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

Science  03 Dec 2010:
Vol. 330, Issue 6009, pp. 1413-1415
DOI: 10.1126/science.1196526

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Syntrophic bacteria live on the metabolic by-products of a partner species. The exchange of the by-products accompanies a flow of electrons in the opposite direction that helps some species grow in conditions that would otherwise be unfavorable. In mixed anaerobic cultures of two related Geobacter species, Summers et al. (p. 1413) observed that one species evolved to promote the transfer of electrons directly to the other, in large aggregated cell clusters, without coupling to common anaerobic by-products such as hydrogen or formate. Selection pressures in nine parallel populations all resulted in a point mutation that truncated a protein involved in the production of small hairlike projections involved in intercellular communication—pili—and indirectly increased the expression of a c-type multiheme cytochrome responsible for extracellular electron transfer. The evolved aggregates were conductive, suggesting that the direct exchange of electrons between partner species is a possible alternative route to anaerobic syntrophy rather than interspecies hydrogen transfer; indeed, deleting a gene that encodes a hydrogenase involved in hydrogen transfer conferred a growth advantage in the cocultures.

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.

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