Physiological approach to understand the mechanisms of hydrogen sulfide tolerance using a fish study system

Abstract

Hydrogen sulfide (H2S) is well known as a toxic gas produced by the decomposition of organic matter and geothermal sources and also produced endogenously by cysteine catabolism. Exposure to H2S drives hormetic effects including toxic inhibition of cytochrome c oxidase of the mitochondrial electron transport chain at high concentrations, and maintenance of normal vascular and neural functions at low concentrations. Abnormal elevation of cellular H2S, due to either environmental exposure or defective detoxification, is correlated with vascular and metabolic dysfunction in most aerobic organisms, however Poecilia mexicana thrives in H2S rich environments. The cellular mechanisms whereby organisms tolerate extreme H2S are not fully understood. Our central hypothesis is that sulfide tolerant fish have an enhanced H2S detoxification capacity and/or resistance to H2S toxicity following exposure, relative to non-tolerant fish. Specifically, we hypothesized that sulfide tolerant fish differentially express genes involved in maintaining H2S homeostasis. We found significant differences in gene expression patterns related to H2S detoxification between lab-reared sulfide tolerant and non-tolerant populations originating from the Tacotalpa drainage. Since mitochondria are both the site of H2S toxicity as well as enzymatic detoxification, we further hypothesized that tolerance is achieved by modifications to mitochondrial respiration. To test this, we compared mitochondrial function between 1) lab-reared and wild captured sulfide tolerant and non-tolerant populations originating from Tacotalpa drainage and 2) wild captured sulfide tolerant and non-tolerant populations originating from the Puyacatengo and Pichucalco drainages. We predicted that sulfide tolerant fish are able to maintain mitochondrial respiration in the presence of increasing concentrations of H2S relative to non-tolerant fish and that the sulfide tolerant population captured from Pichucalco drainage, which has the highest concentration of environmental H2S compared to other drainages tested, would exhibit the greatest degree of H2S tolerance compared to the sulfide tolerant populations from drainages with lower environmental H2S. We determined that mitochondria from sulfide tolerant fish have increased maximal and spare respiratory capacities following exposure to high concentrations of H2S, relative to non-tolerant fish, and that the population captured from Pichucalco exhibits the greatest degree of tolerance compared to the other two drainages.