Toxicity of hydrogen sulfide toward sulfate-reducing bacteria Desulfovibrio piger Vib-7

Hydrogen sulfide (H(2)S) is present in the lumen of the human large intestine at millimolar concentrations. However, the concentration of free (unbound) sulfide is in the micromolar range due to a large capacity of fecal components to bind the sulfide. H(2)S can be produced by the intestinal microbiota from alimentary and endogenous sulfur-containing compounds including amino acids. At excessive concentration, H(2)S is known to severely inhibit cytochrome c oxidase, the terminal oxidase of the mitochondrial electron transport chain, and thus mitochondrial oxygen (O(2)) consumption. However, the concept that sulfide is simply a metabolic troublemaker toward colonic epithelial cells has been challenged by the discovery that micromolar concentration of H(2)S is able to increase the cell respiration and to energize mitochondria allowing these cells to detoxify and to recover energy from luminal sulfide. The main product of H(2)S metabolism by the colonic mucosa is thiosulfate. The enzymatic activities involved in sulfide oxidation by the colonic epithelial cells appear to be sulfide quinone oxidoreductase considered as the first and rate-limiting step followed presumably by the action of sulfur dioxygenase and rhodanese. From clinical studies with human volunteers and experimental works with rodents, it appears that H(2)S can exert mostly pro- but also anti-inflammatory effects on the colonic mucosa. From the available data, it is tempting to propose that imbalance between the luminal concentration of free sulfide and the capacity of colonic epithelial cells to metabolize this compound will result in an impairment of the colonic epithelial cell O(2) consumption with consequences on the process of mucosal inflammation. In addition, endogenously produced sulfide is emerging as a prosecretory neuromodulator and as a relaxant agent toward the intestinal contractibility. Lastly, sulfide has been recently described as an agent involved in nociception in the large intestine although, depending on the experimental design, both pro- and anti-nociceptive effects have been reported.

The aetiology of ulcerative colitis is uncertain but may relate to environmental factors in genetically predisposed individuals. Sulphate-reducing bacteria (SRB) have been implicated through the harmful effects of hydrogen sulphide, a by-product of their respiration. Hydrogen sulphide is freely permeable to cell membranes and inhibits butyrate. This review examines the available evidence relating to SRB as a possible cause of ulcerative colitis. A literature search was conducted using the PubMed database and search terms 'sulphate reducing bacteria', 'hydrogen sulphide', 'ulcerative colitis', 'mucous gel layer' and 'trans-sulphuration'. Search results were scrutinized and 113 pertinent full-text articles were selected for review. Collected data related to hydrogen sulphide metabolism, SRB respiration, mucous gel layer composition and their association with ulcerative colitis. There is evidence to implicate SRB as an environmental factor in ulcerative colitis. More sophisticated mucosal dissection and molecular techniques using bacteria-directed probes are required to determine an association definitively.

Many aquatic animal species can survive sulfide exposure to some extent through oxidation of the sulfide, which results mainly in thiosulfate. In several species, sulfide oxidation is localized in the mitochondria and is accompanied by ATP synthesis. In addition, blood-based and intracellular compounds can augment sulfide oxidation. The formation of thiosulfate requires oxygen, which results in an increase in oxygen consumption of some species. If not all sulfide is detoxified, cytochrome C oxidase is inhibited. Under these conditions, a sulfide-dependent anaerobic energy metabolism commences.