The important life-supporting role of hydrogen sulfide (H2S) has evolved from bacteria to plants, invertebrates, vertebrates, and finally to mammals. Over the centuries, however, H2S had only been known for its toxicity and environmental hazard. Physiological importance of H2S has been appreciated for about a decade. It started by the discovery of endogenous H2S production in mammalian cells and gained momentum by typifying this gasotransmitter with a variety of physiological functions. The H2S-catalyzing enzymes are differentially expressed in cardiovascular, neuronal, immune, renal, respiratory, gastrointestinal, reproductive, liver, and endocrine systems and affect the functions of these systems through the production of H2S. The physiological functions of H2S are mediated by different molecular targets, such as different ion channels and signaling proteins. Alternations of H2S metabolism lead to an array of pathological disturbances in the form of hypertension, atherosclerosis, heart failure, diabetes...

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Physiological Implications of Hydrogen Sulfide: A Whiff Exploration That Blossomed

Reactive oxygen, nitrogen, and sulfur species, referred to as ROS, RNS, and RSS, respectively, are produced during normal cell function and in response to various stimuli. An imbalance in the metabolism of these reactive intermediates results in the phenomenon known as oxidative stress. If left unchecked, oxidative molecules can inflict damage on all classes of biological macromolecules and eventually lead to cell death. Indeed, sustained elevated levels of reactive species have been implicated in the etiology (e.g., atherosclerosis, hypertension, diabetes) or the progression (e.g., stroke, cancer, and neurodegenerative disorders) of a number of human diseases.1 Over the past several decades, however, a new paradigm has emerged in which the aforementioned species have also been shown to function as targeted, intracellular second messengers with regulatory roles in an array of physiological processes.2 Against this backdrop, it is not surprising that considerable ongoing efforts are aimed at elucidating the role that these reactive intermediates play in health and disease.

Site-specific, covalent modification of proteins represents a prominent molecular mechanism for transforming an oxidant signal into a biological response. Amino acids that are candidates for reversible modification include cysteines whose thiol (i.e., sulfhydryl) side chain is deprotonated at physiological pH, which is an important attribute for enhancing reactivity. While reactive species can modify other amino acids (e.g., histidine, methionine, tryptophan, and tyrosine), this Review will focus exclusively on cysteine, whose identity as cellular target or “sensor” of reactive intermediates is most prevalent and established.3 Oxidation of thiols results in a range of sulfur-containing products, not just disulfide bridges, as typically presented in biochemistry textbooks. An overview of the most relevant forms of oxidized sulfur species found in vivo is presented in Chart 1.






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Chart 1

Biologically Relevant Cysteine Chemotypesa

aRed, irreversible modifications. Green, unique enzyme intermediates. Note: Additional modifications can form as enzyme intermediates including thiyl radicals, disulfides, and persulfides.

Cysteine-Mediated Redox Signaling: Chemistry, Biology, and Tools for Discovery

Redox Biochemistry of Hydrogen Sulfide

Signaling by H2S is proposed to occur via persulfidation, a posttranslational modification of cysteine residues (RSH) to persulfides (RSSH). Persulfidation provides a framework for understanding the physiological and pharmacological effects of H2S. Due to the inherent instability of persulfides, their chemistry is understudied. In this review, we discuss the biologically relevant chemistry of H2S and the enzymatic routes for its production and oxidation. We cover the chemical biology of persulfides and the chemical probes for detecting them. We conclude by discussing the roles ascribed to protein persulfidation in cell signaling pathways.

Chemical Biology of H2S Signaling through Persulfidation.

