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

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.