Oxygen isotope effects during microbial sulfate reduction: applications to sediment cell abundances

Abstract

The majority of anaerobic biogeochemical cycling occurs within marine sediments. To understand these processes, quantifying the distribution of active cells and gross metabolic activity is essential. We present an isotope model rooted in thermodynamics to draw quantitative links between cell-specific sulfate reduction rates and active sedimentary cell abundances. This model is calibrated using data from a series of continuous culture experiments with two strains of sulfate reducing bacteria (freshwater bacterium Desulfovibrio vulgaris strain Hildenborough, and marine bacterium Desulfovibrio alaskensis strain G-20) grown on lactate across a range of metabolic rates and ambient sulfate concentrations. We use a combination of experimental sulfate oxygen isotope data and nonlinear regression fitting tools to solve for unknown kinetic, step-specific oxygen isotope effects. This approach enables identification of key isotopic reactions within the metabolic pathway, and defines a new, calibrated framework for understanding oxygen isotope variability in sulfate. This approach is then combined with porewater sulfate/sulfide concentration data and diagenetic modeling to reproduce measured 18 O/ 16 O in porewater sulfate. From here, we infer cell-specific sulfate reduction rates and predict abundance of active cells of sulfate reducing bacteria, the result of which is consistent with direct biological measurements.

Modelling the Effects of Non-Steady State Transport Dynamics on the Sulfur and Oxygen Isotope Composition of Sulfate in Sedimentary Pore Fluids

“…When the recycling parameter is non-zero, (in Figure 4A, r 0) then there is intracellular recycling and oxygen isotopes are exchanged with water through various (unspecified) intermediates. The cross plot shows both the apparent linear phase and the equilibration phase, with an asymptote as δ 34 S continues to increase as the sulfate pool undergoes MSR, while δ 18 O SO4 remains constant once oxygen isotopic equilibrium with water is reached (Fritz et al, 1989;Aller and Blair, 1996;Aller et al, 2010;Antler et al, 2013;Antler et al, 2017;Bertran et al, 2020).…”

“…The oxygen isotope composition of extracellular sulfate is dominated by the rapid, intracellular, exchange of oxygen atoms in intermediate-valence state sulfur species with the ambient water, which ultimately drives δ 18 O SO4 to reflect the pore water value plus the oxygen isotope fractionation of this isotope-exchange. In this way, the residual sulfate pool becomes increasingly enriched in the heavier isotopes as MSR progresses (Böttcher et al, 1998;Böttcher et al, 1999;Canfield, 1998;Wortmann et al, 2001;Canfield et al, 2010;Sim et al, 2011a;Müller, 2013;Wankel et al, 2014;Wing and Halevy, 2014;Giannetta et al, 2019;Bertran et al, 2020;Pellerin et al, 2020). Other processes are known to affect the sulfur and oxygen isotope compositions of marine sediments, chiefly; sulfide and pyrite oxidation (Balci et al, 2007;Brunner et al, 2008;Heidel and Tichomirowa, 2011;Kohl and Bao, 2011;Jørgensen et al, 2019), disproportionation Böttcher et al, 2005;Blonder et al, 2017), and the anaerobic oxidation of methane (Antler et al, 2013;Antler et al, 2014;Antler et al, 2015;Deusner et al, 2014) but we do not consider them further in this study.…”

“…Indeed, the SALP may be one of the foremost geochemical tools available to interpret rate and mechanism of MSR, alongside 35 SO 4 based assays (King, 2001), in the absence of advanced genomic techniques. Other geochemical tools that have been used to investigate the rate and mechanism of MSR include Δ 33 S techniques to identify sulfur reoxidation and disproportionation contributing to sulfur isotope signatures alongside MSR (Johnston, 2005;Johnston et al, 2007;Pellerin et al, 2015) and recent developments in the use the MSR oxygen isotope effects to predict cell specific MSR rates and predict the abundance of active cells performing MSR, as well as providing quantitative links between these factors and environmental conditions (Bertran et al, 2020). Changes in the concentration of sulfate during MSR yield information on the net consumption of sulfate but provide no information on the relative reversibility of the intracellular steps.…”

Deciphering Historical Water-Quality Changes Recorded in Sediments Using eDNA

“…The sediment profile is heterogeneous even in the steady state, which does not have a human disturbance. The oxygen concentration drops sharply in the top profile, and other electron acceptors, for example, sulfate in the upper layer in this research, become dominant oxidants in anaerobic sediment according to the free energy needed for the reaction (Gu et al, 2007;Li et al, 2012;Bertran et al, 2020). While the mircogAMBI did not count this situation in, the long-term biogeochemical cycle can degrade a large portion of pollutants and keep only refractory substances, for example, bromine, chlorine and high molecular-weight PAHs, in the deep sediment in this study, causing relatively indistinctive changes in microgAMBI indices.…”

“…Because natural and anthropogenic activities are the main sources of these chemical substances, we speculated that the present profile of geochemical and microbiological activities could reflect the past environment. However, most studies on sediment profiles have focused on diagenetic processes, such as oxygen availability, nitrate reduction zones and sulfate reduction zones (Gu et al, 2007;Li et al, 2012;Bertran et al, 2020). The possibility of sedimental chemical substances and microbial communities keeping messages of historical water quality remains undiscovered.…”