Dataset Information

Involvement of the Mitochondrial Protein Tyrosine Phosphatase PTPM1 in the Promotion of Conidiation, Development, and Pathogenicity in Colletotrichum graminicola.

ABSTRACT: The phosphorylation status of proteins, which is determined by protein tyrosine kinases (PTKs) and protein tyrosine phosphatases (PTPs), governs many cellular actions. In fungal pathogens, phosphorylation-mediated signal transduction has been considered to be one of the most important mechanisms in pathogenicity. Colletotrichum graminicola is an economically important corn pathogen. However, whether phosphorylation is involved in its pathogenicity is unknown. A mitochondrial protein tyrosine phosphatase gene, designated CgPTPM1, was deduced in C. graminicola through the use of bioinformatics and confirmed by enzyme activity assays and observation of its subcellular localization. We then created a CgPTPM1 deletion mutant (?CgPTPM1) to analyze its biological function. The results indicated that the loss of CgPTPM1 dramatically affected the formation of conidia and the development and differentiation into appressoria. However, the colony growth and conidial morphology of the ?CgPTPM1 strains were unaffected. Importantly, the ?CgPTPM1 mutant strains exhibited an obvious reduction of virulence, and the delayed infected hyphae failed to expand in the host cells. In comparison with the wild-type, ?CgPTPM1 accumulated a larger amount of H₂O₂ and was sensitive to exogenous H₂O₂. Interestingly, the host cells infected by the mutant also exhibited an increased accumulation of H₂O₂ around the infection sites. Since the expression of the CgHYR1, CgGST1, CgGLR1, CgGSH1 and CgPAP1 genes was upregulated with the H₂O₂ treatment, our results suggest that the mitochondrial protein tyrosine phosphatase PTPM1 plays an essential role in promoting the pathogenicity of C. graminicola by regulating the excessive in vivo and in vitro production of H₂O₂.

SUBMITTER: Wang S

PROVIDER: S-EPMC7841309 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Involvement of the Mitochondrial Protein Tyrosine Phosphatase PTPM1 in the Promotion of Conidiation, Development, and Pathogenicity in <i>Colletotrichum graminicola</i>.

Wang Shaowei S Li Guihua G Wei Yi Y Wang Gang G Dang Yuejia Y Zhang Penghui P Zhang Shi-Hong SH

Frontiers in microbiology 20210114

The phosphorylation status of proteins, which is determined by protein tyrosine kinases (PTKs) and protein tyrosine phosphatases (PTPs), governs many cellular actions. In fungal pathogens, phosphorylation-mediated signal transduction has been considered to be one of the most important mechanisms in pathogenicity. <i>Colletotrichum graminicola</i> is an economically important corn pathogen. However, whether phosphorylation is involved in its pathogenicity is unknown. A mitochondrial protein tyros ...[more]

PMID: 33519752

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Project description:Protein-tyrosine phosphorylation in bacteria plays a significant role in multiple cellular functions, including those related to community development and virulence. Metal-dependent protein tyrosine phosphatases that belong to the polymerase and histindinol phosphatase (PHP) family are widespread in Gram-positive bacteria. Here, we show that Porphyromonas gingivalis, a Gram-negative periodontal pathogen, expresses a PHP protein, Php1, with divalent metal ion-dependent tyrosine phosphatase activity. Php1 tyrosine phosphatase activity was attenuated by mutation of conserved histidine residues that are important for the coordination of metal ions and by mutation of a conserved arginine residue, a key residue for catalysis in other bacterial PHPs. The php1 gene is located immediately downstream of the gene encoding the bacterial tyrosine (BY) kinase Ptk1, which was a substrate for Php1 in vitro Php1 rapidly caused the conversion of Ptk1 to a state of low tyrosine phosphorylation in the absence of discernible intermediate phosphoforms. Active Php1 was required for P. gingivalis exopolysaccharide production and for community development with the antecedent oral biofilm constituent Streptococcus gordonii under nutrient-depleted conditions. In contrast, the absence of Php1 had no effect on the ability of P. gingivalis to form monospecies biofilms. In vitro, Php1 enzymatic activity was resistant to the effects of the streptococcal secreted metabolites pABA and H2O2, which inhibited Ltp1, an enzyme in the low-molecular-weight (LMW) phosphotyrosine phosphatase family. Ptk1 reciprocally phosphorylated Php1 on tyrosine residues 159 and 161, which independently impacted phosphatase activity. Loss of Php1 rendered P. gingivalis nonvirulent in an animal model of periodontal disease. Collectively, these results demonstrate that P. gingivalis possesses active PHP and LMW tyrosine phosphatases, a unique configuration in Gram-negatives which may allow P. gingivalis to maintain phosphorylation/dephosphorylation homeostasis in multispecies communities. Moreover, Php1 contributes to the pathogenic potential of the organism.IMPORTANCE Periodontal diseases are among the most common infections of humans and are also associated with systemic inflammatory conditions. Colonization and pathogenicity of P. gingivalis are regulated by signal transduction pathways based on protein tyrosine phosphorylation and dephosphorylation. Here, we identify and characterize a novel component of the tyrosine (de)phosphorylation axis: a polymerase and histindinol phosphatase (PHP) family enzyme. This tyrosine phosphatase, designated Php1, was required for P. gingivalis community development with other oral bacteria, and in the absence of Php1 activity P. gingivalis was unable to cause disease in a mouse model of periodontitis. This work provides significant insights into the protein tyrosine (de)phosphorylation network in P. gingivalis, its adaptation to heterotypic communities, and its contribution to colonization and virulence.

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Dataset Information

Involvement of the Mitochondrial Protein Tyrosine Phosphatase PTPM1 in the Promotion of Conidiation, Development, and Pathogenicity in Colletotrichum graminicola.

Publications

Involvement of the Mitochondrial Protein Tyrosine Phosphatase PTPM1 in the Promotion of Conidiation, Development, and Pathogenicity in <i>Colletotrichum graminicola</i>.

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