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Electron exchange between microorganisms and conductive minerals

Goldshmidt conference, 13 May 2014, Sacramento. Electron exchange between microorganisms and conductive minerals. Souichiro Kato. National Institute of Advanced Industrial Science & Technology, Japan Univ . of Tokyo, Japan Hokkaido Univ ., Japan. (semi)conductive iron minerals.

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Electron exchange between microorganisms and conductive minerals

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  1. Goldshmidt conference, 13 May 2014, Sacramento Electron exchange between microorganisms and conductive minerals Souichiro Kato National Institute of Advanced Industrial Science & Technology, Japan Univ. of Tokyo, Japan HokkaidoUniv., Japan

  2. (semi)conductive iron minerals ◆Iron minerals（Iron oxides/sulfides） 1. Abundantly exist on the Earth 2. Diverse electrochemical properties * Magnetite (Fe3O4): Conductive * Hematite (α-Fe2O3), Pyrite (FeS): Semi-conductive Electric current generation across a black smoker chimney Nakamura R. et al. (2010) Angew. Chem. Int. Ed. Chimney rocks (chalcopyrite/pyrite) show conductivity

  3. (semi)conductive iron minerals ◆Iron minerals（Iron oxides/sulfides） 1. Abundantly exist on the Earth 2. Diverse electrochemical properties * Magnetite (Fe3O4): Conductive * Hematite (α-Fe2O3), Pyrite (FeS): Semi-conductive 3. Microbes often generate (semi)conductive iron minerals BanfieldJS. (2000) Science,etc. 4. Some microbes uptake (or inject) electrons from (or to) conductive minerals Nakamura R. et al. (2009) Angew. Chem. Int. Ed. Kato S. et al. (2011) Environ. Microbiol.

  4. Electricity consuming/generating microbes Electricity Consumers Electricity Generators Current Current ATP Organics e- ATP CO2 NO3- e- Cathode N2 Anode Electric current (free electrons in conductors) as an electron donor Electric current as an electron acceptor

  5. Extracellular electron transfer Extracellular electron transfer Oxygen respiration Organics Organics e- e- CO2 H+ CO2 H+ NADH NADH NAD+ Conductive materials NAD+ H+ Inside Outside e- Redox proteins (c-type cytochromes) H+ H2O e- O2 Outer membrane Inner membrane

  6. Today’s topics Electric syntrophy A novel way of microbial metabolism, in which conductive minerals work as electric wires between two microorganisms 1. Model experiment 2. Enhancement of microbial methane generation

  7. Model experiment Geobactersulfurreducens ○ current generation & acetate oxidation Thiobacillusdenitrificans ○ current consumption & nitrate reduction Potential : +0.4V Electron donor : acetate Potential : -0.4V Electron acceptor : nitrate 20 0 15 Geobacter Geobacter 10 Current density (μA/cm2) Current density (μA/cm2) -5 Thiobacillus 5 Thiobacillus 0 -10 0 10 20 30 40 0 10 20 30 40 Kato S. PNAS. 2012 Time (hr) Time (hr)

  8. Electrochemical analysis Linear sweep voltammetry(1mV/s) Available potential range (Thiobacillus) 40 Geobacter Acetate -0.4 20 Onset CO2 e- -0.2 0 Current (μA) Onset e- EºpH7 (V vs. SHE) -20 0 Thiobacillus NO3- -40 0.2 -0.4 -0.2 0 0.2 NH4+ Potential (V vs. SHE) Available potential range (Geobacter) 0.4 Kato S. et al.,PNAS. 2012

  9. Electric syntrophy with magnetite Kato S. et al.,PNAS. 2012

  10. Electric syntrophy with magnetite + Magnetite Kato S. et al.,PNAS. 2012

  11. Electric syntrophy with magnetite Kato S. et al.,PNAS. 2012 38 33

  12. Electric syntrophy with graphite Graphite nano-particle （Conductive） Al2O3nano-particles (insulative) NO3- NO3- Mixed-culture Acetate Acetate Geobacter Thiobacillus NH4+ NH4+ Kato S. PNAS. 2012

  13. Syntrophic methanogenesis Hydrogen-syntrophy • H2 diffusion limited • Energy gap →　so slow reaction Methanogenic archaea Organics oxidizer Electric syntrophy • Electric current base • No energy gap →　faster reaction ??

  14. Stimulation of methanogenesis Methanogenesis from ethanol by enrichment cultures No minerals ＋Hematite（semi-conductive） ＋Magnetite（conductive） ＋Ferrihydrite（insulative） Kato S. et al.,Environ. Microbiol. 2012

  15. Enriched microbes Non-Fe Hematite Magnetite Ferrihydrite ◆ Methanogens　：　Dominate in all conditions ◆ Geobacter: Dominate when conductive minerals exist Kato S. et al.,Environ. Microbiol. 2012

  16. Growth of Geobacter +BES（inhibitor of methanogenesis） Geobacter　：　Grew when conductive minerals exist Addition of BES　→　Inhibit growth of Geobacter Geobacterdepends on methanogenic archaea Kato S. et al.,Environ. Microbiol. 2012

  17. Summary Microbial extracellular electron transfer A special form of microbial energy metabolism Conductive iron minerals are their “energy sources” Electricsyntrophy Electriccurrentsmediate interspecies electron (energy) transfer Iron oxides (e.g., magnetite) work as “electric wire” Electric interactions between microorganisms and minerals may contribute greatly to diverse biogeochemical reactions

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