The electrifying physiology of Geobacter bacteria, 30 years on.

ABSTRACT

The family Geobacteraceae, with its only valid genus Geobacter, comprises deltaproteobacteria ubiquitous in soil, sediments, and subsurface environments where metal reduction is an active process. Research for almost three decades has provided novel insights into environmental processes and biogeochemical reactions not previously known to be carried out by microorganisms. At the heart of the environmental roles played by Geobacter bacteria is their ability to integrate redox pathways and regulatory checkpoints that maximize growth efficiency with electron donors derived from the decomposition of organic matter while respiring metal oxides, particularly the often abundant oxides of ferric iron. This metabolic specialization is complemented by versatile metabolic reactions, respiratory chains, and sensory networks that allow specific members to adaptively respond to environmental cues to integrate organic and inorganic contaminants in their oxidative and reductive metabolism, respectively. Thus, Geobacteraceae are important members of the microbial communities that degrade hydrocarbon contaminants under iron-reducing conditions and that contribute, directly or indirectly, to the reduction of radionuclides, toxic metals, and oxidized species of nitrogen. Their ability to produce conductive pili as nanowires for discharging respiratory electrons to solid-phase electron acceptors and radionuclides, or for wiring cells in current-harvesting biofilms highlights the unique physiological traits that make these organisms attractive biological platforms for bioremediation, bioenergy, and bioelectronics application. Here we review some of the most notable physiological features described in Geobacter species since the first model representatives were recovered in pure culture. We provide a historical account of the environmental research that has set the foundation for numerous physiological studies and the laboratory tools that had provided novel insights into the role of Geobacter in the functioning of microbial communities from pristine and contaminated environments. We pay particular attention to latest research, both basic and applied, that has served to expand the field into new directions and to advance interdisciplinary knowledge. The electrifying physiology of Geobacter, it seems, is alive and well 30 years on.