Cold seeps occur in geologically active and passive continental margins, where pore waters enriched in methane are forced upward through the sediments by pressure gradients. The advective supply of methane leads to dense microbial communities with high metabolic rates. Anaerobic methane oxidation presumably coupled to sulphate reduction facilitates formation of carbonates and, in many places, generates extremely high concentrations of hydrogen sulphide in pore waters. Increased food supply, availability of hard substratum and high concentrations of methane and sulphide supplied to free-living and symbiotic bacteria provide the basis for the complex ecosystems found at these sites. This review examines the structures of animal communities in seep sediments and how they are shaped by hydrologic, geochemical and microbial processes. The full size range of biota is addressed but emphasis is on the mid-size sediment-dwelling infauna (foraminiferans, metazoan meiofauna and macrofauna), which have received less attention than megafauna or microbes. Megafaunal biomass at seeps, which far exceeds that of surrounding non-seep sediments, is dominated by bivalves (mytilids, vesicomyids, lucinids and thyasirids) and vestimentiferan tube worms, with pogonophorans, cladorhizid sponges, gastropods and shrimp sometimes abundant. In contrast, seep sediments at shelf and upper slope depths have infaunal densities that often differ very little from those in ambient sediments. At greater depths, seep infauna exhibit enhanced densities, modified composition and reduced diversity relative to background sediments. Dorvilleid, hesionid and ampharetid polychaetes, nematodes, and calcareous foraminiferans are dominant. There is extensive spatial heterogeneity of microbes and higher organisms at seeps. Specialized infaunal communities are associated with different seep habitats (microbial mats, clam beds, mussel beds and tube worms aggregations) and with different vertical zones in the sediment. Whereas fluid flow and associated porewater properties, in particular sulphide concentration, appear to regulate the distribution, physiological adaptations and sometimes behaviour of many seep biota, sometimes the reverse is true. Animal-microbe interactions at seeps are complex and involve symbioses, heterotrophic nutrition, geochemical feedbacks and habitat structure. Nutrition of seep fauna varies, with thiotrophic and methanotrophic symbiotic bacteria fueling most of the megafaunal forms but macrofauna and most meiofauna are mainly heterotrophic. Macrofaunal food sources are largely photosynthesis-based at shallower seeps but reflect carbon fixation by chemosynthesis and considerable incorporation of methane-derived C at deeper seeps. Export of seep carbon appears to be highly localized based on limited studies in the Gulf of Mexico. Seep ecosystems remain one of the ocean's true frontiers. Seep sediments represent some of the most extreme marine conditions and offer unbounded opportunities for discovery in the realms of animal-microbe-geochemical interactions, physiology, trophic ecology, biogeography, system-atics and evolution.

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Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes

Solemya reidi, a gutless clam found in sulfide-rich habitats, contains within its gills bacterial symbionts thought to oxidize sulfur compounds and provide a reduced carbon food source to the clam. However, the initial step or steps in sulfide oxidation occur in the animal tissue, and mitochondria isolated from both gill and symbiont-free foot tissue of the clam coupled the oxidation of sulfide to oxidative phosphorylation [adenosine triphosphate (ATP) synthesis]. The ability of Solmya reidi to exploit directly the energy in sulfide for ATP synthesis is unprecedented, and suggests that sulfide-habitat animals that lack bacterial symbionts may also use sulfide as an inorganic energy source.

https://science.sciencemag.org/content/sci/233/4763/563.full.pdf

Hydrogen Sulfide Oxidation Is Coupled to Oxidative Phosphorylation in Mitochondria of Solemya reidi

The detoxification and metabolism of sulfide were studied in three symbiont containing invertebrates from the deep-sea hydrothermal vents: the tube worm, R@ftia pachyptila; the clam, Ca!yptogena nwgn@fica; and the mussel, Bathymodiolus ther mophilus. Sulfide oxidizing activities, due to specific sulfide oxidase enzymes, were found in all tissues, with the greatestactivities occurringin the symbiont-contaiing tissues:the trophosome ofthe tube worm and the gills ofthe bivalves. Sulfideoxidase activity was correlated with the bacterial content of the tissues. The sulfide oxidases in the outer cell layer(s)ofsymbiont-free tissues, e.g., body wall muscle ofRzfiia and foot and mantle of the bivalves, may detoxify sulfide as soon as it enters the body. Sulfideenteringthe blood in Riflia and Ca!yptogenamay be bound by sulfide-binding factors that transportsulfide to the symbionts and protect against sulfide inhibition ofaerobic respiration [via effects on the cytochrome-c oxidase (CytOx) system]. Sulfide strongly inhibited the CytOx systems of these animals, but this inhibition was offset by the additionto the CytOxassaymixtureofblood ofRj/iia or Ca!yptogena.Reduced sulfur compounds, sulfide, sulfite, and thiosulfate, were effective in stimulating ATP synthesis in homogenates of symbiont-containingtissues. The most effective reduced sulfur compound varied among the three symbioses.

