Dataset Information

BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress.

ABSTRACT: To cope with toxic levels of H2S, the plant pathogens Xylella fastidiosa and Agrobacterium tumefaciens employ the bigR operon to oxidize H2S into sulfite. The bigR operon is regulated by the transcriptional repressor BigR and it encodes a bifunctional sulfur transferase (ST) and sulfur dioxygenase (SDO) enzyme, Blh, required for H2S oxidation and bacterial growth under hypoxia. However, how Blh operates to enhance bacterial survival under hypoxia and how BigR is deactivated to derepress operon transcription is unknown. Here, we show that the ST and SDO activities of Blh are in vitro coupled and necessary to oxidize sulfide into sulfite, and that Blh is critical to maintain the oxygen flux during A. tumefaciens respiration when oxygen becomes limited to cells. We also show that H2S and polysulfides inactivate BigR leading to operon transcription. Moreover, we show that sulfite, which is produced by Blh in the ST and SDO reactions, is toxic to Citrus sinensis and that X. fastidiosa-infected plants accumulate sulfite and higher transcript levels of sulfite detoxification enzymes, suggesting that they are under sulfite stress. These results indicate that BigR acts as a sulfide sensor in the H2S oxidation mechanism that allows pathogens to colonize plant tissues where oxygen is a limiting factor.

SUBMITTER: de Lira NPV

PROVIDER: S-EPMC5823870 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress.

de Lira Nayara Patricia Vieira NPV Pauletti Bianca Alves BA Marques Ana Carolina AC Perez Carlos Alberto CA Caserta Raquel R de Souza Alessandra Alves AA Vercesi Aníbal Eugênio AE Paes Leme Adriana Franco AF Benedetti Celso Eduardo CE

Scientific reports 20180222 1

To cope with toxic levels of H2S, the plant pathogens Xylella fastidiosa and Agrobacterium tumefaciens employ the bigR operon to oxidize H2S into sulfite. The bigR operon is regulated by the transcriptional repressor BigR and it encodes a bifunctional sulfur transferase (ST) and sulfur dioxygenase (SDO) enzyme, Blh, required for H2S oxidation and bacterial growth under hypoxia. However, how Blh operates to enhance bacterial survival under hypoxia and how BigR is ...[more]

PMID: 29472641

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Project description:BackgroundIn some sedimentary environments, such as coastal intertidal and subtidal mudflats, sulfide levels can reach millimolar concentrations (2-5 mM) and can be toxic to marine species. Interestingly, some organisms have evolved biochemical strategies to overcome and tolerate high sulfide conditions, such as the echiuran worm, Urechis unicinctus. Mitochondrial sulfide oxidation is important for detoxification, in which sulfur dioxygenase (SDO) plays an indispensable role. Meanwhile, the body wall of the surface of the worm is in direct contact with sulfide. In our study, we chose the body wall to explore the SDO response to sulfide.MethodsTwo sulfide treatment groups (50 µM and 150 µM) and a control group (natural seawater) were used. The worms, U. unicinctus, were collected from the intertidal flat of Yantai, China, and temporarily reared in aerated seawater for three days without feeding. Finally, sixty worms with similar length and mass were evenly assigned to the three groups. The worms were sampled at 0, 6, 24, 48 and 72 h after initiation of sulfide exposure. The body walls were excised, frozen in liquid nitrogen and stored at -80 °C for RNA and protein extraction. Real-time quantitative RT-PCR, enzyme-linked immunosorbent assay and specific activity detection were used to explore the SDO response to sulfide in the body wall.ResultsThe body wall of U. unicinctus consists of a rugal epidermis, connective tissue, outer circular muscle and middle longitudinal muscle. SDO protein is mainly located in the epidermis. When exposed to 50 µM sulfide, SDO mRNA and protein contents almost remained stable, but SDO activity increased significantly after 6 h (P < 0.05). However, in the 150 µM sulfide treatment group, SDO mRNA and protein contents and activity all increased with sulfide exposure time; significant increases all began to occur at 48 h (P < 0.05).DiscussionAll the results indicated that SDO activity can be enhanced by sulfide in two regulation mechanisms: allosteric regulation, for low concentrations, and transcription regulation, which is activated with an increase in sulfide concentration.

Project description:The sulfur-containing amino acid cysteine is abundant in the environment, including in freshwater lakes. Biological cysteine degradation can result in hydrogen sulfide (H2S), a toxic and ecologically relevant compound that is a central player in biogeochemical cycling in aquatic environments. Here, we investigated the ecological significance of cysteine in oxic freshwater, using isolated cultures, controlled experiments, and multiomics. We screened bacterial isolates enriched from natural lake water for their ability to produce H2S when provided cysteine. We identified 29 isolates (Bacteroidota, Proteobacteria, and Actinobacteria) that produced H2S. To understand the genomic and genetic basis for cysteine degradation and H2S production, we further characterized three isolates using whole-genome sequencing (using a combination of short-read and long-read sequencing) and tracked cysteine and H2S levels over their growth ranges: Stenotrophomonas maltophilia (Gammaproteobacteria), S. bentonitica (Gammaproteobacteria), and Chryseobacterium piscium (Bacteroidota). Cysteine decreased and H2S increased, and all three genomes had genes involved in cysteine degradation. Finally, to assess the presence of these organisms and genes in the environment, we surveyed a 5-year time series of metagenomic data from the same isolation source (Lake Mendota, Madison, WI, USA) and identified their presence throughout the time series. Overall, our study shows that diverse isolated bacterial strains can use cysteine and produce H2S under oxic conditions, and we show evidence using metagenomic data that this process may occur more broadly in natural freshwater lakes. Future considerations of sulfur cycling and biogeochemistry in oxic environments should account for H2S production from the degradation of organosulfur compounds. IMPORTANCE Hydrogen sulfide (H2S), a naturally occurring gas with both biological and abiotic origins, can be toxic to living organisms. In aquatic environments, H2S production typically originates from anoxic (lacking oxygen) environments, such as sediments, or the bottom layers of thermally stratified lakes. However, the degradation of sulfur-containing amino acids such as cysteine, which all cells and life forms rely on, can be a source of ammonia and H2S in the environment. Unlike other approaches for biological H2S production such as dissimilatory sulfate reduction, cysteine degradation can occur in the presence of oxygen. Yet, little is known about how cysteine degradation influences sulfur availability and cycling in freshwater lakes. In our study, we identified diverse bacteria from a freshwater lake that can produce H2S in the presence of O2. Our study highlights the ecological importance of oxic H2S production in natural ecosystems and necessitates a change in our outlook on sulfur biogeochemistry.

Dataset Information

BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress.

Publications

BigR is a sulfide sensor that regulates a sulfur transferase/dioxygenase required for aerobic respiration of plant bacteria under sulfide stress.

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