Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic
            <i>Campylobacterota</i>

Wang, Shasha; Jiang, Lijing; Xie, Shaobin; Alain, Karine; Wang, Zhaodi; Wang, Jun; Liu, Delin; Shao, Zongze

doi:10.1128/msystems.00954-22

Cited by 14 publications

(13 citation statements)

References 66 publications

(86 reference statements)

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“…In addition to the direct contact of cells to insoluble S 0 , a non-contact or cooperative mechanism (coexistence of contact and non-contact activation) could be involved in S 0 activation. In this study, we found that strain ST-419 growing via S 0 reduction did not require direct contact to S 0 , whereas cells growing via S 0 oxidation did require direct access ( Figure 5 ), which is consistent with our previous reports in other species of Sulfurovum and Sulfurimonas [ 34 , 75 ]. Thus, a mechanism of activation of S 0 without cell contact also likely exists.…”

Section: Discussionsupporting

confidence: 92%

“…Elemental sulfur is abundant in hydrothermal vents, and its associated catabolism by the dominant chemolithoautotrophic Campylobacterota remains poorly understood. The genus Sulfurovum has been confirmed as one of the most predominant members of deep-sea hydrothermal prokaryotic residents that support the unique chemoautotrophic ecosystem [ 37 ], and is strongly involved in the oxidation of reduced inorganic sulfur compounds [ 26 , 38 , 74 , 75 ]. In the present study, we investigated the mechanisms of cyclooctasulfur activation and metabolisms when it is used as an electron donor or acceptor during sulfur oxidation and reduction in the deep-sea hydrothermal vent bacterium S. indicum .…”

Section: Discussionmentioning

confidence: 99%

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Transcriptome Analysis of Cyclooctasulfur Oxidation and Reduction by the Neutrophilic Chemolithoautotrophic Sulfurovum indicum from Deep-Sea Hydrothermal Ecosystems

et al. 2023

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Chemolithoautotrophic Campylobacterota are widespread and predominant in worldwide hydrothermal vents, and they are key players in the turnover of zero-valence sulfur. However, at present, the mechanism of cyclooctasulfur activation and catabolism in Campylobacterota bacteria is not clearly understood. Here, we investigated these processes in a hydrothermal vent isolate named Sulfurovum indicum ST-419. A transcriptome analysis revealed that multiple genes related to biofilm formation were highly expressed during both sulfur oxidation and reduction. Additionally, biofilms containing cells and EPS coated on sulfur particles were observed by SEM, suggesting that biofilm formation may be involved in S0 activation in Sulfurovum species. Meanwhile, several genes encoding the outer membrane proteins of OprD family were also highly expressed, and among them, gene IMZ28_RS00565 exhibited significantly high expressions by 2.53- and 7.63-fold changes under both conditions, respectively, which may play a role in sulfur uptake. However, other mechanisms could be involved in sulfur activation and uptake, as experiments with dialysis bags showed that direct contact between cells and sulfur particles was not mandatory for sulfur reduction activity, whereas cell growth via sulfur oxidation did require direct contact. This indirect reaction could be ascribed to the role of H2S and/or other thiol-containing compounds, such as cysteine and GSH, which could be produced in the culture medium during sulfur reduction. In the periplasm, the sulfur-oxidation-multienzyme complexes soxABXY1Z1 and soxCDY2Z2 are likely responsible for thiosulfate oxidation and S0 oxidation, respectively. In addition, among the four psr gene clusters encoding polysulfide reductases, only psrA3B3C3 was significantly upregulated under the sulfur reduction condition, implying its essential role in sulfur reduction. These results expand our understanding of the interactions of Campylobacterota with the zero-valence sulfur and their adaptability to deep-sea hydrothermal environments.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Transcriptome Analysis of Cyclooctasulfur Oxidation and Reduction by the Neutrophilic Chemolithoautotrophic Sulfurovum indicum from Deep-Sea Hydrothermal Ecosystems

et al. 2023

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“…Cultivated species of the genus Desulfocapsa are strictly anaerobic and couple autotrophic growth to the disproportionation of intermediate oxidation‐state sulfur species (S 0 , sulfite, and thiosulfate) to form sulfide and sulfate (Finster et al, 1998, 2013; Frederiksen & Finster, 2003, 2004; Janssen et al, 1996; Poser et al, 2013). Recently, it was shown that several species of Sulfurovum from diverse natural environments carry out S 0 disproportionation in pure culture (Wang et al, 2023). It is therefore possible that Sulfurovum populations are also carrying out S 0 disproportionation at Frasassi, although their S 0 ‐disproportionating activity should be confirmed with laboratory studies.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, it was shown that several species of Sulfurovum from diverse natural environments carry out S 0 disproportionation in pure culture (Wang et al, 2023). It is therefore possible that Sulfurovum populations are also carrying out S 0 disproportionation at Frasassi, although their S 0 -disproportionating activity should be confirmed with laboratory studies.…”

Section: S 0 Reduction and Disproportionation In Anoxic Sedimentsmentioning

confidence: 99%

Sulfur disproportionating microbial communities in a dynamic, microoxic‐sulfidic karst system

