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Direct interspecies electron transfer enables anaerobic oxidation of sulfide to elemental sulfur coupled with CO₂-reducing methanogenesis.

ABSTRACT: Electric syntrophy between fatty acid oxidizers and methanogens through direct interspecies electron transfer (DIET) is essential for balancing acidogenesis and methanogenesis in anaerobic digestion. Promoting DIET using electrically conductive additives proved effective in enhancing methanogenesis; however, its possibility to affect other microbial redox reactions in methanogenic systems has been little studied. This study provides the first confirmation of the electro-syntrophic coupling of sulfide oxidation to S⁰ with CO₂-reducing methanogenesis in sulfur-rich methanogenic cultures supplemented with conductive magnetite (100-700-nm particle size). The H₂S content in biogas, initially exceeding 5000 ppmv, decreased to below 1 ppmv along with an accumulation of extracellular S⁰ (60-70 mg/L; initially <1 mg/L) at a magnetite dose of 20 mM Fe, while there were no significant changes in methane yield. A comprehensive polyphasic approach demonstrated that the S⁰ formation occurs through electro-syntrophic oxidation of sulfide coupled with CO₂-reducing methanogenesis, involving Methanothrix as the dominant methanogen.

SUBMITTER: Jung H

PROVIDER: S-EPMC10448109 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Direct interspecies electron transfer enables anaerobic oxidation of sulfide to elemental sulfur coupled with CO<sub>2</sub>-reducing methanogenesis.

Jung Heejung H Yu Hyeonjung H Lee Changsoo C

iScience 20230801 9

Electric syntrophy between fatty acid oxidizers and methanogens through direct interspecies electron transfer (DIET) is essential for balancing acidogenesis and methanogenesis in anaerobic digestion. Promoting DIET using electrically conductive additives proved effective in enhancing methanogenesis; however, its possibility to affect other microbial redox reactions in methanogenic systems has been little studied. This study provides the first confirmation of the electro-syntrophic coupling of su ...[more]

PMID: 37636045

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Project description:A thermophilic filamentous anoxygenic photosynthetic bacterium, Chloroflexus aggregans, is widely distributed in neutral to slightly alkaline hot springs. Sulfide has been suggested as an electron donor for autotrophic growth in microbial mats dominated with C. aggregans, but remarkable photoautotrophic growth of isolated C. aggregans has not been observed with sulfide as the sole electron source. From the idea that sulfide is oxidized to elemental sulfur by C. aggregans and the accumulation of elemental sulfur may have an inhibitory effect for the growth, the effects of an elemental sulfur-disproportionating bacterium that consumes elemental sulfur was examined on the autotrophic growth of C. aggregans, strain NA9-6, isolated from Nakabusa hot spring. A sulfur-disproportionating bacterium, Caldimicrobium thiodismutans strain TF1, also isolated from Nakabusa hot spring was co-cultured with C. aggregans. C. aggregans and C. thiodismutans were successfully co-cultured in a medium containing thiosulfate as the sole electron source and bicarbonate as the sole carbon source. Quantitative conversion of thiosulfate to sulfate and a small transient accumulation of sulfide was observed in the co-culture. Then the electron source of the established co-culture was changed from thiosulfate to sulfide, and the growth of C. aggregans and C. thiodismutans was successfully observed with sulfide as the sole electron donor for the autotrophic growth of the co-culture. During the cultivation in the light, simultaneous consumption and accumulation of sulfide and sulfate, respectively, were observed, accompanied with the increase of cellular DNAs of both species. C. thiodismutans likely works as an elemental sulfur scavenger for C. aggregans, and C. aggregans seems to work as a sulfide scavenger for C. thiodismutans. These results suggest that C. aggregans grows autotrophically with sulfide as the electron donor in the co-culture with C. thiodismutans, and the consumption of elemental sulfur by C. thiodismutans enabled the continuous growth of the C. aggregans in the symbiotic system. This study shows a novel symbiotic relationship between a sulfide-oxidizing photoautotroph and an elemental sulfur-disproportionating chemolithoautotroph via cooperative dissimilatory sulfide oxidation to sulfate.

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Direct interspecies electron transfer enables anaerobic oxidation of sulfide to elemental sulfur coupled with CO₂-reducing methanogenesis.

Publications

Direct interspecies electron transfer enables anaerobic oxidation of sulfide to elemental sulfur coupled with CO<sub>2</sub>-reducing methanogenesis.

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Direct interspecies electron transfer enables anaerobic oxidation of sulfide to elemental sulfur coupled with CO2-reducing methanogenesis.

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Direct interspecies electron transfer enables anaerobic oxidation of sulfide to elemental sulfur coupled with CO<sub>2</sub>-reducing methanogenesis.

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OmicsDI is part of the ELIXIR infrastructure

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Direct interspecies electron transfer enables anaerobic oxidation of sulfide to elemental sulfur coupled with CO₂-reducing methanogenesis.