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21 pages, 4549 KiB

Open AccessArticle

Impact of Reactive Sulfur Species on Entamoeba histolytica: Modulating Viability, Motility, and Biofilm Degradation Capacity

by Jun Ye, Talal Salti, Eva Zanditenas, Meirav Trebicz-Geffen, Moran Benhar and Serge Ankri

Antioxidants 2024, 13(2), 245; https://doi.org/10.3390/antiox13020245 - 19 Feb 2024

Viewed by 1012

Abstract

Reactive sulfur species (RSS) like hydrogen sulfide (H₂S) and cysteine persulfide (Cys-SSH) emerged as key signaling molecules with diverse physiological roles in the body, depending on their concentration and the cellular environment. While it is known that H₂S and [...] Read more.

Reactive sulfur species (RSS) like hydrogen sulfide (H₂S) and cysteine persulfide (Cys-SSH) emerged as key signaling molecules with diverse physiological roles in the body, depending on their concentration and the cellular environment. While it is known that H₂S and Cys-SSH are produced by both colonocytes and by the gut microbiota through sulfur metabolism, it remains unknown how these RSS affect amebiasis caused by Entamoeba histolytica, a parasitic protozoan that can be present in the human gastrointestinal tract. This study investigates H₂S and Cys-SSH’s impact on E. histolytica physiology and explores potential therapeutic implications. Exposing trophozoites to the H₂S donor, sodium sulfide (Na₂S), or to Cys-SSH led to rapid cytotoxicity. A proteomic analysis of Cys-SSH-challenged trophozoites resulted in the identification of >500 S-sulfurated proteins, which are involved in diverse cellular processes. Functional assessments revealed inhibited protein synthesis, altered cytoskeletal dynamics, and reduced motility in trophozoites treated with Cys-SSH. Notably, cysteine proteases (CPs) were significantly inhibited by S-sulfuration, affecting their bacterial biofilm degradation capacity. Immunofluorescence microscopy confirmed alterations in actin dynamics, corroborating the proteomic findings. Thus, our study reveals how RSS perturbs critical cellular functions in E. histolytica, potentially influencing its pathogenicity and interactions within the gut microbiota. Understanding these molecular mechanisms offers novel insights into amebiasis pathogenesis and unveils potential therapeutic avenues targeting RSS-mediated modifications in parasitic infections. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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21 pages, 5489 KiB

Open AccessArticle

In the Alphaproteobacterium Hyphomicrobium denitrificans SoxR Serves a Sulfane Sulfur-Responsive Repressor of Sulfur Oxidation

by Jingjing Li, Kaya Törkel, Julian Koch, Tomohisa Sebastian Tanabe, Hsun Yun Hsu and Christiane Dahl

Antioxidants 2023, 12(8), 1620; https://doi.org/10.3390/antiox12081620 - 16 Aug 2023

Viewed by 1010

Abstract

In organisms that use reduced sulfur compounds as alternative or additional electron donors to organic compounds, transcriptional regulation of genes for enzymes involved in sulfur oxidation is needed to adjust metabolic flux to environmental conditions. However, little is known about the sensing and [...] Read more.

In organisms that use reduced sulfur compounds as alternative or additional electron donors to organic compounds, transcriptional regulation of genes for enzymes involved in sulfur oxidation is needed to adjust metabolic flux to environmental conditions. However, little is known about the sensing and response to inorganic sulfur compounds such as thiosulfate in sulfur-oxidizing bacteria. In the Alphaproteobacterium Hyphomicrobium denitrificans, one strategy is the use of the ArsR–SmtB-type transcriptional regulator SoxR. We show that this homodimeric repressor senses sulfane sulfur and that it is crucial for the expression not only of sox genes encoding the components of a truncated periplasmic thiosulfate-oxidizing enzyme system but also of several other sets of genes for enzymes of sulfur oxidation. DNA binding and transcriptional regulatory activity of SoxR are controlled by polysulfide-dependent cysteine modification. The repressor uses the formation of a sulfur bridge between two conserved cysteines as a trigger to bind and release DNA and can also form a vicinal disulfide bond to orchestrate a response to oxidizing conditions. The importance of the sulfur bridge forming cysteines was confirmed by site-directed mutagenesis, mass spectrometry, and gel shift assays. In vivo, SoxR interacts directly or indirectly with a second closely related repressor, sHdrR. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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10 pages, 1736 KiB

Open AccessCommunication

Thioredoxin-2 Regulates SqrR-Mediated Polysulfide-Responsive Transcription via Reduction of a Polysulfide Link in SqrR

by Takayuki Shimizu, Masaru Hashimoto and Tatsuru Masuda

Antioxidants 2023, 12(3), 699; https://doi.org/10.3390/antiox12030699 - 11 Mar 2023

Cited by 1 | Viewed by 1211

Abstract

Polysulfide plays an essential role in controlling various physiological activities in almost all organisms. We recently investigated the impact of polysulfide metabolic enzymes on the temporal dynamics of cellular polysulfide speciation and transcriptional regulation by the polysulfide-responsive transcription factor SqrR in Rhodobacter capsulatus [...] Read more.

