Endogenous hydrogen sulfide reprograms mitochondrial respiration and modulates pathogenicity in Ustilago maydis

Highlights

  • •
    Respiratory growth with cysteine increases H2S production in U. maydis.
  • •
    Endogenous H2S promotes mitochondrial biogenesis and metabolic remodeling.
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    H2S shifts respiration toward alternative oxidase-dependent electron transport.
  • •
    Elevated H2S increases global protein S-sulfenylation and S-persulfidation.
  • •
    Endogenous H2S modulates disease severity during maize infection.

Abstract

Sulfur metabolism is a central determinant of microbial physiology and adaptation to environmental conditions. Hydrogen sulfide (H2S), a reactive sulfur species produced during cysteine metabolism, has recently emerged as a key regulator of mitochondrial function and redox signaling. However, its role in phytopathogenic fungi and its potential impact on fungal pathogenic behavior remain poorly understood.
Here, we show that metabolic conditions that enhance endogenous H2S production in the maize phytopathogen Ustilago maydis trigger coordinated cellular remodeling. Elevated intracellular H2S levels were associated with mitochondrial biogenesis, a shift from cytochrome-dependent respiration toward alternative oxidase (AOX)-mediated electron transport, and widespread proteomic reprogramming affecting mitochondrial, metabolic, and proteasomal pathways. These changes were accompanied by increased global protein S-sulfenylation and S-persulfidation, altered lipid distribution, and elevated hydrogen peroxide levels, indicating substantial remodeling of cellular redox homeostasis.
Functional consequences of this metabolic state were evaluated in maize infection assays. Although infection rates were not significantly altered, plants infected with cells exhibiting elevated endogenous H2S levels displayed increased tumor formation and altered symptom progression.
Together, our findings indicate that increased H2S production modulates mitochondrial respiration, redox regulation, and fungal pathogenic behavior in Ustilago maydis. This work highlights endogenous H2S as an important regulatory node connecting microbial metabolism with host-pathogen interactions.

Read full article for free (open access):
https://www.sciencedirect.com/science/article/pii/S2666517426000726



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