Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria

TLDR

Microbial consortia that exchange electrons are crucial for anaerobic organic matter processing, and while interspecies hydrogen transfer is common in laboratory cultures, natural aggregates often form multispecies consortia. Evolution of a Geobacter metallireducens–Geobacter sulfurreducens coculture on ethanol produced electrically conductive aggregates driven by a mutation that boosts a c‑type cytochrome, and mutants lacking hydrogen transfer formed aggregates even faster, indicating direct interspecies electron transfer.

Abstract

Microbial consortia that cooperatively exchange electrons play a key role in the anaerobic processing of organic matter. Interspecies hydrogen transfer is a well-documented strategy for electron exchange in dispersed laboratory cultures, but cooperative partners in natural environments often form multispecies aggregates. We found that laboratory evolution of a coculture of Geobacter metallireducens and Geobacter sulfurreducens metabolizing ethanol favored the formation of aggregates that were electrically conductive. Sequencing aggregate DNA revealed selection for a mutation that enhances the production of a c-type cytochrome involved in extracellular electron transfer and accelerates the formation of aggregates. Aggregate formation was also much faster in mutants that were deficient in interspecies hydrogen transfer, further suggesting direct interspecies electron transfer.