Cable bacteria generate a firewall against euxinia in seasonally hypoxic basins

Abstract

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 euxiniapreventing firewall mechanism could be widely active, and may explain why euxinia is relatively infrequently observed in the coastal ocean. sediment biogeochemistry | cable bacteria | coastal hypoxia | sulfur cycling | microbial competition

Phosphorus Cycling and Burial in Sediments of a Seasonally Hypoxic Marine Basin

“…12). A seasonal succession in the dominant type of sulphur-oxidising bacteria in the sediments was observed from 2011 to 2015 with cable bacteria dominating in spring and Beggiatoaceae in autumn (Seitaj et al 2015). The seasonal changes in bottom-water oxygen and the bacterial community have major implications for the release of P from the sediment, as shown previously for site 1 by Sulu-Gambari et al (2016a).…”

“…3). In early summer, when the cable bacteria population has declined, reductive dissolution of the Fe-(oxyhydr)oxides by sulphides (Seitaj et al 2015), leads to a release of associated PO 4 (Sulu-Gambari et al 2016a). The production of Fe 2+ and PO 4 in the pore water of the surface sediment is then coupled.…”

“…Short sediment cores (~40 cm) with 20 cm of overlying water were collected at the three sites with a gravity corer (UWITEC, Austria) using Plexiglas ® core liners (6 cm inner diameter; 60 cm length). Further details on sediment sampling are given by Seitaj et al (2015) and SuluGambari et al (2016b). The sites are characterised by sediment accumulation rates ranging from~0.4 to 2 cm year −1 (Fig.…”

“…Cable bacteria were identified in the surface sediment at sites 1 and 3 in March and May 2012, using fluorescence in situ hybridisation (FISH) and based on typical pH, O 2 and H 2 S profiles, but were not detected at site 2 (Seitaj et al 2015;Sulu-Gambari et al 2016a, b). Beggiatoaceae were present at all three sites in autumn (Seitaj et al 2015;Sulu-Gambari et al 2016a, b). The clear signals of activity in the bulk porewater geochemistry (e.g.…”

“…This typically leads to a distinct pH fingerprint with a surficial pH peak due to proton consumption via the reduction of oxygen and a pH minimum at depth due to the oxidation of sulphide (H 2 S) deeper in the sediment (Meysman et al 2015). Both laboratory (Rao et al 2016;Risgaard-Petersen et al 2012) and field studies (Seitaj et al 2015;Sulu-Gambari et al 2016a) have demonstrated that the acidification of the pore water at depth leads to the dissolution of iron monosulphide (FeS) and calcium carbonate (CaCO 3 ) and subsequent formation of Fe-(oxyhydr)oxides upon oxidation of upward diffusing Fe 2+ , with oxygen (Rao et al 2016;Risgaard-Petersen et al 2012;van de Velde et al 2016) or with Mn-oxides (Sulu-Gambari et al 2016a;.…”