H2S exposure elicits differential expression of candidate genes in fish adapted to sulfidic and non-sulfidic environments

Tobler, Michael; Henpita, Chathurika; Bassett, Brandon; Kelley, Joanna L.; Shaw, Jennifer H.

doi:10.1016/j.cbpa.2014.04.012

Cited by 34 publications

(37 citation statements)

References 58 publications

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“…The gene encoding sulphide:quinone oxidoreductase, a conserved protein that catalyses the first step of enzymatic H 2 S oxidation in many metazoans 9 is consistently higher expressed in natural sulphide spring populations. Furthermore, common garden reared Tac-S individuals retain higher constitutive expression of ARTICLE this gene even in the absence of environmental H 2 S in the laboratory 10 . This indicates that adaptation to H 2 S may include mechanisms that reduce adverse effects of elevated exogenous concentrations (like a tolerant COX) and mechanisms that maintain low internal concentrations despite the constant influx of environmental H 2 S. Phylogenetic hypothesis testing showed that the nonsusceptible P. sulphuraria and P. mexicana lineages arose independently and at different timescales (Fig.…”

Section: Discussionmentioning

confidence: 94%

Parallel evolution of cox genes in H2S-tolerant fish as key adaptation to a toxic environment

et al. 2014

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Populations that repeatedly adapt to the same environmental stressor offer a unique opportunity to study adaptation, especially if there are a priori predictions about the genetic basis underlying phenotypic evolution. Hydrogen sulphide (H 2 S) blocks the cytochrome-c oxidase complex (COX), predicting the evolution of decreased H 2 S susceptibility of the COX in three populations in the Poecilia mexicana complex that have colonized H 2 S-containing springs. Here, we demonstrate that decreased H 2 S susceptibility of COX evolved in parallel in two sulphide lineages, as evidenced by shared amino acid substitutions in cox1 and cox3 genes. One of the shared substitutions likely triggers conformational changes in COX1 blocking the access of H 2 S. In a third sulphide population, we detect no decreased H 2 S susceptibility of COX, suggesting that H 2 S resistance is achieved through another mechanism. Our study thus demonstrates that even closely related lineages follow both parallel and disparate molecular evolutionary paths to adaptation in response to the same selection pressure.

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Section: Discussionmentioning

confidence: 94%

Parallel evolution of cox genes in H2S-tolerant fish as key adaptation to a toxic environment

et al. 2014

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“…The mechanism is complex and depends upon details of the active-site structure (see Discussion), and relatively resistant forms of the enzyme are found in a few higher organisms that routinely experience sulfide stress (Martin & Maricle, 2015, Pfenninger et al , 2013, Tobler et al , 2014). The impact of sulfide upon bacterial cytochrome bo oxidase has not been reported.…”

Section: Resultsmentioning

confidence: 99%

The cytochrome bd oxidase of Escherichia coli prevents respiratory inhibition by endogenous and exogenous hydrogen sulfide

Korshunov

Imlay

2016

Molecular Microbiology

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Summary When sulfur compounds are scarce or difficult to process, E. coli adapts by inducing the high-level expression of sulfur-compound importers. If cystine then becomes available, the cystine is rapidly overimported and reduced, leading to a burgeoning pool of intracellular cysteine. Most of the excess cysteine is exported, but some is adventitiously degraded, with the consequent release of sulfide. Sulfide is a potent ligand of copper and heme moieties, raising the prospect that it interferes with enzymes. We observed that when cystine was provided and sulfide levels rose, E. coli became strictly dependent upon cytochrome bd oxidase for continued respiration. Inspection revealed that low-micromolar levels of sulfide inhibited the proton-pumping cytochrome bo oxidase that is regarded as the primary respiratory oxidase. In the absence of the back-up cytochrome bd oxidase, growth failed. Exogenous sulfide elicited the same effect. The potency of sulfide was enhanced when oxygen concentrations were low. Natural oxic-anoxic interfaces are often sulfidic, including the intestinal environment where E. coli dwells. We propose that the sulfide resistance of the cytochrome bd oxidase is a key trait that permits respiration in such habitats.

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“…Based on previous research, we also expected sulphide spring fishes to have a lower carbon (C) content due to energetic costs associated with life in extreme environments (Passow et al ., ) and associated differences in body condition between sulphidic and non‐sulphidic populations (Tobler, ). Finally, sulphide spring fishes may exhibit elevated phosphorus (P) content, because of potential increases in P‐rich bone mass associated with enlarged heads (Tobler et al ., ) and high rates of transcription of genes (P‐rich RNA) associated with H 2 S detoxification (Tobler et al ., ). (2) How do genetic and plastic differences among populations interact to shape variation in organismal stoichiometry?…”

Section: Introductionmentioning

confidence: 97%

Using replicated evolution in extremophile fish to understand diversification in elemental composition and nutrient excretion

et al. 2015

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Summary Ecological sources of selection are key drivers of evolutionary change in populations. Information on the ecological relevance of such evolutionary shifts is comparatively sparse and has received renewed interest. The framework of ecological stoichiometry is useful to investigate the reciprocal effects between ecology and evolution, because data on somatic stoichiometry of ancestral and descendent populations can be used to predict ecological functions, such as nutrient recycling, using mass balance‐based models. Here, we investigated whether divergent populations of livebearing fishes (genus Poecilia) have diverged in elemental composition. We tested whether adaptation to local environmental conditions is manifested in changes of somatic stoichiometry by measuring carbon (C), nitrogen (N), phosphorus (P) and sulphur (S) contents of wild‐caught individuals inhabiting sulphidic (extreme) and non‐sulphidic (benign) habitats. We also attempted to isolate the sources (i.e. genetic, environmental and their interaction) of intraspecific variation in stoichiometry. Finally, we tested whether shifts in somatic stoichiometry impinge on the rates at which key nutrients (N and P) are excreted. We found significant differentiation in somatic stoichiometry between fish from the two different habitat types in two of three river drainages, with fish from sulphidic habitats having lower C but higher P and S contents. Even though there was evidence for temporal variation and plasticity in elemental composition, differences between sulphidic and non‐sulphidic populations in P and S contents were maintained in laboratory populations over multiple generations. Finally, some sulphidic and non‐sulphidic population pairs differed in the rates of N and P excretions, although excretion rates were not related to somatic stoichiometry. Together, these results show that the elemental composition of organisms appears to have the characteristics typically observed in the evolution of biochemical, physiological and morphological traits. Studying taxa that have undergone replicated evolution illuminate some of the evolutionary mechanisms that drive variation in somatic elemental composition. Applying stoichiometric principles to such variation, as we have performed here, is a useful, yet underutilised approach to understand the ecological relevance of evolutionary change.

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H2S exposure elicits differential expression of candidate genes in fish adapted to sulfidic and non-sulfidic environments

Cited by 34 publications

References 58 publications

Parallel evolution of cox genes in H2S-tolerant fish as key adaptation to a toxic environment

Parallel evolution of cox genes in H2S-tolerant fish as key adaptation to a toxic environment

The cytochrome bd oxidase of Escherichia coli prevents respiratory inhibition by endogenous and exogenous hydrogen sulfide

Using replicated evolution in extremophile fish to understand diversification in elemental composition and nutrient excretion

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