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Unravelling the key steps impairing the metabolic state of Xanthomonas cells undergoing programmed cell death

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Abstract

Programmed cell death (PCD) has been reported in Xanthomonas axonopodis pv. glycines (Xag) wild type earlier and was indirectly shown to be induced by metabolic stress; however, deciphering the key proteins regulating the metabolic stress remained unrevealed. In this study, transcriptomic and proteomic analyses were performed to investigate the prominent pathways, having a role in the induction of metabolic stress in Xag cells undergoing PCD. A comprehensive analysis of transcriptome and proteome data revealed the major involvement of metabolic pathways related to branched chain amino acid degradation, such as acyl-CoA dehydrogenase and energy-yielding, ubiquinol:cytochrome c oxidoreductase complex, in Xag cells undergoing PCD. Consequently, oxidative stress response genes showed major upregulation in Xag cells in PCD-inducing medium; however, no such upregulation was observed at the protein level, indicative of depleted protein levels under excessive stress conditions. Activation of stress response and DNA repair proteins was also observed in Xag cells grown in PCD-inducing medium, which is indicative of excessive cellular damage. Thus, the findings indicate that programmed cell death in Xag is an outcome of metabolic stress in nutrient condition not suitable for a plant pathogen like Xanthomonas, which is more acclimatised with altogether a different nutritional requirement predominantly having an enriched carbohydrate source.

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Data availability

The data will be made available from the corresponding author upon reasonable request

Abbreviations

Xag wt:

Xanthomonas axonopodis pv. glycines wild type

PCD:

Programmed cell death

ROS:

Reactive oxygen species

RNA-seq:

Ribonucleic acid sequencing

DEGs:

Differentially expressed genes

DAPs:

Differentially abundant proteins

LC-MS/MS:

Liquid chromatography-tandem mass spectrometry

SWATH-MS:

Sequential Window Acquisition of All Theoretical Mass Spectra

QC:

Quality control

NCBI:

National Center for Biotechnology Information

FDR:

False discovery rate

COG:

Clusters of orthologous groups

GO:

Gene ontology

BCAAs:

Branched chain amino acids

H2O2 :

Hydrogen peroxide

NADH:

Nicotinamide adenine dinucleotide (NAD) + hydrogen (H)

SOD:

Superoxide dismutase

GST:

Glutathione S-transferase

GSH:

Glutathione

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Funding

The sole funding agency is the Government of India and no external source of fund or study sponsor is involved.

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Authors and Affiliations

  1. Food Technology Division, Bhabha Atomic Research Centre, Trombay, Mumbai, Maharashtra, 400085, India

    Jyoti Tripathi & Satyendra Gautam

  2. Homi Bhabha National Institute, Anushaktinagar, Mumbai, 400094, India

    Jyoti Tripathi & Satyendra Gautam

Authors
  1. Jyoti Tripathi
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  2. Satyendra Gautam
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Contributions

JT performed the laboratory experiments, methodology, validation, and analysis; prepared the manuscript draft; and contributed to reviewing and editing. SG contributed to the conceptualization, validation, supervision, and reviewing and editing of the manuscript.

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Correspondence to Satyendra Gautam.

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Tripathi, J., Gautam, S. Unravelling the key steps impairing the metabolic state of Xanthomonas cells undergoing programmed cell death. Int Microbiol (2024). https://doi.org/10.1007/s10123-023-00471-w

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