Cable bacteria generate a firewall against euxinia in seasonally hypoxic basins

Seasonal oxygen depletion (hypoxia) in coastal bottom waters can lead to the release and persistence of free sulfide (euxinia), which is highly detrimental to marine life. Although coastal hypoxia is relatively common, reports of euxinia are less frequent, which suggests that certain environmental controls can delay the onset of euxinia. However, these controls and their prevalence are poorly understood. Here we present field observations from a seasonally hypoxic marine basin (Grevelingen, The Netherlands), which suggest that the activity of cable bacteria, a recently discovered group of sulfur-oxidizing microorganisms inducing long-distance electron transport, can delay the onset of euxinia in coastal waters. Our results reveal a remarkable seasonal succession of sulfur cycling pathways, which was observed over multiple years. Cable bacteria dominate the sediment geochemistry in winter, whereas, after the summer hypoxia, Beggiatoaceae mats colonize the sediment. The specific electrogenic metabolism of cable bacteria generates a large buffer of sedimentary iron oxides before the onset of summer hypoxia, which captures free sulfide in the surface sediment, thus likely preventing the development of bottom water euxinia. As cable bacteria are present in many seasonally hypoxic systems, this euxinia-preventing firewall mechanism could be widely active, and may explain why euxinia is relatively infrequently observed in the coastal ocean

Cable bacteria delay euxinia and modulate phosphorus release in coastal hypoxic systems

Abstract: Cable bacteria are long, filamentous bacteria with a unique metabolism involving centimetre-scale electron transport. They are widespread in the sediment of seasonally hypoxic systems and their metabolic activity stimulates the dissolution of iron sulfides (FeS), releasing large quantities of ferrous iron (Fe2+) into the pore water. Upon contact with oxygen, Fe2+ oxidation forms a layer of iron(oxyhydr)oxides (FeOx), which in its turn can oxidize free sulfide (H2S) and trap phosphorus (P) diffusing upward. The metabolism of cable bacteria could thus prevent the release of H2S from the sediment and reduce the risk of euxinia, while at the same time modulating P release over seasonal timescales. However, experimental support for this so-called 'iron firewall hypothesis' is scarce. Here, we collected natural sediment in a seasonally hypoxic basin in three different seasons. Undisturbed sediment cores were incubated under anoxic conditions and the effluxes of H2S, dissolved iron (dFe) and phosphate (PO4 3-) were monitored for up to 140 days. Cores with recent cable bacterial activity revealed a high stock of sedimentary FeOx, which delayed the efflux of H2S for up to 102 days. Our results demonstrate that the iron firewall mechanism could exert an important control on the prevalence of euxinia and regulate the P release in coastal oceans

Cable bacteria delay euxinia and modulate phosphorus release in coastal hypoxic systems

Cable bacteria are long, filamentous bacteria with a unique metabolism involving centimetre-scale electron transport. They are widespread in the sediment of seasonally hypoxic systems and their metabolic activity stimulates the dissolution of iron sulfides (FeS), releasing large quantities of ferrous iron (Fe2+) into the pore water. Upon contact with oxygen, Fe2+ oxidation forms a layer of iron(oxyhydr)oxides (FeOx), which in its turn can oxidize free sulfide (H2S) and trap phosphorus (P) diffusing upward. The metabolism of cable bacteria could thus prevent the release of H2S from the sediment and reduce the risk of euxinia, while at the same time modulating P release over seasonal timescales. However, experimental support for this so-called ‘iron firewall hypothesis’ is scarce. Here, we collected natural sediment in a seasonally hypoxic basin in three different seasons. Undisturbed sediment cores were incubated under anoxic conditions and the effluxes of H2S, dissolved iron (dFe) and phosphate (PO43−) were monitored for up to 140 days. Cores with recent cable bacterial activity revealed a high stock of sedimentary FeOx, which delayed the efflux of H2S for up to 102 days. Our results demonstrate that the iron firewall mechanism could exert an important control on the prevalence of euxinia and regulate the P release in coastal oceans.BT/Environmental Biotechnolog

