Novel Extracellular Electron Transfer Channels in a Gram-Positive Thermophilic Bacterium
Sergey N. Gavrilov, Д. Г. Заварзина, Ivan M. Elizarov, Т.В. Тихонова, Н. И. Дергоусова, Vladimir O. Popov, Jonathan R. Lloyd, David Knight, Mohamed Y. El‐Naggar, Sahand Pirbadian, Kar Man Leung, Frank T. Robb, Maksim Zakhartsev, Orianna Bretschger, E. A. Bonch-Osmolovskaya
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.