Polysulfide plays an essential role in controlling various physiological activities in almost all organisms. We recently investigated the impact of polysulfide metabolic enzymes on the temporal dynamics of cellular polysulfide speciation and transcriptional regulation by the polysulfide-responsive transcription factor SqrR in Rhodobacter capsulatus. However, how the polysulfidation of thiol groups in SqrR is reduced remains unclear. In the present study, we examined the reduction of polysulfidated thiol residues by the thioredoxin system. TrxC interacted with SqrR in vitro and reduced the polysulfide crosslink between two cysteine residues in SqrR. Furthermore, we found that exogenous sulfide-induced SqrR de-repression during longer culture times is maintained upon disruption of the trxC gene. These results establish a novel signaling pathway in SqrR-mediated polysulfide-induced transcription, by which thioredoxin-2 restores SqrR to a transcriptionally repressed state via the reduction of polysulfidated thiol residues. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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22 pages, 3519 KiB

Open AccessArticle

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

by Shasha Wang, Lijing Jiang, Liang Cui, Karine Alain, Shaobin Xie and Zongze Shao

Antioxidants 2023, 12(3), 627; https://doi.org/10.3390/antiox12030627 - 03 Mar 2023

Cited by 3 | Viewed by 1786

Abstract

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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17 pages, 5944 KiB

Open AccessArticle

The Transcriptional Repressor PerR Senses Sulfane Sulfur by Cysteine Persulfidation at the Structural Zn²⁺ Site in Synechococcus sp. PCC7002

by Daixi Liu, Hui Song, Yuanning Li, Ranran Huang, Hongyue Liu, Kunxian Tang, Nianzhi Jiao and Jihua Liu

Antioxidants 2023, 12(2), 423; https://doi.org/10.3390/antiox12020423 - 09 Feb 2023

Cited by 2 | Viewed by 1758

Abstract

Cyanobacteria can perform both anoxygenic and oxygenic photosynthesis, a characteristic which ensured that these organisms were crucial in the evolution of the early Earth and the biosphere. Reactive oxygen species (ROS) produced in oxygenic photosynthesis and reactive sulfur species (RSS) produced in anoxygenic [...] Read more.

Cyanobacteria can perform both anoxygenic and oxygenic photosynthesis, a characteristic which ensured that these organisms were crucial in the evolution of the early Earth and the biosphere. Reactive oxygen species (ROS) produced in oxygenic photosynthesis and reactive sulfur species (RSS) produced in anoxygenic photosynthesis are closely related to intracellular redox equilibrium. ROS comprise superoxide anion (O₂^●−), hydrogen peroxide (H₂O₂), and hydroxyl radicals (^●OH). RSS comprise H₂S and sulfane sulfur (persulfide, polysulfide, and S₈). Although the sensing mechanism for ROS in cyanobacteria has been explored, that of RSS has not been elucidated. Here, we studied the function of the transcriptional repressor PerR in RSS sensing in Synechococcus sp. PCC7002 (PCC7002). PerR was previously reported to sense ROS; however, our results revealed that it also participated in RSS sensing. PerR repressed the expression of prxI and downregulated the tolerance of PCC7002 to polysulfide (H₂S_n). The reporter system indicated that PerR sensed H₂S_n. Cys¹²¹ of the Cys4:Zn²⁺ site, which contains four cysteines (Cys¹²¹, Cys¹²⁴, Cys¹⁶⁰, and Cys¹⁶³) bound to one zinc atom, could be modified by H₂S_n to Cys¹²¹-SSH, as a result of which the zinc atom was released from the site. Moreover, Cys¹⁹ could also be modified by polysulfide to Cys¹⁹-SSH. Thus, our results reveal that PerR, a representative of the Cys₄ zinc finger proteins, senses H₂S_n. Our findings provide a new perspective to explore the adaptation strategy of cyanobacteria in Proterozoic and contemporary sulfurization oceans. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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12 pages, 6375 KiB

Open AccessArticle

The Pleiotropic Regulator AdpA Regulates the Removal of Excessive Sulfane Sulfur in Streptomyces coelicolor

by Ting Lu, Qingda Wang, Qun Cao, Yongzhen Xia, Luying Xun and Huaiwei Liu

Antioxidants 2023, 12(2), 312; https://doi.org/10.3390/antiox12020312 - 29 Jan 2023

Viewed by 1549

Abstract

Reactive sulfane sulfur (RSS), including persulfide, polysulfide, and elemental sulfur (S₈), has important physiological functions, such as resisting antibiotics in Pseudomonas aeruginosa and Escherichia coli and regulating secondary metabolites production in Streptomyces spp. However, at excessive levels it is toxic. Streptomyces [...] Read more.

