Hydrogen Sulfide Plays a Crucial Role in Bacterial Survival

Two crucial biological processes that support the growth of bacteria, particularly pathogenic bacteria like Escherichia coli, are antibiotic resistance and the oxidative stress response. A chemical messenger called hydrogen sulfide (H2S) controls a number of intracellular processes in bacteria, including how they react to antibiotics and oxidative stress.

The pathogenic bacterium Vibrio cholerae has been shown to exhibit increased iron uptake in response to intracellular H2S levels, which plays a role in the bacterium’s oxidative stress response. The exact mechanism underlying E. coli’s H2S-dependent cellular responses is still unknown, though. The study was published in the journal mBio.

To better understand the underlying mechanism and relationship between intracellular H2S and iron uptake in E. coli, a team of researchers led by Professor Shinji Masuda from the Department of Life Science & Technology, Tokyo Institute of Technology, Japan, has been working on the problem.

The 3-mercaptopyruvate sulfur transferase enzyme, which is responsible for producing H2S, is encoded by the mstA gene, which was overexpressed in a genetically modified wild-type (WT) E. coli strain. To determine the molecular pathways involved in the overall regulation of iron uptake in response to H2S availability, they also used sophisticated genetic sequencing techniques and assays.

Our research group had previously identified and characterized the arsenic repressor-type H2S-/supersulfide-responsive transcription factor SqrR in the purple photosynthetic bacterium Rhodobacter capsulatus, where SqrR regulated gene expression in response to H2S availability. YgaV, the SqrR homolog in E. coli, has also been reported for repressing the transcription of anaerobic respiratory genes in the absence of extracellular sulfide. This motivated our team to further investigate the relationship between intracellular H2S, YgaV dependent transcription, and iron uptake in E. coli.”

Shinji Masuda, Professor, Department of Life Science & Technology, Tokyo Institute of Technology

First, the scientists noticed that the WT strain that overexpressed mstA generated higher intracellular H2S levels, which led to noticeably greater antibiotic resistance. After that, they carried out an RNA sequencing analysis and discovered that the overproduction of H2S caused the upregulation of specific genes.

The genetic transcript levels of tcyP, the protein that encodes the transporter of the sulfur-containing amino acid L-cysteine, were found to have increased tenfold. Furthermore, they discovered that the gene for cysteinyl-tRNA synthase, which catalyzes the synthesis of supersulfides—molecules with self-linked sulfur atoms—was notably elevated.

In E. coli with mstA overexpression, super sulfides can directly inactivate β-lactam antibiotics and contribute to general antibiotic resistance. Furthermore, in the WT strain overexpressing mstA, dipeptide/heme transporter genes were downregulated, and genes linked to antibiotic efflux pumps were upregulated, suggesting the impact of H2S hyperaccumulation on iron absorption.

Additionally, the researchers verified that the upregulation of iron uptake genes in E. coli is caused by the H2S/supersulfide-responsive transcription factor YgaV. They found that the expression of iron uptake genes, such as fes, fepA, fhuE, fhuF, nfeF, and cirA, was dependent on the presence of YgaV, which in turn is dependent on intracellular H2S levels. The scientist did this by using a ΔygaV mutant strain of E. coli where ygaV is not expressed but mstA is overexpressed.

Our study provides valuable insights into the iron uptake dynamics in E. coli and substantiates the role of H2S-dependent YgaV in regulating the overall oxidative stress response and antibiotic resistance.”

Shinji Masuda, Professor, Department of Life Science & Technology, Tokyo Institute of Technology

Source:
Journal reference:

Nonoyama, S., et al. (2024) Increased intracellular H2S levels enhance iron uptake in Escherichia coli. Environmental Microbiology. doi.org/10.1128/mbio.01991-24

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