https://www.jstor.org/stable/info/1541923

Adaptations to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism

Clumps of Bathymodiolus thermophilus were collected from three discrete areas at the ‘Rose Garden’ site on the Galapagos Rift using the deep submersible Alvin. Two mussel collections were made from the central Riftia mass, an area associated with very active venting, and three other collections were of two different peripheral mussel clumps. Before collection the clumps were extensively photographed and the water at two of the ‘microhabitats’ was analysed in situ for oxygen silica, sulfide and temperature. Sulfide levels of up to 300 μM were recorded at the central collection site, while the highest sulfide level recorded at the peripheral site assayed was 35 μM. Levels of RuBP carboxylase activity in the gills were significantly higher in mussels collected from the central ‘Riftia site’ than in either peripheral site. ATP sulfurylase was significantly higher in the gills of mussels from the central clump than in one of the peripheral clump collections. The chemical composition (% water, protein, carbohydrate, lipid and ash) and stable carbon isotope ratios (δ13C) of the mussels showed the same trends, with highest lipid and carbohydrate and the lowest water content and δ13C in the central site mussels. Similarly, the mussels from the central site were significantly depleted in stable nitrogen (δ15N) when compared with the peripheral site mussels. Variations between sites and tissues of the same animal may be indicative of differential utilization of inorganic or dissolved molecular nitrogen sources. The condition index (CI = soft tissue dry mass / internal shell volume) was similar for all animals collected at Rose Garden. The presence of a commensal polychaete, Branchipolynoe symmytilida, in the mantle cavity of the mussels was also correlated with the collection site, with the highest incidence of occurrence in the central clump. Levels of the enzyme RuBP carboxylase are quite variable in B. thermophilus and are on the average much lower (0.001 international units) than either Calyptogena magnifica (0.006 I.U.) or Riftia pachyptila (0.16 I.U.). We conclude that the mussels are able to thrive over a wider range of conditions than either C. magnifica or R. pachypila and that this is due to a lesser reliance on their symbiotic bacteria as a source of nutrition.

Microhabitat variation in the hydrothermal vent mussel, Bathymodiolus thermophilus, at the Rose Garden vent on the Galapagos Rift

A gutless clam, Solemya reidi, from sulfide-rich habitats has gills containing symbiotic, chemoautolithotrophic bacteria that are presumed to oxidize sulfide to provide a major energy source for the symbiosis. Sulfide oxidation was studied for S. reidi; activity of gill and foot extracts displayed Michaelis-Menten kinetics and was presumably due to sulfide oxidase enzymes. The activity of S. reidi gill extracts was protease sensitive and heat sensitive and was 10 to 20 times higher than in tissues from bivalves not living in sulfide-rich environments. The site of sulfide oxidation was studied by cytochemistry, 35S-sulfide autoradiography, cell fractionation methods, and by X-ray microanalysis. In gills of S. reidi, the sulfide-oxidizing activity was detected not in the symbiotic bacteria, but within organelles of the gill cells we have named sulfide oxidizing bodies. In foot tissue of S. reidi, sulfide oxidation activity was distributed diffusely throughout the superficial cell layers of the foot. The dis...

Sulfide oxidation occurs in the animal tissue of the gutless clam, solemya reidi

Respiration of plume tissue of the hydrothermal vent tube worm Riftia pachyptila is insensitive to sulfide poisoning in contrast to tissues of animals that do not inhabit vents. Permeability barriers may not be responsible for this insensitivity since plume homogenates are also resistant to sulfide poisoning. Cytochrome c oxidase of plume, however, is strongly inhibited by sulfide at concentrations less than 10 microM. Factors present in blood, but not in cytosol, prevent sulfide from inhibiting cytochrome c oxidase. Avoidance of sulfide poisoning of respiration in Riftia pachyptila thus appears to involve a blood-borne factor having a higher sulfide affinity than that of cytochrome c oxidase, with the result that appreciable amounts of free sulfide are prevented from accumulating in the blood and entering the intracellular compartment.

M. A. Powell

Papers

Hydrogen Sulfide Oxidation Is Coupled to Oxidative Phosphorylation in Mitochondria of Solemya reidi

Adaptations to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism

Microhabitat variation in the hydrothermal vent mussel, Bathymodiolus thermophilus, at the Rose Garden vent on the Galapagos Rift

Sulfide oxidation occurs in the animal tissue of the gutless clam, solemya reidi

Blood Components Prevent Sulfide Poisoning of Respiration of the Hydrothermal Vent Tube Worm Riftia pachyptila