From an extremophilic community to an electroautotrophic production strain: identifying a novel Knallgas bacterium as cathodic biofilm biocatalyst

• Published in: The ISME Journal 2020-05, Vol.14 (5), p.1125-1140
• Main Authors: Reiner, Johannes Eberhard, Geiger, Katharina, Hackbarth, Max, Fink, Marielle, Lapp, Christian Jonas, Jung, Tobias, Dötsch, Andreas, Hügler, Michael, Wagner, Michael, Hille-Reichel, Andrea, Wilcke, Wolfgang, Kerzenmacher, Sven, Horn, Harald, Gescher, Johannes
• Format: Article
• Language: English
• Subjects: 14/28; 14/32; 38/39; 45/23; 45/91; 631/326/2522; 631/326/46; 631/337/2019; Autotrophic Processes; Bacillales - physiology; Bacteria; Bacteria - metabolism; Biocatalysts; Biofilms; Biofilms - growth & development; Biomedical and Life Sciences; Carbon dioxide; Carbon Dioxide - metabolism; Carbon dioxide fixation; Cathodes; Cell culture; Ecology; Electrodes; Evolutionary Biology; Extremophiles - metabolism; Extremophiles - physiology; Gene expression; Hydrogenase - metabolism; Life Sciences; Metagenomics; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Microorganisms; Optical Coherence Tomography; Polyhydroxybutyrate; Polyhydroxybutyric acid; Pure culture; Renewable energy sources; Sulfur; Sulfur cycle
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-020-0595-5

Coupling microbial electrosynthesis to renewable energy sources can provide a promising future technology for carbon dioxide conversion. However, this technology suffers from a limited number of suitable biocatalysts, resulting in a narrow product range. Here, we present the characterization of the first thermoacidophilic electroautotrophic community using chronoamperometric, metagenomic, and 13 C-labeling analyses. The cathodic biofilm showed current consumption of up to −80 µA cm −2 over a period of 90 days (−350 mV vs. SHE). Metagenomic analyses identified members of the genera Moorella , Desulfofundulus , Thermodesulfitimonas , Sulfolobus , and Acidianus as potential primary producers of the biofilm, potentially thriving via an interspecies sulfur cycle. Hydrogenases seem to be key for cathodic electron uptake. An isolation campaign led to a pure culture of a Knallgas bacterium from this community. Growth of this organism on cathodes led to increasing reductive currents over time. Transcriptomic analyses revealed a distinct gene expression profile of cells grown at a cathode. Moreover, pressurizable flow cells combined with optical coherence tomography allowed an in situ observation of cathodic biofilm growth. Autotrophic growth was confirmed via isotope analysis. As a natural polyhydroxybutyrate (PHB) producer, this novel species, Kyrpidia spormannii , coupled the production of PHB to CO 2 fixation on cathode surfaces.