Cable bacteria activity and impacts in Fe and Mn depleted carbonate sediments

Abstract

The metabolic activities of cable bacteria enable the oxidation of sulfide to sulfate in anoxic sediment at depth through long distance electron transport coupled to the reductions of O2 and NO3−/NO2− in surface sediment. The spatial separation of oxidation and reduction half reactions requires modification of diagenetic models that assume electron donors and acceptors are coupled with each other locally within sedimentary deposits. In this study, we show that cable bacteria can become established and remain metabolically active in sulfidic, but Fe, Mn, and solid phase sulfide-depleted, carbonate muds from Florida Bay, USA. Sediment surface pH maxima reflecting electrogenic metabolism developed between 1 and 3 weeks in sediment incubated in laboratory microcosms with oxic overlying water. Cable filament cell abundances varied over time, with the increase initially focused within the subsurface, but by the end of experiments, cell abundances increased both in subsurface and oxic surface sediment. The development of cable bacteria activity in carbonate muds demonstrates that long-distance electron transport metabolism can utilize subsurface dissolved sulfide (e.g., H2S) as a sole reductant source for sustained periods without transition to Fe-sulfide and apparently without formation of an intermediate suboxic region associated with Fe and Mn cycling. H2S consumption occurs initially within the O2-NO3− rich oxic – suboxic zone and transitions to a dominant, but not exclusive, subsurface cable bacteria anodic zone. Once established, cable bacteria significantly altered sediment carbonate cycling. Thermodynamic calculations demonstrated that aragonite and hi-Mg-calcites were supersaturated (Ω ∼2.0–3.2) in the surface sediment layer (< 0.25 cm depth) and were undersaturated (Ω ∼ 0.2) in the anodic zone (1–2 cm depth). Hi-Mg-calcites and aragonite likely precipitated in the surface sediment and dissolved in the anodic region, the dissolution confirmed by elevated porewater Ca2+, Mg2+ concentrations. P cycling was coupled to remineralization of organic matter, carbonate mineral cycling, and apparently intracellular accumulation of polyphosphates. Thus, cable bacteria may play an important role in the acquisition of P by seagrasses in carbonate deposits where P is otherwise limited by irreversible adsorption and authigenic mineral precipitation.