Cable bacteria with electric connection to oxygen attract flocks of diverse bacteria

Abstract

Cable bacteria are centimeter-long filamentous bacteria that conduct electrons via internal wires, thus coupling sulfide oxidation in deeper, anoxic sediment with oxygen reduction in surface sediment. This activity induces geochemical changes in the sediment, and other bacterial groups appear to benefit from the electrical connection to oxygen. Here, we report that diverse bacteria swim in a tight flock around the anoxic part of oxygen-respiring cable bacteria and disperse immediately when the connection to oxygen is disrupted (by cutting the cable bacteria with a laser). Raman microscopy shows that flocking bacteria are more oxidized when closer to the cable bacteria, but physical contact seems to be rare and brief, which suggests potential transfer of electrons via unidentified soluble intermediates. Metagenomic analysis indicates that most of the flocking bacteria appear to be aerobes, including organotrophs, sulfide oxidizers, and possibly iron oxidizers, which might transfer electrons to cable bacteria for respiration. The association and close interaction with such diverse partners might explain how oxygen via cable bacteria can affect microbial communities and processes far into anoxic environments.

Fig. 1. Documentation and main properties of bacterial flocks around cable bacteria.

A Flocking bacteria attracted to a cable bacterium filament (center) (Scale bar, 10 µm). B Counts of swimming bacteria at different distances to the cable bacterium filament (960,071 counts of 3211 flocking bacteria in 12 video frames, mean distance 17.42 µm. The means of the individual samples ranged from 4.96 to 24.58 µm. C Difference in mean swimming speed of bacterial cells relative to their distance to the cable bacterium filament. The shaded blue area corresponds to a distance within 20 µm of a cable bacterium, shaded green to more than 20 µm. Welch’s two-sample t-test (two-sided) shows that the swimming speed of cells is significantly different between these two distance groups (indicated by *); p-value = 2.2e⁻¹⁶ (N_samples = 11, N_cells = 2712). D Density plot of bacterial cell sizes from all samples (n = 12), showing that the majority of interacting cells is small. E Phase contrast images of the different cell morphologies found. Source data are provided as a Source Data file.

Fig. 2. Principle and example of results of the laser cut experiment (n = 9).

A Schematic representation. A cable bacterium connected to oxygen at the right side is cut near the oxic-anoxic interface using a laser microdissection microscope. B Result. Bacterial tracks on the suboxic part of a cable bacterium generated from a video before and after a cut. Red lines are tracks of swimming bacteria, and black lines and dots denote the position of the cable bacterium for every 50 frames. The cable bacterium moves more after the cut as if the filament begins its oxygen chemotaxis (Scale bar, 10 µm). Source data are provided as a Source Data file.

Fig. 3. Genome-based phylogeny and selected key features of putative cable bacteria-associated bacteria.

Data were derived from the annotation of metagenome-assembled genomes and from literature searches. EET, extracellular electron transfer. Source data are provided in Supplementary Datasets 1–3.

Fig. 4. Cytochromes in flocking bacteria are more oxidized when close to a cable bacterium.

A Schematic representation of the experiment. A flocking cell is captured and moved right next to a cable bacterium filament, measured by Raman microscopy, then moved ~50–100 µm away and measured again after ~3 s. B The change in normalized intensity of the 750 cm⁻¹ band for each individual cell when moved next to and away from the cable bacterium. The 750 cm⁻¹ band is indicative of cytochrome redox state, with high values for reduced and low values for oxidized cytochromes. Band intensities and, thus, cytochrome redox states are significantly different between the two positions (N_{native cells} = 5, p-value = 0.015, indicated by *; N_A.facilis = 8, p-value = 0.0387 indicated by **, two-sided t-test for dependent samples,); a.u., arbitrary units. Source data are provided as a Source Data file.