Summary Cable bacteria (CB) are Desulfobulbaceae that couple sulphide oxidation to oxygen reduction over centimetre distances by mediating electric currents. Recently, it was suggested that the CB clade is composed of two genera, Ca. Electronema and Ca. Electrothrix, with distinct freshwater and marine habitats respectively. However, only a few studies have reported CB from freshwater sediment, making this distinction uncertain. Here, we report novel data to show that salinity is a controlling factor for the diversity and the species composition within CB populations. CB sampled from a freshwater site (salinity 0.3) grouped into Ca. Electronema and could not grow under brackish conditions (salinity 21), whereas CB from a brackish site (salinity 21) grouped into Ca. Electrothrix and decreased by 93% in activity under freshwater conditions. On a regional scale (Baltic Sea), salinity significantly influenced species richness and composition. However, other environmental factors, such as temperature and quantity and quality of organic matter were also important to explain the observed variation. A global survey of 16S rRNA gene amplicon sequencing revealed that the two genera did not co‐occur likely because of competitive exclusion and identified a possible third genus.

Cable bacteria are filamentous Desulfobulbaceae that split the energy-conserving reaction of sulphide oxidation into two half reactions occurring in distinct cells. Cable bacteria can use nitrate, but the reduction pathway is unknown, making it difficult to assess their direct impact on the N-cycle. Here we show that the freshwater cable bacterium Ca. Electronema sp. GS performs dissimilatory nitrate reduction to ammonium (DNRA). 15 NO 3 --amended sediment with Ca. Electronema sp. GS showed higher rates of DNRA and nitrite production than sediment without Ca. Electronema sp. GS. Electron flux from sulphide oxidation, inferred from electric potential measurements, matched the electron flux needed to drive cable bacteria-mediated nitrate reduction. Ca. Electronema sp. GS expressed a complete nap operon for periplasmic nitrate reduction to nitrite, and genes encoding a periplasmic multiheme cytochrome (pMHC), homolog to a pMHC that can catalyse nitrite reduction to ammonium in Ca. Maribeggiatoa. Phylogenetic analysis suggests that the capacity for DNRA was acquired in multiple events through horizontal gene transfer from different organisms, before cable bacteria split into different salinity niches. The architecture of the nitrate reduction system suggests absence of energy conservation through oxidative phosphorylation,indicating that cable bacteria primarily conserve energy through the half reaction of sulfide oxidation..

Cable bacteria are filamentous Desulfobulbaceae that split the energy-conserving reaction of sulphide oxidation into two half reactions occurring in distinct cells. Cable bacteria can use nitrate, but the reduction pathway is unknown, making it difficult to assess their direct impact on the N-cycle. Here we show that the freshwater cable bacterium Ca. Electronema sp. GS performs dissimilatory nitrate reduction to ammonium (DNRA). 15NO3−-amended sediment with Ca. Electronema sp. GS showed higher rates of DNRA and nitrite production than sediment without Ca. Electronema sp. GS. Electron flux from sulphide oxidation, inferred from electric potential measurements, matched the electron flux needed to drive cable bacteria-mediated nitrate reduction. Ca. Electronema sp. GS expressed a complete nap operon for periplasmic nitrate reduction to nitrite, and genes encoding a periplasmic multiheme cytochrome (pMHC), homolog to a pMHC that can catalyse nitrite reduction to ammonium in Ca. Maribeggiatoa. Phylogenetic analysis suggests that the capacity for DNRA was acquired in multiple events through horizontal gene transfer from different organisms, before cable bacteria split into different salinity niches. The architecture of the nitrate reduction system suggests absence of energy conservation through oxidative phosphorylation, indicating that cable bacteria primarily conserve energy through the half reaction of sulfide oxidation.