Reactive sulfane sulfur (RSS), including persulfide, polysulfide, and elemental sulfur (S₈), has important physiological functions, such as resisting antibiotics in Pseudomonas aeruginosa and Escherichia coli and regulating secondary metabolites production in Streptomyces spp. However, at excessive levels it is toxic. Streptomyces cells may use known enzymes to remove extra sulfane sulfur, and an unknown regulator is involved in the regulation of these enzymes. AdpA is a multi-functional transcriptional regulator universally present in Streptomyces spp. Herein, we report that AdpA was essential for Streptomyces coelicolor survival when facing external RSS stress. AdpA deletion also resulted in intracellular RSS accumulation. Thioredoxins and thioredoxin reductases were responsible for anti-RSS stress via reducing RSS to gaseous hydrogen sulfide (H₂S). AdpA directly activated the expression of these enzymes at the presence of excess RSS. Since AdpA and thioredoxin systems are widely present in Streptomyces, this finding unveiled a new mechanism of anti-RSS stress by these bacteria. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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22 pages, 4254 KiB

Open AccessArticle

The Sulfide-Responsive SqrR/BigR Homologous Regulator YgaV of Escherichia coli Controls Expression of Anaerobic Respiratory Genes and Antibiotic Tolerance

by Rajalakshmi Balasubramanian, Koichi Hori, Takayuki Shimizu, Shingo Kasamatsu, Kae Okamura, Kan Tanaka, Hideshi Ihara and Shinji Masuda

Antioxidants 2022, 11(12), 2359; https://doi.org/10.3390/antiox11122359 - 28 Nov 2022

Cited by 4 | Viewed by 4632

Abstract

Compositions and activities of bacterial flora in the gastrointestinal tract significantly influence the metabolism, health, and disease of host humans and animals. These enteric bacteria can switch between aerobic and anaerobic growth if oxygen tension becomes limited. Interestingly, the switching mechanism is important [...] Read more.

Compositions and activities of bacterial flora in the gastrointestinal tract significantly influence the metabolism, health, and disease of host humans and animals. These enteric bacteria can switch between aerobic and anaerobic growth if oxygen tension becomes limited. Interestingly, the switching mechanism is important for preventing reactive oxygen species (ROS) production and antibiotic tolerance. Studies have also shown that intracellular and extracellular sulfide molecules are involved in this switching control, although the mechanism is not fully clarified. Here, we found that YgaV, a sulfide-responsive transcription factor SqrR/BigR homolog, responded to sulfide compounds in vivo and in vitro to control anaerobic respiratory gene expression. YgaV also responded to H₂O₂ scavenging in the enteric bacterium Escherichia coli. Although the wild-type (WT) showed increased antibiotic tolerance under H₂S-atmospheric conditions, the ygaV mutant did not show such a phenotype. Additionally, antibiotic sensitivity was higher in the mutant than in the WT of both types in the presence and absence of exogenous H₂S. These results, therefore, indicated that YgaV-dependent transcriptional regulation was responsible for maintaining redox homeostasis, ROS scavenging, and antibiotic tolerance. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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12 pages, 2314 KiB

Open AccessArticle

Sulfane Sulfur Is an Intrinsic Signal for the Organic Peroxide Sensor OhrR of Pseudomonas aeruginosa

by Huangwei Xu, Guanhua Xuan, Huaiwei Liu, Honglei Liu, Yongzhen Xia and Luying Xun

Antioxidants 2022, 11(9), 1667; https://doi.org/10.3390/antiox11091667 - 26 Aug 2022

Cited by 3 | Viewed by 1591

Abstract

Sulfane sulfur, including organic persulfide and polysulfide, is a normal cellular component, and its level varies during growth. It is emerging as a signaling molecule in bacteria, regulating the gene regulator MarR in Escherichia coli, MexR in Pseudomonas aeruginosa, and MgrA [...] Read more.

