Happy together: microbial communities that hook up to swap electrons

Abstract

The discovery of direct interspecies electron transfer (DIET) and cable bacteria has demonstrated that microbial cells can exchange electrons over long distances (μm-cm) through electrical connections. For example, in the presence of cable bacteria electrons are rapidly transported over centimeter distances, coupling the oxidation of reduced sulfur compounds in anoxic sediments to oxygen reduction in overlying surficial sediments. Bacteria and archaea wired for DIET are found in anaerobic methane-producing and methane-consuming communities. Electrical connections between gut microbes and host cells have also been proposed. Iterative environmental and defined culture studies on methanogenic communities revealed the importance of electrically conductive pili and c-type cytochromes in natural electrical grids, and demonstrated that conductive carbon materials and magnetite can substitute for these biological connectors to facilitate DIET. This understanding has led to strategies to enhance and stabilize anaerobic digestion. Key unknowns warranting further investigation include elucidation of the archaeal electrical connections facilitating DIET-based methane production and consumption; and the mechanisms for long-range electron transfer through cable bacteria. A better understanding of mechanisms for cell-to-cell electron transfer could facilitate the hunt for additional electrically connected microbial communities with omics approaches and could advance spin-off applications such as the development of sustainable bioelectronics materials and bioelectrochemical technologies.

Figure 1

Model for long-range electron transport through the interior of cable bacteria with proposed reactions and relevant references. Lightning bolts depict the direction of electron flow.

Figure 2

Model for electron exchange between Desulfovibrio vulgaris and Clostridium acetobutylicum proposed in Benomar et al., 2015. An electron shuttle, such as ferrodoxin, provides interspecies electron exchange by moving between the two species through an intercellular connection.

Figure 3

Model for direct interspecies electron transfer in consortium of ANME-2 (green) and syntrophic sulfate-reducing partner (pink) anaerobically oxidizing methane with the reduction of sulfate. Cytochrome (hexagons, diamonds and crosses)-based electron transfer proposed for adjacent cells (lightning bolts) and longer percolation path (yellow line) proposed for electron transfer to non-adjacent cells.

Figure 4

Model for direct interspecies electron transfer between Geobacter and Methanosaeta species. The gray tube illustrates the proposed metallic-like mechanism for conduction along the length of the e-pili via delocalized electrons associated with tightly packed aromatic amino acids.

Figure 5

Model for electron exchange between Geobacter and Methanosarcina species mediated by carbon cloth. Lightning bolts depict electron transfer from Geobacter (red rods) through the cloth and to Methanosarcina (blue coccoids).