PgFur participates differentially in expression of virulence factors in more virulent A7436 and less virulent ATCC 33277 Porphyromonas gingivalis strains

Śmiga, Michał; Stępień, Paulina; Olczak, Mariusz; Olczak, Teresa

doi:10.1186/s12866-019-1511-x

Cited by 7 publications

(38 citation statements)

References 86 publications

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Section: Introductioncontrasting

confidence: 56%

“…Prevotella intermedia strain 17 (GenBank: CP003502.1 and CP003503.1) and Tannerella forsythia (ATCC 43037) were maintained as described previously [37]. Streptococcus gordonii (ATCC 10558) was grown in TSB agar or liquid medium (5% TBS) under an increased concentration of CO 2 using the Atmosphere generation system (Thermo Scientific, Waltham, MA, USA) as reported previously [16].…”

Section: Bacterial Strains and Growth Conditionsmentioning

confidence: 99%

“…Gene expression was initially examined in bacteria cultured for 20 h in iron/heme rich (Hm) or depleted (DIP) medium using microarray analysis as reported previously [13,16]. Additionally, reverse transcriptase-quantitative polymerase chain reaction (RT-qPCR) was used as reported previously [16,40].…”

Section: Gene Expression Analysismentioning

confidence: 99%

“…P. gingivalis has developed numerous sophisticated mechanisms for the acquisition of nutrients, enabling its survival as well as its proliferation inside and spread between host cells [12][13][14][15][16]. Among the most important virulence factors are proteases, mainly lysine-and arginine-specific gingipains encoded by kgp, rgpA, and rgpB genes, which play a crucial role in the degradation of host proteins and tissue components [17][18][19].…”

Section: Introductionmentioning

confidence: 99%

“…Recently, we have shown that P. gingivalis ferric uptake regulator homolog (PgFur) is an important transcription factor, regulating genes involved in interaction with host cells and other periodontopathogens [13,16]. A P. gingivalis mutant strain lacking a pgfur gene showed reduced tolerance to H 2 O 2 and was more sensitive to air exposure, although we did not observe regulation of typical genes responsible for the oxidative stress response [13,16]. We discovered that the expression of many genes involved in regulation of gene expression was altered in the mutant strain, including the downregulated PGA7_00004090 gene, encoding a putative transcription factor belonging to the cAMP receptor protein/fumarate and nitrate reductase regulator (Crp/Fnr) superfamily.…”

Section: Introductionmentioning

confidence: 99%

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PgRsp Is a Novel Redox-Sensing Transcription Regulator Essential for Porphyromonas gingivalis Virulence

Śmiga

Olczak

2019

Microorganisms

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Porphyromonas gingivalis is one of the etiological agents of chronic periodontitis. Both heme and oxidative stress impact expression of genes responsible for its survival and virulence. Previously we showed that P. gingivalis ferric uptake regulator homolog affects expression of a gene encoding a putative Crp/Fnr superfamily member, termed P. gingivalis redox-sensing protein (PgRsp). Although PgRsp binds heme and shows the highest similarity to proteins assigned to the CooA family, it could be a member of a novel, separate family of proteins with unknown function. Expression of the pgrsp gene is autoregulated and iron/heme dependent. Genes encoding proteins engaged in the oxidative stress response were upregulated in the pgrsp mutant (TO11) strain compared with the wild-type strain. The TO11 strain showed higher biomass production, biofilm formation, and coaggregation ability with Tannerella forsythia and Prevotella intermedia. We suggest that PgRsp may regulate production of virulence factors, proteases, Hmu heme acquisition system, and FimA protein. Moreover, we observed growth retardation of the TO11 strain under oxidative conditions and decreased survival ability of the mutant cells inside macrophages. We conclude that PgRsp protein may play a role in the oxidative stress response using heme as a ligand for sensing changes in redox status, thus regulating the alternative pathway of the oxidative stress response alongside OxyR.

