Succession of cable bacteria and electric currents in marine sediment

Abstract

Filamentous Desulfobulbaceae have been reported to conduct electrons over centimetre-long distances, thereby coupling oxygen reduction at the surface of marine sediment to sulphide oxidation in sub-surface layers. To understand how these 'cable bacteria' establish and sustain electric conductivity, we followed a population for 53 days after exposing sulphidic sediment with initially no detectable filaments to oxygen. After 10 days, cable bacteria and electric currents were established throughout the top 15 mm of the sediment, and after 21 days the filament density peaked with a total length of 2 km cm(-2). Cells elongated and divided at all depths with doubling times over the first 10 days of <20 h. Active, oriented movement must have occurred to explain the separation of O2 and H2S by 15 mm. Filament diameters varied from 0.4-1.7 μm, with a general increase over time and depth, and yet they shared 16S rRNA sequence identity of >98%. Comparison of the increase in biovolume and electric current density suggested high cellular growth efficiency. While the vertical expansion of filaments continued over time and reached 30 mm, the electric current density and biomass declined after 13 and 21 days, respectively. This might reflect a breakdown of short filaments as their solid sulphide sources became depleted in the top layers of the anoxic zone. In conclusion, cable bacteria combine rapid and efficient growth with oriented movement to establish and exploit the spatially separated half-reactions of sulphide oxidation and oxygen consumption.

Figure 1

(a) Depth distribution of oxygen (red), sulphide (green), cable bacteria density (grey bars) and cable bacteria diameter (black line) over time during sediment incubations. Time of incubation is given in days (t0–t53). Mean values (±s.d.; n=3) are shown for triplicate chemical profiles. Mean values of diameters (±s.d.; n=3–15) are weighted by the square and on the basis of all analysed cables for each time point and depth. (b) Close-up of the oxic zone with microprofiles of oxygen (red) and pH (black); mean±s.d. (n=3). In addition, single pH profiles (grey) are shown for control cores, from which cable bacteria growth was excluded by polycarbonate filters.

Figure 2

Diffusive O₂ uptake (DOU) (black), cathodic oxygen consumption (COC) as mean of triplicate cores (blue) and depth integrated cable bacteria density detected by FISH (red).

Figure 3

(A) Cable bacteria in incubated marine sediment targeted by the DSB706 probe, showing different phenotypes of cable bacteria with (a) 0.7 μm (t21) and (b) 1.2 μm (t21) diameters. (B) Different stages of cell division were detected in cells along the multicellular cables (1) daughter chromosomes located side by side, (2) cell division is initiated in the middle, (3) daughter chromosomes are located in the middle of the daughter cells. Scale bars, 10 μm.

Figure 4

Phylogenetic affiliation by maximum-likelihood of 16S rRNA sequences obtained in this study. Bootstrap support (1000 replicates) >50% is displayed at the nodes. Sequences obtained from single cable bacteria are shown in blue with their filament diameter indicated, sequences from bulk sediment rRNA are shown in red with the day of sampling indicated. Clone identifier and EMBL accession numbers are given in parentheses. The tree is rooted to Escherichia coli and Vibrio fischeri. The bar represents 10% estimated sequence difference.