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.

Mud, Microbes, and Macrofauna: Seasonal Dynamics of the Iron Biogeochemical Cycle in an Intertidal Mudflat

“…The Desulfobulbaceae is a diverse family within the Deltaproteobacteria that contains the so-called "cable bacteria" that transport electrons from sulfur oxidation over centimeter scale distances and catalyze oxygen reduction at sediment-water interfaces (Nielsen et al, 2010;Meysman et al, 2015;Nielsen and Risgaard-Petersen, 2015). We have observed on many occasions the presence of cable bacteria-like filaments from this field site ( Figure 1F), and hypothesize that they are functional in these bioturbated sediments, which has been recently demonstrated (Aller et al, 2019), and may impact iron dynamics (Sulu-Gambari et al, FIGURE 5 | A heatmap of the relative abundance of bacterial and archaeal taxonomic units (OTUs) clustered at 85% identity that were at least 0.5% relative abundance in one sample (n = 76 OTUs). The different samples were clustered using average linkage hierarchical clustering of the Bray-Curtis dissimilarity as implemented in the R package vegan (Oksanen et al, 2019).…”

Inducing the attachment of cable bacteria on oxidizing electrodes

“…This CV behavior suggests that any current generated by the biomass of electroactive bacteria, including CB, was obscured during scans by current arising from irreversible redox reactions, such as oxidation of dissolved iron. A reduction peak was unidentifiable throughout the scans, a common phenomenon in sediment MFCs (Babauta and Beyenal, 2015). Taken together, these results demonstrate that the electrode surface was altered during the course of the bioreactor experiment by mineral and chemical precipitate deposition (Imran et al, 2019).…”

“…Besides the recognized forms of CB, short filaments within the family of Desulfobulbaceae that possessed different morphologies were also observed on the anode surface. Aller et al (2019) suggest that redox environment may play an important role in controlling the length of CB filaments. For example, in the bioturbated zone as-sociated with the tube worm Chaetopterus variopedatus, in which redox conditions often oscillated between oxic and hypoxic, CB were present predominately in short filaments.…”

“…The interpretation of such voltammograms may be complicated by a high uncompensated resistance between working electrode and reference electrode (Babauta and Beyenal, 2015). While an oxidation peak can be clearly identified at potentials near where the anode was held, the peak current did not increase with an increase in scan rate (Fig.…”

The Critical Role of Bioturbation for Particle Dynamics, Priming Potential, and Organic C Remineralization in Marine Sediments: Local and Basin Scales

“…There is a tendency to focus labile planktonic C org into the shallower regions (Sun et al, 1994). cosmogenic nuclide 7 Be (t 1/2 = 53 days) that show penetration to >12 cm (Aller et al, 2019).…”