Worm tubes as conduits for the electrogenic microbial grid in marine sediments

Abstract

Electrogenic cable bacteria can couple spatially separated redox reaction zones in marine sediments using multicellular filaments as electron conductors. Reported as generally absent from disturbed sediments, we have found subsurface cable aggregations associated with tubes of the parchment worm Chaetopterus variopedatus in otherwise intensely bioturbated deposits. Cable bacteria tap into tubes, which act as oxygenated conduits, creating a three-dimensional conducting network extending decimeters into sulfidic deposits. By elevating pH, promoting Mn, Fe-oxide precipitation in tube linings, and depleting S around tubes, they enhance tube preservation and favorable biogeochemical conditions within the tube. The presence of disseminated filaments a few cells in length away from oxygenated interfaces and the reported ability of cable bacteria to use a range of redox reaction couples suggest that these microbes are ubiquitous facultative opportunists and that long filaments are an end-member morphological adaptation to relatively stable redox domains.

Fig. 1. Example Chaetopterus tube and tube-associated cable bacteria.

(A) Example Chaetopterus tube (small), with agglutinated mud layer exhumed from box core and suspended in seawater (GPB; May 2018). Dotted scale line is located along sediment-water interface. (B) Cable bacteria filament in 1-mm layer scrapped from a tube lining (GPB; July 2017). Length, ~350 μm. (C) Cable bacteria filaments in agglutinated mud layer, 2- to 3-mm-thick annulus surrounding a tube lining [adjacent to (B); scale as in (D)]. Mean length, 20 ± 9 μm (SD); minimum, 5 μm; maximum, 80 μm. (D) Filaments in radial zone 3 to 5 mm surrounding a tube lining [adjacent to (C)]. Mean length, 11 ± 8 μm (SD); minimum, 5 μm; maximum, 40 μm.

Fig. 2. 2D vertical Br⁻tracer penetration, alkalinity, and bacterial distributions.

(A) Br⁻ tracer penetration pattern in 2D vertical plane (5 cm thick perpendicular to section) after ~20 hours (GPB; June 2016; sediment-water interface at depth 0). A schematic net outlines approximate position of an inhabited U-shaped Chaetopterus tube located along the inner boundary of the sampled sediment section (~5 to 6 cm from the core face; right arm angled slightly into the core). Dots indicate locations of pore water samples. (B) Pore water alkalinity distribution in box core. (C) Cable bacteria filament cell counts (white indicates below detection for sample size). (D) Free bacteria cell counts corresponding to sub-array of (A). Both cable filament cells and free cells have elevated abundance near Chaetopterus tube sections and subdomains of enhanced solute exchange with overlying oxygenated water.

Fig. 3. 2D horizontal Br⁻tracer and cable bacteria distributions.

(A) Stacked horizontal sections (3 to 5 cm thick) showing Br⁻ penetration as a function of depth and horizontal planes. High penetration regions are associated primarily with two inhabited Chaetopterus tube sections (July 2017). (B) Box-whisker diagrams showing lengths of cable filaments at varying horizontal x positions separated along two transects within the 3- to 8-cm, level 2 interval (y = 6 and 8 cm; arrows). Black square, mean; line, median; red diamonds, outliers; box, 25 to 75% quartiles. (C) Filament cell abundance corresponding to array positions along transects (3- to 8-cm depth interval). Filaments occur through the sediment but with the longest filaments and most abundant filament cells found closest to regions of greatest Br⁻ concentrations near Chaetopterus tubes.

Fig. 4. pH, sediment S, and dissolved Fe²⁺distributions around Chaetopterus tubes.

(A) 2D radial pH distribution around Chaetopterus tube revealed in horizontal section of a core by planar pH optode, demonstrating elevated pH associated with tube lining and immediately surrounding sediment (LIS Smithtown Bay site). The low pH trail (bottom left) is the body surface of a polychaete, Nepthys incisa, moving horizontally within the sampling plane. The water level in the oxygenated tube lumen was below the pH sensor film during imaging and is shown as black. The curved core liner boundary is also shown as black. The white dotted lines represent locations of radial pH transects beginning at the tube lining boundary. (B) Radial transects of pH derived from (A). The radial geometry enhances the apparent elevated pH zone extent relative to the pH minimum zone (i.e., annulus areas defined by radius distance differences, change as a function of radius). (C) Radial transects of CRS around Chaetopterus tube showing depletion of solid-phase S toward tube within all vertical depth intervals (0 to 3, 3 to 6, and 6 to 9 cm). Bars indicate radial annulus of sample. (D) 2D dissolved Fe²⁺ distribution around Chaetopterus tube from GPB site. SWI, sediment-water interface. A radial distribution of Fe²⁺ at a depth of ~5 cm (horizontal dotted line on image) illustrates enhanced concentrations at distances of 1 to 2 cm from the tube wall (vertical dotted lines) and concentration gradients toward the lining that result in Fe-oxide deposition.

Fig. 5. Chaetopterus tube lining formed in seawater or within sediment.

(A) SEM image of tube lining formed by Chaetopterus in a laboratory aquarium in the absence of sediment. No authigenic mineral precipitates are evident. The ~60° × 120° oriented polymer strand structure is common in polychaete tube linings (20). (B) Chaetopterus tube linings formed in situ are permeated with micronodules of Mn oxide, often preferentially aligned with polymer strands. Fe oxide–rich precipitates are also present and can dominate in some sections of linings; however, Mn enrichment is more common (SEM; scale bar, 10 μm).