Poster Presentation Australian Microbial Ecology 2019

Potential Mechanism of Subsurface Life Fuelled by Extracellular Electron Uptake (#123)

Xiao Deng 1 , Naoshi Dohmae 2 , Kenneth H Nealson 3 , Kazuhito Hashimoto 4 , Akihiro Okamoto 4
  1. CSIRO, Floreat, WA, Australia
  2. RIKEN Centre for Sustainable Resource Science, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
  3. University of Southern California, California, USA
  4. National Institute for Materials Science, 1-1 Namiki, Tsukuba, Ibaraki, Japan

Subsurface microbes constitute nearly half of total microbial cells on Earth and represent important bioresources1, yet have remained mostly uncultivable due to their unknown energy sources. Identifying energy sources in the subsurface is therefore crucial for establishing novel cultivation methods to grow and isolate subsurface microbes. So far, abiotic hydrogen (H­2) generated in water radiolysis and water-rock reactions has been considered as the main energy source in subsurface environments. However, due to its low concentration (nM – μM) it is greatly outcompeted by that of electron acceptors (mM), and thus remains questionable to be sufficient for supporting the vast subsurface biosphere2. Here, we show that multi-heme cytochrome proteins, which enable cells to extract electrons from electrodes coupled with energy acquisition, are present in various sedimentary microbes. By performing genome sequencing and electrochemical analysis with a sulfate-reducing bacterium, Desulfovibrio ferrophilus IS5, which was isolated from marine sediments using iron coupons as the sole energy source3, we identified two gene clusters encoding seven multi-heme cytochromes with extracellular and periplasmic localizations and two β-propeller proteins which potentially enable interactions between extracellular and periplasmic cytochromes forming a transmembrane electron-uptake conduit. Cells under organic starvation condition overexpress surface cytochromes, produce segmented nanowire structures covered by cytochromes, and become capable of electron uptake from electrodes. Whole-cell electrochemistry identifies the onset of electron-uptake potential at −0.3 V versus standard hydrogen electrode, which is very close to the redox potential of nicotinamide adenine dinucleotide [NAD(P)+/NAD(P)H = −0.32 V], a ubiquitous energy carrier in cell respiration, indicating that electron uptake provides cells with a sufficient but minimum amount of energy for survival under organic-scarce conditions. Furthermore, identical genes encoding cytochromes are present in diverse sedimentary microbes across three phyla, Proteobacteria, Thermodesulbacteria, and Aquificae, suggesting that electron uptake widely fuels subsurface biosphere.

  1. S. D’Hondt, et al., PNAS, 2009, 106, 11651.
  2. R. T. Anderson, et al., Sci., 1998, 281, 976.
  3. H. T. Dinh, et al., Nat., 2004, 427, 829.