Abstract
Biogenic transformation of Fe minerals, associated with extracellular electron transfer (EET), allows microorganisms to exploit high-potential refractory electron acceptors for energy generation. EET-capable thermophiles are dominated by hyperthermophilic archaea and Gram-positive bacteria. Information on their EET pathways is sparse. Here, we describe EET channels in the thermophilic Gram-positive bacterium Carboxydothermus ferrireducens that drive exoelectrogenesis and rapid conversion of amorphous mineral ferrihydrite to large magnetite crystals. Microscopic studies indicated biocontrolled formation of unusual formicary-like ultrastructure of the magnetite crystals and revealed active colonization of anodes in bioelectrochemical systems (BESs) by C. ferrireducens. The internal structure of micron-scale biogenic magnetite crystals is reported for the first time. Genome analysis and expression profiling revealed three constitutive c-type multiheme cytochromes involved in electron exchange with ferrihydrite or an anode, sharing insignificant homology with previously described EET-related cytochromes thus representing novel determinants of EET. Our studies identify these cytochromes as extracellular and reveal potentially novel mechanisms of cell-to-mineral interactions in thermal environments.
Highlights
Extracellular electron transfer (EET) is a unique energy conservation mechanism of prokaryotic organisms that allows them to exploit a wide variety of redox-active minerals for energy generation and to maintain direct interspecies electron transfer in complex sedimentary milieus (Shi et al, 2016)
We describe several novel secreted multiheme cytochromes, fairly distantly related to previously reported determinants of EET, and provide evidence for their metabolic significance and differential involvement in electron transfer chains (ETCs) to different insoluble electron acceptors, Fe(III) oxide ferrihydrite, and the anodes of bioelectrochemical systems (BESs)
Growth of C. ferrireducens with ferrihydrite as the only electron acceptor is accompanied by the formation of biogenic cellmagnetite conglomerates (Gavrilov et al, 2012)
Summary
Extracellular electron transfer (EET) is a unique energy conservation mechanism of prokaryotic organisms that allows them to exploit a wide variety of redox-active minerals for energy generation and to maintain direct interspecies electron transfer in complex sedimentary milieus (Shi et al, 2016). Most studies of electron exchange between microbial cells and insoluble electron acceptors are based on the data obtained for diderm Gram-negative Fe(III) reducing microorganisms. Extracellular electron transfer processes drive important biogeochemical transformations in thermal sediments where insoluble Fe(III) compounds are abundant electron acceptors that can energize microbial life adapted to high temperature growth and survival (Kashefi et al, 2002). Thermophilic dissimilatory metal-reducers are dominated by monoderm prokaryotes (Firmicutes and hyperthermophilic Archaea), which represent many deep phylogenetic lineages (see Lusk, 2019 and the references therein). Their monolayer cell envelope obviates the need for soluble diffusible periplasmic electron shuttles and short-circuits their respiratory electron transport chains for access to such insoluble electron acceptors as Fe(III) or Mn(VI) oxides, ferruginous silicates, etc
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