Cable Bacteria Control Iron–Phosphorus Dynamics in Sediments of a Coastal Hypoxic Basin

Abstract

Phosphorus is an essential nutrient for life. The release of phosphorus from sediments is critical in sustaining phytoplankton growth in many aquatic systems and is pivotal to eutrophication and the development of bottom water hypoxia. Conventionally, sediment phosphorus release is thought to be controlled by changes in iron oxide reduction driven by variations in external environmental factors, such as organic matter input and bottom water oxygen. Here, we show that internal shifts in microbial communities, and specifically the population dynamics of cable bacteria, can also induce strong seasonality in sedimentary iron-phosphorus dynamics. Field observations in a seasonally hypoxic coastal basin demonstrate that the long-range electrogenic metabolism of cable bacteria leads to a dissolution of iron sulfides in winter and spring. Subsequent oxidation of the mobilized ferrous iron with manganese oxides results in a large stock of iron-oxide-bound phosphorus below the oxic zone. In summer, when bottom water hypoxia develops and cable bacteria are undetectable, the phosphorus associated with these iron oxides is released, strongly increasing phosphorus availability in the water column. Future research should elucidate whether formation of iron-oxide-bound phosphorus driven by cable bacteria, as observed in this study, contributes to the seasonality in iron-phosphorus cycling in aquatic sediments worldwide.

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

“…This has been attributed to binding of P to Fe-(oxyhydr)oxides, which is supported by the presence of a large stock of Fe-bound P in the surface sediment (Sulu-Gambari et al 2016a). In this latter study, however, the stock of Fe-bound P was determined with an operational SEDEX extraction (Ruttenberg 1992) that can also extract vivianite (Dijkstra et al 2014;Dijkstra et al 2016;Egger et al 2015).…”

“…Furthermore, in a recent study of P cycling at a site in a seasonally hypoxic coastal marine basin (Lake Grevelingen, the Netherlands), Sulu-Gambari et al (2016a) demonstrated a lack of authigenic Ca-P formation at a site where polyphosphate-bearing Beggiatoaceae were abundant in autumn. In the latter setting, cable bacteria, a g r o u p o f s u l p h u r -o x i d i s i n g b a c t e r i a f r o m t h e Desulfobulbaceae family (Burdorf et al 2016;Nielsen et al 2010;Pfeffer et al 2012;Risgaard-Petersen et al 2012;Trojan et al 2016) that can also form polyphosphates in their cells were active in spring (Sulu-Gambari et al 2016a).…”

“…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;.…”

“…In sediments where cable bacteria are active, upwarddiffusing dissolved phosphate is retained in the surface sediment and does not escape to the overlying water (Rao et al 2016;Sulu-Gambari et al 2016a). This has been attributed to binding of P to Fe-(oxyhydr)oxides, which is supported by the presence of a large stock of Fe-bound P in the surface sediment (Sulu-Gambari et al 2016a).…”

“…In this study, we build on our prior work on Fe and P dynamics in sediments subject to seasonal bottom-water hypoxia (Sulu-Gambari et al 2016a;. We present data for the same study area, Lake Grevelingen (the Netherlands), but specifically focus on determining the types of P phases present in the surface sediment using X-ray absorption spectroscopy (XAS).…”