gblocks 0.91.1 (default settings) accessed from the website Phylogeny.fr (https://ngphylogeny.fr) (Lemonie et al. 2019) on October 22, 2019. The tree was constructed using phylogeny PhyML 3.0 using maximum likelihood bootstrap 100; substitution model HKY85 from the atgc‐montpellier.fr website (www.atgc‐montpellier.fr/phyml/) accessed on October 22, 2019. iTol interactive tree of Life V.5 (Letunic and Bork 2016) was used to generate the final tree.

Other than Geobacter and Shewanella, where the iron‐reducing pathway has been studied, a number of bacteria (and archaea) have been observed to be capable of reducing iron. However, neither their pathways of iron reduction are known, nor whether they are representative of their phylogenetic groups in terms of iron reduction. For example, Sinorhodobacter ferrireducens (Yang et al. 2013), a non‐phototrophic iron‐reducing bacterium from the genus Rhodobacter, and Desulfotalea arctica (Knoblauch et al. 1999), a psychrophilic sulfate‐reducing bacterium of the Class Deltaproteobacteria, have been isolated from marine sediments. They have been shown to reduce iron oxide in batch experiments but they have not yet been genetically characterized and their pathways of iron reduction remain unknown. We can nevertheless speculate whether representatives that are commonly found in shallow marine sediments use known metabolic pathways to reduce iron.

      Other than members of the Geobacteraceae, members of the SRB have yet to be genetically investigated to determine which genes are necessary for their iron reduction abilities, including potential extracellular electron transport mechanisms (Reyes et al. 2016). Moreover, molecular models that track the electron transport from oxidation of substrate to the reduction of iron are also needed for these organisms. Recently, the proteome of an SRB belonging to the Firmicutes, Desulfotomaculum reducens strain MI‐1, was studied in cultures with Fe‐oxide as the only electron acceptor, and a multiheme cytochrome was shown to be highly expressed under these conditions, hinting at the possibility of its involvement in iron reduction (Otwell et al. 2016).

      Overall, some over‐representation of iron reducers within the Deltaproterobacteria may result from a cultivation bias. In particular, sulfate reducers have been intensively cultivated under diverse anaerobic conditions, including ferruginous conditions. Nevertheless, based on the wide distribution of iron reducers among many groups in the phylogenetic tree, we may conclude also that the electron‐transporting machinery is widespread. While the pathways may not really be specific to iron as an electron acceptor, many microorganisms could modify their electron transport chains to take advantage of the electron potential difference and gain the maximum ATP. On the other hand, solid‐phase electron acceptors pose a serious challenge, requiring complex strategies and extracellular electron transport pathways. It is known that certain genes involved in extracellular electron transport pathways result from horizontal and vertical gene transfer (Holmes et al., 2016; Baker et al. 2022). Such systems may already be established in many microorganisms using other metabolic pathways, and their application to reduce iron would require only minor modifications. The observation that iron reduction is a widespread ability in the microbial tree of life highlights that these systems require further investigation and perhaps hold the key to a better understanding of the ecological role microbial communities play in natural environments, such as marine sediments.

3.5. SUMMARY AND CONCLUSIONS

      Microbial iron reduction may occur in sulfide‐free zones in marine sediments to the extent where organisms outcompete other organisms using other electron acceptors to oxidize the same organic carbon substrate. Specificity towards iron reduction arises from the ability of the pathway to maximize its energy yield. Even though iron reduction per se may be non‐specific, it requires an elaborate extracellular electron transport system or uptake system to access the solid phase iron. Strategies involve electron shuttles, siderophores, or direct contact via nanowires, pili, or connected cells forming a bacterial “cable”. Redox zonation in natural sediments probably involves organization with respect to long‐distance electron transport to access solid‐phase electron acceptors, depending on the availability of other, dissolved electron acceptors. Recent phylogenetic studies have revealed that zones of ongoing iron reduction are preferentially inhabited by phylogenetic groups that have members known to reduce iron, although these may not necessarily be the known model organisms Shewanella and Geobacter. More often versatiles are present, correlating with the redox zonation, in particular suboxic zones or sulphide‐free methanogenic zones. Future studies will not only require phylogenetic analysis but will also need to provide elucidation of the complex electron‐transport mechanisms and how they interact among different microbial groups within the community.

REFERENCES