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Microbial interspecies electron transfer via electric currents through conductive minerals
Edited by James M. Tiedje, Michigan State University, East Lansing, MI, and approved May 03, 2012 (received for review October 27, 2011)

Abstract
In anaerobic biota, reducing equivalents (electrons) are transferred between different species of microbes [interspecies electron transfer (IET)], establishing the basis of cooperative behaviors and community functions. IET mechanisms described so far are based on diffusion of redox chemical species and/or direct contact in cell aggregates. Here, we show another possibility that IET also occurs via electric currents through natural conductive minerals. Our investigation revealed that electrically conductive magnetite nanoparticles facilitated IET from Geobacter sulfurreducens to Thiobacillus denitrificans, accomplishing acetate oxidation coupled to nitrate reduction. This two-species cooperative catabolism also occurred, albeit one order of magnitude slower, in the presence of Fe ions that worked as diffusive redox species. Semiconductive and insulating iron-oxide nanoparticles did not accelerate the cooperative catabolism. Our results suggest that microbes use conductive mineral particles as conduits of electrons, resulting in efficient IET and cooperative catabolism. Furthermore, such natural mineral conduits are considered to provide ecological advantages for users, because their investments in IET can be reduced. Given that conductive minerals are ubiquitously and abundantly present in nature, electric interactions between microbes and conductive minerals may contribute greatly to the coupling of biogeochemical reactions.
Footnotes
↵1Present address: Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Sapporo 062-8517, Japan.
- ↵2To whom correspondence may be addressed. E-mail: hashimoto{at}light.t.u-tokyo.ac.jp or kazuyaw{at}toyaku.ac.jp.
Author contributions: S.K., K.H., and K.W. designed research; S.K. performed research; S.K. and K.W. analyzed data; and S.K. and K.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1117592109/-/DCSupplemental.