Aronson,

Clark,

LaRowe

et al. 2023

Geobiology

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Biogeochemical sulfur cycling in sulfidic karst systems is largely driven by abiotic and biological sulfide oxidation, but the fate of elemental sulfur (S0) that accumulates in these systems is not well understood. The Frasassi Cave system (Italy) is intersected by a sulfidic aquifer that mixes with small quantities of oxygen‐rich meteoric water, creating Proterozoic‐like conditions and supporting a prolific ecosystem driven by sulfur‐based chemolithoautotrophy. To better understand the cycling of S0 in this environment, we examined the geochemistry and microbiology of sediments underlying widespread sulfide‐oxidizing mats dominated by Beggiatoa. Sediment populations were dominated by uncultivated relatives of sulfur cycling chemolithoautotrophs related to Sulfurovum, Halothiobacillus, Thiofaba, Thiovirga, Thiobacillus, and Desulfocapsa, as well as diverse uncultivated anaerobic heterotrophs affiliated with Bacteroidota, Anaerolineaceae, Lentimicrobiaceae, and Prolixibacteraceae. Desulfocapsa and Sulfurovum populations accounted for 12%–26% of sediment 16S rRNA amplicon sequences and were closely related to isolates which carry out autotrophic S0 disproportionation in pure culture. Gibbs energy (∆Gr) calculations revealed that S0 disproportionation under in situ conditions is energy yielding. Microsensor profiles through the mat‐sediment interface showed that Beggiatoa mats consume dissolved sulfide and oxygen, but a net increase in acidity was only observed in the sediments below. Together, these findings suggest that disproportionation is an important sink for S0 generated by microbial sulfide oxidation in this oxygen‐limited system and may contribute to the weathering of carbonate rocks and sediments in sulfur‐rich environments.

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“…Cultivated species of the genus Desulfocapsa are strictly anaerobic and couple autotrophic growth to the disproportionation of intermediate oxidation state sulfur species (S 0 , sulfite, and thiosulfate) to form sulfide and sulfate (Janssen et al ., 1996; Finster et al ., 1998, 2013; Frederiksen & Finster, 2003, 2004; Poser et al ., 2013). Recently it was shown that several species of Sulfurovum from diverse natural environments carry out S 0 disproportionation in pure culture (Wang et al ., 2022). It is therefore possible that Sulfurovum populations are also carrying out S 0 disproportionation at Frasassi, although their S 0 -disproportionating activity should be confirmed with laboratory studies.…”

Section: Discussionmentioning

confidence: 99%

Sulfur disproportionating microbial communities in a dynamic, microoxic-sulfidic karst system

Aronson

Clark

LaRowe

et al. 2023

Preprint

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Biogeochemical sulfur cycling in sulfidic karst systems is largely driven by abiotic and biological sulfide oxidation, but the fate of elemental sulfur (S0) that accumulates in these systems is not well understood. The Frasassi Cave system (Italy) is intersected by a sulfidic aquifer that mixes with small quantities of oxygen-rich meteoric water, creating Proterozoic-like conditions and supporting a prolific ecosystem driven by sulfur-based chemolithoautotrophy. To better understand the cycling of S0in this environment, we examined the geochemistry and microbiology of sediments underlying widespread sulfide-oxidizing mats dominated byBeggiatoa. Sediment populations were dominated by uncultivated relatives of sulfur cycling chemolithoautotrophs related toSulfurovum,Halothiobacillus,Thiofaba,Thiovirga,Thiobacillus, andDesulfocapsa, as well as diverse uncultivated anaerobic heterotrophs affiliated with Bacteroidota, Anaerolineaceae, Lentimicrobiaceae, and Prolixibacteraceae.DesulfocapsaandSulfurovumpopulations accounted for 12-26% of sediment 16S rRNA amplicon sequences and were closely related to isolates which carry out autotrophic S0disproportionation in pure culture. Gibbs energy (ΔGr) calculations revealed that S0disproportionation under in situ conditions is energy yielding. Microsensor profiles through the mat-sediment interface showed thatBeggiatoamats consume dissolved sulfide and oxygen, but a net increase in acidity was only observed in the sediments below. Together, these findings suggest that disproportionation is an important sink for S0generated by microbial sulfide oxidation in this oxygen-limited system and may contribute to the weathering of carbonate rocks and sediments in sulfur-rich environments.

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Disproportionation of Inorganic Sulfur Compounds by Mesophilic Chemolithoautotrophic Campylobacterota

Abstract: The phylum Campylobacterota , notably represented by the genera Sulfurimonas and Sulfurovum , is ubiquitous and predominant in deep-sea hydrothermal systems. It is well-known to be the major chemolithoautotrophic sulfur-oxidizing group in these habitats.

Cited by 14 publications

References 66 publications

Transcriptome Analysis of Cyclooctasulfur Oxidation and Reduction by the Neutrophilic Chemolithoautotrophic Sulfurovum indicum from Deep-Sea Hydrothermal Ecosystems

Transcriptome Analysis of Cyclooctasulfur Oxidation and Reduction by the Neutrophilic Chemolithoautotrophic Sulfurovum indicum from Deep-Sea Hydrothermal Ecosystems

Sulfur disproportionating microbial communities in a dynamic, microoxic‐sulfidic karst system

Sulfur disproportionating microbial communities in a dynamic, microoxic-sulfidic karst system

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