Evolution of glutathione metabolism in phototrophic microorganisms

Fahey, Robert C.; Buschbacher, Ralph M.; Newton, Gerald L.

doi:10.1007/bf02422045

Cited by 10 publications

(16 citation statements)

References 17 publications

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“…An obligatory phototrophic representative of larger, strictly anaerobic Chromatium species, C. buderi (ATCC 25588), was found to produce GASSH at levels similar to those of C. gracile and C. vinosum when grown on sulfide medium ( Table 1). The total level of production of GASH and GASSH by Chromatium species varies from 0.66 to 1.7 mol g Ϫ1 of residual dry weight and is slightly lower than, but comparable to, the production of GSH (0.4 to 24 mol g Ϫ1 of residual dry weight) by most cyanobacteria and other purple bacteria (9). The production of GASH thus appears to be fairly widespread among Chromatium species of varied metabolic capacity.…”

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confidence: 86%

“…Among prokaryotes, GSH production is restricted almost entirely to the cyanobacteria and the purple bacteria (9,20), the former being oxygenic phototrophs and the latter including bacteria responsible for the evolution of pathways involved in mitochondrial oxidative phosphorylation (6,13). GSH metabolism appears to have been introduced into eukaryotes during the endosymbiotic processes that gave rise to mitochondria and chloroplasts (11,21,24).…”

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confidence: 99%

“…However, it is difficult to understand how GSH production could have evolved and become uniformly distributed among cyanobacteria and purple bacteria after the appearance of oxygenic photosynthesis; a more likely scenario is that GSH metabolism was present in an anaerobic ancestor of the cyanobacteria and purple bacteria, in which it served a different function (12). The report of GSH production by the anaerobic sulfur phototroph Chromatium vinosum (9) and of the presence of a GSH reductase in this organism (7) suggested that Chromatium spp. might be suitable organisms in which to search for an anaerobic function for GSH.…”

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Glutathione amide and its perthiol in anaerobic sulfur bacteria

et al. 1996

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Chromatium species produced the novel biological thiol glutathione amide, ␥-L-glutamyl-L-cysteinylglycine amide (GASH), when grown photoheterotrophically. GASH was largely converted to the corresponding perthiol during photoautotrophic growth on sulfide, suggesting that GASH may have a function in anaerobic sulfide metabolism. This unprecedented form of glutathione metabolism was probably present in anaerobic ancestors of modern cyanobacteria and purple bacteria.Interest in glutathione (GSH) metabolism has undergone explosive growth during the past two decades as evidence has accumulated documenting its important role in protecting animal cells against the toxicity of oxygen and its by-products (5,8,12,17,18,23,27,29). Among prokaryotes, GSH production is restricted almost entirely to the cyanobacteria and the purple bacteria (9, 20), the former being oxygenic phototrophs and the latter including bacteria responsible for the evolution of pathways involved in mitochondrial oxidative phosphorylation (6,13). GSH metabolism appears to have been introduced into eukaryotes during the endosymbiotic processes that gave rise to mitochondria and chloroplasts (11,21,24). The association between the evolution of GSH metabolism and that of oxygenic photosynthesis and oxygen-dependent respiratory metabolism is consistent with GSH's role as a protective antioxidant. However, it is difficult to understand how GSH production could have evolved and become uniformly distributed among cyanobacteria and purple bacteria after the appearance of oxygenic photosynthesis; a more likely scenario is that GSH metabolism was present in an anaerobic ancestor of the cyanobacteria and purple bacteria, in which it served a different function (12). The report of GSH production by the anaerobic sulfur phototroph Chromatium vinosum (9) and of the presence of a GSH reductase in this organism (7) suggested that Chromatium spp. might be suitable organisms in which to search for an anaerobic function for GSH. We show here that Chromatium spp. do not, in fact, produce GSH but instead produces two novel GSH derivatives whose structure and variation in content with growth conditions indicate that these GSH derivatives may be involved in anaerobic sulfide metabolism.C. gracile (DSM 1712) was grown photoheterotrophically on the medium of Arnon et al. (2) supplemented with NaCl (20 g/liter). Cells were extracted in 50% acetonitrile-water at 60ЊC in the presence of monobromobimane (mBBr) to produce fluorescent bimane derivatives (RSmB) which were analyzed by high-performance liquid chromatography (HPLC; Fig. 1A) as detailed elsewhere (10). No GSH derivative (GSmB) was detected, showing that GSH is not produced in significant amounts, but two unknown thiol derivatives, 2U9 and 2U13 (for HPLC method 2, Unknown, x-min retention time), were observed which could not be assigned to any of the common biological thiols used as standards (10). A full description of HPLC methods 1 and 2 and the elution times for the mBBr derivatives of common thiols has been published ...

