Elemental sulfur reduction in the deep‐sea vent thermophile, <i>Thermovibrio ammonificans</i>

Jelen, Benjamin I.; Giovannelli, Donato; Falkowski, Paul G.; Vetriani, Costantino

doi:10.1111/1462-2920.14280

Cited by 19 publications

(17 citation statements)

References 74 publications

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“…All of these sulfur-reducing archaea lack a conventional sulfur reduction pathway. Therefore, we hypothesize that in elemental-sulfur/polysulfiderich environments, SQR-like proteins might catalyze the reduction of elemental sulfur/ polysulfide to H 2 S. A similar hypothesis has been proposed in a deep-sea thermophile, Thermovibrio ammonificans, after detection of the overexpression of SQR-like genes during sulfur respiration (68). While SQR-like proteins have not been shown to reversibly catalyze sulfide oxidation/reduction yet, there are precedents for reversible enzymes.…”

Section: Discussionsupporting

confidence: 55%

Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

et al. 2019

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Gulf of Mexico sediments harbor numerous hydrocarbon seeps associated with high sedimentation rates and thermal maturation of organic matter. These ecosystems host abundant and diverse microbial communities that directly or indirectly metabolize components of the emitted fluid. To investigate microbial function and activities in these ecosystems, metabolic potential (metagenomic) and gene expression (metatranscriptomic) analyses of two cold seep areas of the Gulf of Mexico were carried out. Seeps emitting biogenic methane harbored microbial communities dominated by archaeal anaerobic methane oxidizers of phylogenetic group 1 (ANME-1), whereas seeps producing fluids containing a complex mixture of thermogenic hydrocarbons were dominated by ANME-2 lineages. Metatranscriptome measurements in both communities indicated high levels of expression of genes for methane metabolism despite their distinct microbial communities and hydrocarbon composition. In contrast, the transcription level of sulfur cycle genes was quite different. In the thermogenic seep community, high levels of transcripts indicative of syntrophic anaerobic oxidation of methane (AOM) coupled to sulfate reduction were detected. This syntrophic partnership between the dominant ANME-2 and sulfate reducers potentially involves direct electron transfer through multiheme cytochromes. In the biogenic methane seep, genes from an ANME-1 lineage that are potentially involved in polysulfide reduction were highly expressed, suggesting a novel bacterium-independent anaerobic methane oxidation pathway coupled to polysulfide reduction. The observed divergence in AOM activities provides a new model for bacterium-independent AOM and emphasizes the variation that exists in AOM pathways between different ANME lineages.IMPORTANCECold seep sediments are complex and widespread marine ecosystems emitting large amounts of methane, a potent greenhouse gas, and other hydrocarbons. Within these sediments, microbial communities play crucial roles in production and degradation of hydrocarbons, modulating oil and gas emissions to seawater. Despite this ecological importance, our understanding of microbial functions and methane oxidation pathways in cold seep ecosystems is poor. Based on gene expression profiling of environmental seep sediment samples, the present work showed that (i) the composition of the emitted fluids shapes the microbial community in general and the anaerobic methanotroph community specifically and (ii) AOM by ANME-2 in this seep may be coupled to sulfate reduction byDeltaproteobacteriaby electron transfer through multiheme cytochromes, whereas AOM by ANME-1 lineages in this seep may involve a different, bacterium-independent pathway, coupling methane oxidation to elemental sulfur/polysulfide reduction.

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Section: Discussionsupporting

confidence: 55%

Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

et al. 2019

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“…recently also proposed a cytoplasmatic sulfur reduction mediated by an NSR‐like protein in a deep‐sea vent thermophile, Thermovibrio ammonificans , based on transcriptomic and proteomic analyses (Jelen et al ., 2018). T. ammonificans grows chemolithoautotrophically at optimal temperature of 75 °C and forms a deep branch within the phylum Aquificae (Jelen et al ., 2018). Prior to our study, cytoplasmic sulfur reduction was only reported in A. aeolicus and T. ammonificans , both of which are deep‐branched in bacterial phylogenetic tree and hyperthermophilic.…”

Section: Discussionmentioning

confidence: 99%

Elemental sulfur reduction by a deep‐sea hydrothermal vent CampylobacteriumSulfurimonassp.NW10

Wang

Jiang

et al. 2020

Environmental Microbiology

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Summary Sulfurimonas species (class Campylobacteria, phylum Campylobacterota) were globally distributed and especially predominant in deep‐sea hydrothermal environments. They were previously identified as chemolithoautotrophic sulfur‐oxidizing bacteria (SOB), whereas little is known about their potential in sulfur reduction. In this report, we found that the elemental sulfur reduction is quite common in different species of genus Sulfurimonas. To gain insights into the sulfur reduction mechanism, growth tests, morphology observation, as well as genomic and transcriptomic analyses were performed on a deep‐sea hydrothermal vent bacterium Sulfurimonas sp. NW10. Scanning electron micrographs and dialysis tubing tests confirmed that elemental sulfur reduction occurred without direct contact of cells with sulfur particles while direct access strongly promoted bacterial growth. Furthermore, we demonstrated that most species of Sulfurimonas probably employ both periplasmic and cytoplasmic polysulfide reductases, encoded by genes psrA1B1CDE and psrA2B2, respectively, to accomplish cyclooctasulfur reduction. This is the first report showing two different sulfur reduction pathways coupled to different energy conservations could coexist in one sulfur‐reducing microorganism, and demonstrates that most bacteria of Sulfurimonas could employ both periplasmic and cytoplasmic polysulfide reductases to perform cyclooctasulfur reduction. The capability of sulfur reduction coupling with hydrogen oxidation may partially explain the prevalenceof Sulfurimonas in deep‐sea hydrothermal vent environments.

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“…Sulfate is highly abundant on the current earth. Hence, sulfate reduction dominates reductive processes in the global sulfur cycle, although the reduction and disproportionation of the intermediate sulfur species, e.g., sulfur ( 7 , 8 ), sulfite ( 8 ), thiosulfate, and tetrathionate ( 9 , 10 ), could be significant in localized settings.…”

Section: Introductionmentioning

confidence: 99%

Microbial Diversity and Sulfur Cycling in an Early Earth Analogue: From Ancient Novelty to Modern Commonality

Hahn

Farag

Murphy

et al. 2022

mBio

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Elemental sulfur reduction in the deep‐sea vent thermophile, Thermovibrio ammonificans

Cited by 19 publications

References 74 publications

Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments

Elemental sulfur reduction by a deep‐sea hydrothermal vent CampylobacteriumSulfurimonassp.NW10

Microbial Diversity and Sulfur Cycling in an Early Earth Analogue: From Ancient Novelty to Modern Commonality

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