Extracellular Electron Transfer to Fe(III) Oxides by the Hyperthermophilic Archaeon Geoglobus ahangari via a Direct Contact Mechanism

Abstract

The microbial reduction of Fe(III) plays an important role in the geochemistry of hydrothermal systems, yet it is poorly understood at the mechanistic level. Here we show that the obligate Fe(III)-reducing archaeon Geoglobus ahangari uses a direct-contact mechanism for the reduction of Fe(III) oxides to magnetite at 85°C. Alleviating the need to directly contact the mineral with the addition of a chelator or the electron shuttle anthraquinone-2,6-disulfonate (AQDS) stimulated Fe(III) reduction. In contrast, entrapment of the oxides within alginate beads to prevent cell contact with the electron acceptor prevented Fe(III) reduction and cell growth unless AQDS was provided. Furthermore, filtered culture supernatant fluids had no effect on Fe(III) reduction, ruling out the secretion of an endogenous mediator too large to permeate the alginate beads. Consistent with a direct contact mechanism, electron micrographs showed cells in intimate association with the Fe(III) mineral particles, which once dissolved revealed abundant curled appendages. The cells also produced several heme-containing proteins. Some of them were detected among proteins sheared from the cell's outer surface and were required for the reduction of insoluble Fe(III) oxides but not for the reduction of the soluble electron acceptor Fe(III) citrate. The results thus support a mechanism in which the cells directly attach and transfer electrons to the Fe(III) oxides using redox-active proteins exposed on the cell surface. This strategy confers on G. ahangari a competitive advantage for accessing and reducing Fe(III) oxides under the extreme physical and chemical conditions of hot ecosystems.

The Geoglobus acetivorans Genome: Fe(III) Reduction, Acetate Utilization, Autotrophic Growth, and Degradation of Aromatic Compounds in a Hyperthermophilic Archaeon

“…1B), are more likely to serve for adhesion than for twitching motility. The production of two distinct types of filaments, flagella and curled pilus-like thin appendages, was also reported for G. ahangari (27). Interestingly, cells simultaneously producing both flagellum-and pilus-like structures have not been identified in G. acetivorans cultures, suggesting that these processes are strictly regulated in the organism.…”

“…Aciduliprofundum boonei" are also available; however, there are no published data on the genomic determinants of Fe(III) reduction in these organisms (26). It was recently shown that the obligate Fe(III)-reducing hyperthermophilic archaeon Geoglobus ahangari uses a direct-contact mechanism for the reduction of Fe(III) oxides to magnetite (27), but genomic determinants of these processes are unknown.…”

Mechanisms Involved in Fe(III) Respiration by the Hyperthermophilic Archaeon Ferroglobus placidus

“…Direct contact with Fe(III) oxides and reliance on electron-shuttling or chelating compounds for reduction of Fe(III) are traits seen in both bacterial and archaeal species (1,(11)(12)(13)(14)(15)(16)61). In fact, the majority of electron transport proteins that transcriptomic and proteomic studies showed to be important for reduction of insoluble Fe(III) oxide by F. placidus have homologues in mesophilic Fe(III)-reducing bacteria.…”

“…The involvement of c-type cytochrome proteins in Fe(III) reduction also seems to vary among hyperthermophilic archaea. While c-type cytochrome proteins appear to be involved in electron transfer to Fe(III) by G. ahangari (14), they are not required for Fe(III) respiration by Pyrobaculum species (13,16). In this study, Fe(III) respiration was examined in Ferroglobus placidus, a hyperthermophilic archaeon that was isolated from hydrocarbon-and iron-rich sediments associated with a hydrothermal system in Vulcano Island (17,18).…”

“…For example, Pyrobaculum aerophilum seems to release an electron-shuttling compound(s) that transfers electrons from the cell surface to the surface of Fe(III) oxides not in direct contact with the cells (13), while Geoglobus ahangari and Geoglobus acetivorans require direct contact with Fe(III) hydroxides in the absence of chelated iron or reduced electron shuttles (14,15). The involvement of c-type cytochrome proteins in Fe(III) reduction also seems to vary among hyperthermophilic archaea.…”