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confidence: 86%

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Glutathione amide and its perthiol in anaerobic sulfur bacteria

et al. 1996

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“…Glutathione (GSH) is considered to play a key role in protecting cells against oxygen toxicity, but its production among prokaryotes appears to be largely restricted to the cyanobacteria and the purple bacteria (4,5,17,19). Most of the bacteria that lack glutathione, including many strictly aerobic species, produce other low-molecular-weight thiols, and we have sought to determine whether one or more of these thiols might play a role analogous to that of GSH.…”

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Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes

et al. 1996

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Mycothiol [2-(N-acetylcysteinyl)amido-2-deoxy-␣-D-glucopyranosyl-(131)-myo-inositol] (MSH. Since this novel thiol is more resistant than glutathione to heavy-metal ion-catalyzed oxidation, it seems likely to be the antioxidant thiol used by aerobic gram-positive bacteria that do not produce glutathione (GSH). In the present study we sought to define the spectrum of organisms that produce MSH. GSH was absent in all actinomycetes and some of the other gram-positive bacteria studied. Surprisingly, the streptococci and enterococci contained GSH, and some strains appeared to synthesize it rather than import it from the growth medium. MSH was found at significant levels in most actinomycetes examined. Among the actinobacteria four Micrococcus species produced MSH, but MSH was not found in representatives of the Arthrobacter, Agromyces, or Actinomyces genera. Of the nocardioforms examined, Nocardia, Rhodococcus, and Mycobacteria spp. all produced MSH. In addition to the established production of MSH by streptomycetes, we found that Micromonospora, Actinomadura, and Nocardiopsis spp. also synthesized MSH. Mycothiol production was not detected in Propionibacterium acnes or in representative species of the Listeria, Staphylococcus, Streptococcus, Enterococcus, Bacillus, and Clostridium genera. Examination of representatives of the cyanobacteria, purple bacteria, and spirochetes also gave negative results, as did tests of rat liver, bonito, Candida albicans, Neurospora crassa, and spinach leaves. The results, which indicate that MSH production is restricted to the actinomycetes, could have significant implications for the detection and treatment of infections with actinomycetes, especially those caused by mycobacteria.

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“…zooplankton, fish fecal pellets) (Montani and Okaichi 19 8 5). Bacteria, including heterotrophic, aerobic, Gram-negative eubacteria also contain GSH and may contribute to the observed distributions (Fahey and Newton 1983;Fahey et al in press).…”

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Particulate thiols in coastal waters: The effect of light and nutrients on their planktonic production

Matrai

Vetter

1988

Limnology & Oceanography

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Reduced sulfur compounds of low molecular weight, mainly particulate glutathione, were present in concentrations up to 600 pM in Saanich Inlet and off southern California. The vertical distributions of particulate glutathione (PGSH) in Saanich Inlet showed a subsurface maximum and decreased with depth in close correspondence with chlorophyll profiles. As with other measures of phytoplankton standing stock, PGSH decreased offshore in the Southern California Bight. In response to exposure to lower than ambient light levels, PGSH decreased in samples after 24‐h, on‐deck incubations except when the ambient nitrate concentration was high. Nitrate enrichment experiments, however, did not lead to enhanced PGSH production in offshore samples that were initially low in nitrate. Diel changes in PGSH were calculated to represent 0.5–4.5% of the corresponding calculated change in total particulate sulfur.

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Evolution of glutathione metabolism in phototrophic microorganisms

Cited by 10 publications

References 17 publications

Glutathione amide and its perthiol in anaerobic sulfur bacteria

Glutathione amide and its perthiol in anaerobic sulfur bacteria

Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes

Particulate thiols in coastal waters: The effect of light and nutrients on their planktonic production

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