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Combined transcriptome and metabolome analysis reveals the regulatory network of histidine kinase QseC in the two-component system of Glaesserella parasuis

ABSTRACT: Glaesserella parasuis is the causative agent of Glässer's disease in pigs, which can lead to polyserositis, arthritis, and meningitis. This study used transcriptome and metabolomics sequencing techniques to investigate the mechanism of action of qseC gene in Glaesserella parasuis. Transmission electron microscopy revealed that the ΔqseC mutant strain exhibited localized dissolution and rupture of the cell wall and membrane. The cytoplasmic wall separation was obvious, and the cytoplasm appeared sparse. These findings suggest an imbalance in membrane homeostasis。Metabolomics analysis identified 819 metabolites, among which 24 metabolites showed significant differences under positive ion mode, including upregulation of Methionine, Prostaglandin F2 α -1-glyceryl ester, and downregulation of Hypoxantine, UDP, and others. There were significant differences in 36 metabolites under negative ion mode. KEGG enrichment analysis revealed abnormalities in pathways related to amino acid synthesis, lipid metabolism, and quorum sensing. Transcriptomic analysis identified 663 differentially expressed genes, including upregulation of membrane synthesis-related genes (such as plsB and wecA) and downregulation of virulence factors (such as hrpA and pilW). This study systematically analyzed the regulatory networks of differentially expressed genes and metabolites by integrating transcriptome and metabolome data. Key genes such as plsB and wecA form a strong association network with metabolites such as methionine and prostaglandin F2α-1-glyceride. KEGG pathway co-enrichment analysis showed that amino acid synthesis (such as cysteine/methionine metabolism) and purine metabolism pathways were co regulated in positive ion mode, while peptidoglycan synthesis and glycerophospholipid metabolism were significantly enriched in negative ion mode. This study constructed a cross-omics regulatory map of “gene-metabolism” mediated by QseC, revealing the global regulatory role of QseC in Glaesserella parasuis, providing a theoretical basis for the development of new prevention and control strategies against Glaesserella parasuis infection.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - positive - reverse phase

PROVIDER: MTBLS12504 | MetaboLights | 2025-08-11

REPOSITORIES: MetaboLights

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Project description:As a dynamic structure with a barrier between the cell and the outside world, maintenance of cell wall integrity (CWI) is important for fungal growth, development and pathogenicity processes. Here we characterized a MADS-box transcription factor RlmA (AoRlmA) downstream of the CWI regulatory pathway in the nematode-trapping fungus Arthrobotrys oligospora. Deletion of AorlmA caused a reduction in mycelial growth and the number of nuclei, and significant downregulation of transcript levels of genes related to nucleus synthesis and DNA damage repair, such as rad3, spo11, and rad25. Meanwhile, the ΔAorlmA mutant strains showed a significant reduction in spore production compared with the wild-type (WT) strain, and the transcript levels of sporulation-related genes was downregulated in the ΔAorlmA mutant during the early and middle stages of condiation, such as flbA, medA, and vosA. Meanwhile, the mycelial cell wall of the ΔAorlmA mutant strain showed breakage. Also, the transcript levels of genes related to cell wall synthesis were significantly down-regulated in the mutant strain compared to the WT strain, and the mutant strain was more sensitive to stresses of cell wall synthesis disruptors, oxidative stress and osmotic stress than the WT strain. Compared with the WT strain, the ΔAorlmA mutant strain not only had a reduced number of traps and nematicidal ability, but also, the shape of the traps of the mutants has also changed. In addition, In addition, AoRlmA also regulates autophagy and endocytosis. Transcriptome analysis of ΔAorlmA mutant strains showed that AorlmA regulates redox, cell wall synthesis, DNA replication and damage repair, and pathogenic processes. Metabolomic analysis showed that AorlmA is involved in the biosynthesis of secondary metabolites of A. oligospora. To summarise, our data suggest that AorlmA is involved in growth, sporulation, spore germination, maintenance of cell wall integrity, DNA replication and damage repair, pathogenesis, autophagy and secondary metabolite biosynthesis processes.

Project description:Background The sphingolipid Glucosylceramide (GlcCer) and factors involved in the fungal GlcCer pathways were shown earlier to be an integral part of fungal virulence, especially in fungal replication at 37°C, in neutral/alkaline pH and 5% CO2 environments (e.g. alveolar spaces). Two mutants (null mutants’ delta-gcs1 and delta-smt1 lacking glucosylceramide synthase 1 gene and C9 sphingolipid methyltransferase 1 gene respectively) of this pathway were attenuated in virulence and have a growth defect at the above-mentioned conditions. These mutants with either no or structurally modified GlcCer located on the cell-membrane have reduced membrane rigidity, which may have altered not only the physical location of membrane proteins but also their expression, as the pathogen’s mode of adaptation to changing need. Importantly, pathogens are known to adapt themselves to the changing host environments by altering their patterns of gene expression. Results By transcriptional analysis of gene expression, we identified six genes whose expression was changed from their wild-type counterpart grown in the same conditions, i.e they became either down regulated or up regulated in these two mutants. The microarray data was validated by real-time PCR, which confirmed their fold change in gene expression. The 6 genes we identified, viz siderochrome-iron transporter (CNAG_02083), monosaccharide transporter (CNAG_05340), glucose transporter (CNAG_03772), membrane protein (CNAG_03912), membrane transport protein (CNAG_00539), and sugar transporter (CNAG_06963), all of which are membrane-localized and have significantly altered gene expression levels. Therefore, we speculate that these genes function either independently or in tandem with a structurally modified cell wall/plasma membrane resulting from the modifications of the GlcCer pathway and thus possibly disrupt trans membrane signaling complex, which in turn contributes to Cryptococcal osmotic, pH, ion homeostasis and its pathobiology. Conclusion Gene expression microarrays identified 6 genes by gene set enrichment analysis and validated by qRT-PCR, which are involved in the trans membrane signaling network in Cryptococcus neoformans, controlling the rigidity of the membrane in neutral-alkaline pH and therefore the pathobiology of the fungus in these conditions.

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Combined transcriptome and metabolome analysis reveals the regulatory network of histidine kinase QseC in the two-component system of Glaesserella parasuis

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