AUTHOR=Gavrilov Sergey N. , Zavarzina Daria G. , Elizarov Ivan M. , Tikhonova Tamara V. , Dergousova Natalia I. , Popov Vladimir O. , Lloyd Jonathan R. , Knight David , El-Naggar Mohamed Y. , Pirbadian Sahand , Leung Kar Man , Robb Frank T. , Zakhartsev Maksim V. , Bretschger Orianna , Bonch-Osmolovskaya Elizaveta A. 

TITLE=Novel Extracellular Electron Transfer Channels in a Gram-Positive Thermophilic Bacterium

JOURNAL=Frontiers in Microbiology

VOLUME=11

YEAR=2021

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2020.597818

DOI=10.3389/fmicb.2020.597818

ISSN=1664-302X

ABSTRACT=<p>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 <italic>Carboxydothermus ferrireducens</italic> 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 <italic>C. ferrireducens</italic>. The internal structure of micron-scale biogenic magnetite crystals is reported for the first time. Genome analysis and expression profiling revealed three constitutive <italic>c</italic>-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.</p>