Conservation of energetic pathways for electroautotrophy in the uncultivated candidate order Tenderiales

Abstract

Electromicrobiology can be used to understand extracellular electron uptake in previously undescribed chemolithotrophs. Enrichment and characterization of the uncultivated electroautotroph "Candidatus Tenderia electrophaga" using electromicrobiology led to the designation of the order Tenderiales. Representative Tenderiales metagenome assembled genomes (MAGs) have been identified in a number of environmental surveys, yet a comprehensive characterization of conserved genes for extracellular electron uptake has thus far not been conducted. Using comparative genomics we identified conserved orthologous genes within the Tenderiales and nearest neighbor orders important for extracellular electron uptake based on a previously proposed pathway from "Ca. Tenderia electrophaga". The Tenderiales contained a conserved cluster we designated uetABCDEFGHIJ, which encodes proteins containing features that would enable transport of extracellular electrons to cytoplasmic membrane bound energy transducing complexes such as two conserved cytochrome cbb3 oxidases. For example, UetJ is predicted to be an extracellular undecaheme c-type cytochrome that forms a heme wire. We also identified clusters of genes predicted to facilitate assembly and maturation of electron transport proteins, as well as cellular attachment to surfaces. Autotrophy among the Tenderiales is supported by the presence of carbon fixation and stress response pathways that could allow cellular growth by extracellular electron uptake. Key differences between the Tenderiales and other known neutrophilic iron oxidizers were revealed, including very few Cyc2 genes in the Tenderiales. Our results reveal a possible conserved pathway for extracellular electron uptake and suggests the Tenderiales have an distribution unlimited ecological role coupling metal or mineral redox chemistry and the carbon cycle in marine and brackish sediments. ImportanceElectromicrobiology enables enrichment and identification of chemolithotrophic bacteria capable of extracellular electron uptake to drive energy metabolism and CO2 fixation. The recently described order Tenderiales contains the uncultivated electroautotroph "Candidatus Tenderia electrophaga". The "Ca. Tenderia electrophaga" genome contains genes proposed to make up a previously undescribed extracellular electron uptake pathway. Here we use comparative genomics to show that this pathway is well conserved among Tenderiales spp. recovered by metagenome assembled genomes. This conservation extends to near neighbors of the Tenderiales, but not to other well-studied chemolithotrophs including iron and sulfur oxidizers. Our findings suggest that extracellular electron uptake may be pervasive among the Tenderiales and the geographic location from which metagenome assembled genomes were recovered offers clues to their natural ecological niche.