Sulfane sulfur, including organic persulfide and polysulfide, is a normal cellular component, and its level varies during growth. It is emerging as a signaling molecule in bacteria, regulating the gene regulator MarR in Escherichia coli, MexR in Pseudomonas aeruginosa, and MgrA of Staphylococcus aureus. They are MarR-family regulators and are often repressors for multiple antibiotic resistance genes. Here, we report that another MarR-type regulator OhrR that represses the expression of itself and a thiol peroxidase gene ohr in P. aeruginosa PAO1 also responded to sulfane sulfur. PaOhrR formed disulfide bonds between three Cys residues within a dimer after polysulfide treatment. The modification reduced its affinity to its cognate DNA binding site. An Escherichia coli reporter system, in which mKate was under the repression of OhrR, showed that PaOhrR derepressed its controlled gene when polysulfide was added, whereas the mutant PaOhrR with two Cys residues changed to Ser residues did not respond to polysulfide. The expression of the PaOhrR-repressed mKate was significantly increased when the cells enter the late log phase when cellular sulfane sulfur reached a maximum, but the mKate expression under the control of the PaOhrR-C9SC19S double mutant was not increased. Furthermore, the expression levels of ohrR and ohr in P. aeruginosa PAO1 were significantly increased when cellular sulfane sulfur was high. Thus, PaOhrR senses both exogenous and intrinsic sulfane sulfur to derepress its controlled genes. The finding also suggests that sulfane sulfur may be a common inducer of the MarR-type regulators, which may confer the bacteria to resist certain stresses without being exposed to the stresses. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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Review

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20 pages, 2535 KiB

Open AccessReview

Recent Advances in Biotechnologies for the Treatment of Environmental Pollutants Based on Reactive Sulfur Species

by Kaili Fan, Wei Wang, Xijun Xu, Yuan Yuan, Nanqi Ren, Duu-Jong Lee and Chuan Chen

Antioxidants 2023, 12(3), 767; https://doi.org/10.3390/antiox12030767 - 21 Mar 2023

Cited by 4 | Viewed by 2120

Abstract

The definition of reactive sulfur species (RSS) is inspired by the reactivity and variable chemical valence of sulfur. Sulfur is an essential element for life and is a part of global geochemical cycles. Wastewater treatment bioreactors can be divided into two major categories: [...] Read more.

The definition of reactive sulfur species (RSS) is inspired by the reactivity and variable chemical valence of sulfur. Sulfur is an essential element for life and is a part of global geochemical cycles. Wastewater treatment bioreactors can be divided into two major categories: sulfur reduction and sulfur oxidation. We review the origins of the definition of RSS and related biotechnological processes in environmental management. Sulfate reduction, sulfide oxidation, and sulfur-based redox reactions are key to driving the coupled global carbon, nitrogen, and sulfur co-cycles. This shows the coupling of the sulfur cycle with the carbon and nitrogen cycles and provides insights into the global material−chemical cycle. We also review the biological classification and RSS metabolic mechanisms of functional microorganisms involved in the biological processes, such as sulfate-reducing and sulfur-oxidizing bacteria. Developments in molecular biology and genomic technologies have allowed us to obtain detailed information on these bacteria. The importance of RSS in environmental technologies requires further consideration. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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26 pages, 3515 KiB

Open AccessReview

Generation and Physiology of Hydrogen Sulfide and Reactive Sulfur Species in Bacteria

by Sirui Han, Yingxi Li and Haichun Gao

Antioxidants 2022, 11(12), 2487; https://doi.org/10.3390/antiox11122487 - 17 Dec 2022

Cited by 6 | Viewed by 3272

Abstract

Sulfur is not only one of the most abundant elements on the Earth, but it is also essential to all living organisms. As life likely began and evolved in a hydrogen sulfide (H₂S)-rich environment, sulfur metabolism represents an early form of [...] Read more.

Sulfur is not only one of the most abundant elements on the Earth, but it is also essential to all living organisms. As life likely began and evolved in a hydrogen sulfide (H₂S)-rich environment, sulfur metabolism represents an early form of energy generation via various reactions in prokaryotes and has driven the sulfur biogeochemical cycle since. It has long been known that H₂S is toxic to cells at high concentrations, but now this gaseous molecule, at the physiological level, is recognized as a signaling molecule and a regulator of critical biological processes. Recently, many metabolites of H₂S, collectively called reactive sulfur species (RSS), have been gradually appreciated as having similar or divergent regulatory roles compared with H₂S in living organisms, especially mammals. In prokaryotes, even in bacteria, investigations into generation and physiology of RSS remain preliminary and an understanding of the relevant biological processes is still in its infancy. Despite this, recent and exciting advances in the fields are many. Here, we discuss abiotic and biotic generation of H₂S/RSS, sulfur-transforming enzymes and their functioning mechanisms, and their physiological roles as well as the sensing and regulation of H₂S/RSS. Full article

(This article belongs to the Special Issue Reactive Sulfur Species in Microorganisms)

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