Sulfur Isotope Fractionation by Sulfate-Reducing Microbes Can Reflect Past Physiology

Abstract

Sulfur (S) isotope fractionation by sulfate-reducing microorganisms is a direct manifestation of their respiratory metabolism. This fractionation is apparent in the substrate (sulfate) and waste (sulfide) produced. The sulfate-reducing metabolism responds to variability in the local environment, with the response determined by the underlying genotype, resulting in the expression of an "isotope phenotype". Sulfur isotope phenotypes have been used as a diagnostic tool for the metabolic activity of sulfate-reducing microorganisms in the environment. Our experiments with Desulfovibrio vulgaris Hildenborough (DvH) grown in batch culture suggest that the S isotope phenotype of sulfate respiring microbes may lag environmental changes on time scales that are longer than generational. When inocula from different phases of growth are assayed under the same environmental conditions, we observed that DvH exhibited different net apparent fractionations of up to -9‰. The magnitude of fractionation was weakly correlated with physiological parameters but was strongly correlated to the age of the initial inoculum. The S isotope fractionation observed between sulfate and sulfide showed a positive correlation with respiration rate, contradicting the well-described negative dependence of fractionation on respiration rate. Quantitative modeling of S isotope fractionation shows that either a large increase (≈50×) in the abundance of sulfate adenylyl transferase (Sat) or a smaller increase in sulfate transport proteins (≈2×) is sufficient to account for the change in fractionation associated with past physiology. Temporal transcriptomic studies with DvH imply that expression of sulfate permeases doubles over the transition from early exponential to early stationary phase, lending support to the transport hypothesis proposed here. As it is apparently maintained for multiple generations (≈1-6) of subsequent growth in the assay environment, we suggest that this fractionation effect acts as a sort of isotopic "memory" of a previous physiological and environmental state. Whatever its root cause, this physiological hysteresis effect can explain variations in fractionations observed in many environments. It may also enable new insights into life at energetic limits, especially if its historical footprint extends deeper than generational.

Proteomic and Isotopic Response of Desulfovibrio vulgaris to DsrC Perturbation

“…DsrC is less abundant in IPFG07 than in the WT, resulting in a smaller fractionation at the same csSRR. This is broadly consistent with recent observations of fractionation as functionally dependent on predicted enzyme abundances (Pellerin et al, 2018). Together this indicates that the magnitude of fractionation responds to the degree of utilization by a cell (or population) of its inherent sulfate reduction capacity.…”

The Biogeochemical Sulfur Cycle of Marine Sediments

“…Right axis (green squares): Distribution of csSRR in laboratory cultures where also sulfur isotope fractionation factors were determined. Rates compiled for marine sediment are taken from D’Hondt et al (2002); Leloup et al (2009), and Beulig et al (2018), while pure culture data are a non-exhaustive compilation from Kaplan and Rittenberg (1964), Chambers et al (1975), Detmers et al (2001), Habicht et al (2005), Hoek et al (2006), Johnston et al (2007), Davidson et al (2009), Eckert et al (2011), Sim et al (2011a,b, 2012), Leavitt et al (2013), Pellerin et al (2015a), Antler et al (2017), Zaarur et al (2017) and Pellerin et al (2018b).…”

“…When transferred to fresh medium, however, the expressed 34 ε does not immediately reflect the new growth conditions. Rather, a delay is observed in re-adjusting 34 ε which can even last longer than a generation (Pellerin et al, 2018b).…”

Large sulfur isotope fractionation by bacterial sulfide oxidation

“…All experiments were performed in the same medium under the same environmental conditions with the exception of the initial nitrate and sulfide concentrations, which varied between batches. Because sulfur isotope fractionation was under strong physiological control ( 35 ), in the three experiments that aimed at quantifying growth parameters and sulfur isotope fractionation (they were numbered 1 to 3; Table 1 and figs. S1 to S3), the same culture configuration was used; actively growing cells in the exponential phase were transferred to fresh medium three times without entering stationary phase before innoculating the assay bottles.…”