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

Abstract

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.

Exceptionally high respiration rates in the reactive surface layer of sediments underlying oxygen-deficient bottom waters

“…Note the difference in the y -axis for all sites. Red lines in ( b ) and ( c ) indicate diagenetic model fits used to derive production profiles with FLIPPER [40]; arrows indicate bottom-water concentration.…”

“…Hence, the integrated respiration rate can be estimated from the integrated sulphate production (RprodSO42−) as follows Rtrueprefixminint=2RprodSO42−,where the two accounts for the stoichiometric ratio of carbon versus sulfur during sulphate reduction, and the negative sign is because SO42− is consumed as OC is respired. The production rates RprodDIC and RprodSO42− were calculated by inversely fitting a diagenetic model to the measured porewater profile using the R-script FLIPPER [40], which follows a similar procedure as outlined in [41]. FLIPPER analysis results are shown in the electronic supplementary material, figures S3 and S4.…”

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

“…The metabolic activity of cable bacteria appears to have a large impact on the biogeochemical cycling of Fe, Mn, P, S and trace elements in Lake Grevelingen [ 9 , 19 , 25 , 46 , 47 ]. The build-up of FeO x in the spring is an immediate consequence of the acidifying metabolism of cable bacteria and our experiments demonstrate that this large FeO x pool forms an effective barrier against sulfide release from the sediment later in the hypoxia season.…”

Sedimentary Pyrite Formation in a Seasonally Oxygen‐Stressed Estuary: Potential Imprints of Microbial Ecology and Position‐Specific Isotope Fractionation

“…We hypothesize that this may stem from the different SOM communities that dominate each site (Figure 7). The Beggiatoa that predominate at the shoal site may provide ZVS in a more soluble, reactive form than the ZVS at the channel site; alternately, the cable bacteria that predominate at the channel site may delay the seasonal growth of pyrite by accumulating arsenic in surface sediments in spring and early summer (Baya et al., 2021; S. J. van de Velde et al., 2022) in a process analogous to the seasonal delay of sulfide release from sediments (Seitaj et al., 2015).…”

“…Although comparative shoal‐channel data are not available for As, cable bacteria may accumulate As in surficial sediments of the channel site. Active cable bacteria colonization promotes adsorption of As onto Fe‐oxides in surficial sediments, attaining As/Fe molar ratios as high as ∼0.2% until anoxic conditions release the As into bottom waters (S. J. van de Velde et al., 2022). Surface sediments from the channel site in July 2019 had an As/Fe ratio of 0.03% (Supporting Information ), and although this ratio is lower than the As/Fe ratios that were experimentally demonstrated to impede pyrite nucleation, this measurement was taken during the apex of summertime anoxia in the Chesapeake Bay channel, by which point most of the As accumulated by cable bacteria colonization already would have dissolved.…”