Extracellular electron transfer genes expressed by candidate flocking bacteria in cable bacteria sediment

Abstract

Cable bacteria, filamentous sulfide oxidizers that live in sediments, are at times associated with large flocks of swimming bacteria. It has been proposed that these flocks of bacteria transport electrons extracellularly to cable bacteria via an electron shuttle intermediate, but the identity and activity of these bacteria in freshwater sediment remains mostly uninvestigated. We coupled metagenomics and metatranscriptomics to 16S rRNA amplicon-based correlations with cable bacteria from two time series experiments up to 155 days. We identified bacteria expressing genes for extracellular electron transfer and motility, including synthesis genes for potential extracellular electron shuttles: phenazines and flavins. Of the 85 high quality MAGs (Metagenome Assembled Genomes >90% complete and <5% contaminated), 56 had genes encoding flagellar proteins, and of these 22 had genes encoding extracellular electron transport proteins. The candidate flockers constituted 21.4% of all MAGs and 42.1% of the proposed flocking bacteria expressed extracellular electron transfer genes. The proposed flockers belonged to a large variety of taxonomic groups: 18 genera spread across 9 phyla. Our data suggest that electric relationships in freshwater sediments between cable bacteria and other microbes likely help to generate and/or sustain cryptic element cycling and ‘deep oxygen breathing’, affecting more element cycles than sulfur, like metal– and in particular iron– and carbon cycles.