Supplementary Materials from Cable bacteria delay euxinia and modulate phosphorus release in coastal hypoxic systems

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Cable Bacteria Activity Modulates Arsenic Release From Sediments in a Seasonally Hypoxic Marine Basin

Eutrophication and global change are increasing the occurrence of seasonal hypoxia (bottom-water oxygen concentration <63 μM) in coastal systems worldwide. In extreme cases, the bottom water can become completely anoxic, allowing sulfide to escape from the sediments and leading to the development of bottom-water euxinia. In seasonally hypoxic coastal basins, electrogenic sulfur oxidation by long, filamentous cable bacteria has been shown to stimulate the formation of an iron oxide layer near the sediment-water interface, while the bottom waters are oxygenated. Upon the development of bottom-water anoxia, this iron oxide “firewall” prevents the sedimentary release of sulfide. Iron oxides also act as an adsorption trap for elements such as arsenic. Arsenic is a toxic trace metal, and its release from sediments can have a negative impact on marine ecosystems. Yet, it is currently unknown how electrogenic sulfur oxidation impacts arsenic cycling in seasonally hypoxic basins. In this study, we presented results from a seasonal field study of an uncontaminated marine lake, complemented with a long-term sediment core incubation experiment, which reveals that cable bacteria have a strong impact on the arsenic cycle in a seasonally hypoxic system. Electrogenic sulfur oxidation significantly modulates the arsenic fluxes over a seasonal time scale by enriching arsenic in the iron oxide layer near the sediment-water interface in the oxic period and pulse-releasing arsenic during the anoxic period. Fluxes as large as 20 μmol m−2 day−1 were measured, which are comparable to As fluxes reported from highly contaminated sediments. Since cable bacteria are recognized as active components of the microbial community in seasonally hypoxic systems worldwide, this seasonal amplification of arsenic fluxes is likely a widespread phenomenon.BT/Environmental Biotechnolog

Electrogenic sulfur oxidation by cable bacteria in two seasonally hypoxic coastal systems

Abstract: Cable bacteria can reach high densities in coastal sediments, and as a result of their unusual electrogenic lifestyle and intense metabolic activity, exert a major and distinct impact on biogeochemical cycling, both locally in sediments and at the ecosystem level. This appears to be particularly true for seasonally hypoxic systems, but the driving force behind the proliferation of cable bacteria in these systems is not well understood. Moreover, the metabolism of cable bacteria induces strong acid production, which can be buffered through carbonate dissolution in sediments. A strong depletion of alkalinity in the pore water is therefore expected in carbonate-poor sediments. To evaluate the impact of cable bacteria metabolism on sediment geochemistry, we performed field sampling and laboratory sediment incubations in two seasonally hypoxic sites: one carbonate-poor site with low levels of free sulfide in pore water (Yarra Estuary, Australia) and one carbonate-rich site with high free sulfide (Lake Grevelingen, The Netherlands). Active cable bacteria populations were found in both field locations, with higher abundance and activity observed in spring compared to autumn. The sediment incubations tracked the metabolic activity of cable bacteria over time (maximum 84 days), and confirmed the fast development of an electric network (cell doubling time: similar to 19 h). These results suggest that cable bacteria are widespread in seasonally hypoxic systems, supporting previous findings. Cable bacteria acidified the sediment by > 1.5 pH units in 6-13 days (differing per site) and their activity accounted for >70% of the oxygen uptake. A clear subsurface accumulation of Fe2+ was observed after 8 days of Yarra sediment incubations, indicative of increased FeS dissolution as e-SOx developed. The increased availability of sulfide from FeS dissolution promotes a positive-feedback loop that we infer allowed for a faster development of cable bacteria in the carbonate-poor sediments. A depletion of total alkalinity was observed in the deeper Yarra sediment, whereas, a higher alkalinity efflux was previously observed in the carbonate-rich sediments from Lake Grevelingen. These results suggest a differential pH and alkalinity dynamic due to the interaction between the local carbonate content of the sediment and cable bacteria activity