Biogenic structures and cable bacteria interactions: redox domain residence times and the generation of complex pH distributions

Abstract

Cable bacteria are multicellular filamentous bacteria that conduct electrons nonlocally between anoxic and oxic sediment regions, creating characteristic electrogenic pH fingerprints. These microbes aggregate in 3D patterns near biogenic structures, and filament fragments are also dispersed throughout deposits. Utilizing pH-sensitive planar optodes to investigate the dynamic response of electrogenic pH fingerprints to sediment reworking, we found that mobile bioturbators like nereid polychaetes (ragworms) can disturb the pH signatures. Sudden sediment disturbance associated with burrows at sub- to multi-centimeter scales eliminates detection of pH signatures. However, electrogenic pH fingerprints can recover in as little as 13 h near abandoned, closed burrows. Sequential collapse and regeneration of electrogenic pH fingerprints are associated with occupied and dynamic burrow structures, with the response time positively related to the scale of disturbance. In the case of relatively stable tube structures, built by benthos like spionid polychaetes and extending mm to cm into deposits, the electrogenic pH fingerprint is evident around the subsurface tubes. Cable filaments clearly associate with subsurface regions of enhanced solute exchange (oxidant supply) and relatively stable biogenic structures, including individual tubes and patches of tubes (e.g. made by Sabaco, a bamboo worm). Physically stable environments, favorable redox gradients, and enhanced organic/inorganic substrate availability promote the activity of cable bacteria in the vicinity of tubes and burrows. These findings suggest complex interactions between electrogenic activity fingerprints and species-specific patterns of bioturbation at multiple spatial and temporal scales, and a substantial impact of electrogenic metabolism on subsurface pH and early diagenetic reaction distributions in bioturbated deposits.