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Section: Introductioncontrasting

confidence: 56%

Section: Bacterial Strains and Growth Conditionsmentioning

confidence: 99%

Section: Gene Expression Analysismentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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PgRsp Is a Novel Redox-Sensing Transcription Regulator Essential for Porphyromonas gingivalis Virulence

Śmiga

Olczak

2019

Microorganisms

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Hemophore-like proteins of the HmuY family in the oral and gut microbiome: unraveling the mystery of their evolution

Olczak,

Śmiga,

Antonyuk

et al. 2024

Microbiol Mol Biol Rev

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SUMMARY Heme (iron protoporphyrin IX, FePPIX) is the main source of iron and PPIX for host-associated pathogenic bacteria, including members of the Bacteroidota (formerly Bacteroidetes) phylum. Porphyromonas gingivalis , a keystone oral pathogen, uses a unique heme uptake (Hmu) system, comprising a hemophore-like protein, designated as the first member of the novel HmuY family. Compared to classical, secreted hemophores utilized by Gram-negative bacteria or near-iron transporter domain-based hemophores utilized by Gram-positive bacteria, the HmuY family comprises structurally similar proteins that have undergone diversification during evolution. The best characterized are P. gingivalis HmuY and its homologs from Tannerella forsythia (Tfo), Prevotella intermedia (PinO and PinA), Bacteroides vulgatus (Bvu), and Bacteroides fragilis (BfrA, BfrB, and BfrC). In contrast to the two histidine residues coordinating heme iron in P. gingivalis HmuY, Tfo, PinO, PinA, Bvu, and BfrA preferentially use two methionine residues. Interestingly, BfrB, despite conserved methionine residue, binds the PPIX ring without iron coordination. BfrC binds neither heme nor PPIX in keeping with the lack of conserved histidine or methionine residues used by other members of the HmuY family. HmuY competes for heme binding and heme sequestration from host hemoproteins with other members of the HmuY family to increase P. gingivalis competitiveness. The participation of HmuY in the host immune response confirms its relevance in relation to the survival of P. gingivalis and its ability to induce dysbiosis not only in the oral microbiome but also in the gut microbiome or other host niches, leading to local injuries and involvement in comorbidities.

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Comparative analysis of Porphyromonas gingivalis A7436 and ATCC 33277 strains reveals differences in the expression of heme acquisition systems

Śmiga,

Ślęzak,

Olczak

2024

Microbiol Spectr

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Porphyromonas gingivalis strains exhibit different phenotypes in vitro , different virulence potential in animal models, and different associations with human diseases, with strains classified as virulent/more virulent (e.g., A7436 and W83) or as less virulent/avirulent (e.g., ATCC 33277). In this study, we comparatively analyzed the A7436 and ATCC 33277 strains to better understand their variability. Global gene expression analysis in response to heme and iron limitation revealed more pronounced differences in the A7436 than in the ATCC 33277 strain; however, in both strains, the largest changes were observed in genes encoding hypothetical proteins, genes whose products participate in energy metabolism, and in genes encoding proteins engaged in transport and binding proteins. Our results confirmed that variability between P. gingivalis strains is due to differences in the arrangement of their genomes. Analysis of gene expression of heme acquisition systems demonstrated that not only the availability of iron and heme in the external environment but also the ability to store iron intracellularly can influence the P. gingivalis phenotype. Therefore, we assume that differences in virulence potential may also be due to differences in the production of systems involved in iron and heme acquisition, mainly the Hmu system. In addition, our study showed that hemoglobin, in a concentration-dependent manner, differentially influences the virulence potential of P. gingivalis strains. We conclude that iron and heme homeostasis may add to the variability observed between P. gingivalis strains. IMPORTANCE Periodontitis belongs to a group of multifactorial diseases, characterized by inflammation and destruction of tooth-supporting tissues. P. gingivalis is one of the most important microbial factors involved in the initiation and progression of periodontitis. To survive in the host, the bacterium must acquire heme as a source of iron and protoporphyrin IX. P. gingivalis strains respond differently to changing iron and heme concentrations, which may be due to differences in the expression of systems involved in iron and heme acquisition. The ability to accumulate iron intracellularly, being different in more and less virulent P. gingivalis strains, may influence their phenotypes, production of virulence factors (including proteins engaged in heme acquisition), and virulence potential of this bacterium.

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PgFur participates differentially in expression of virulence factors in more virulent A7436 and less virulent ATCC 33277 Porphyromonas gingivalis strains

Cited by 7 publications

References 86 publications

PgRsp Is a Novel Redox-Sensing Transcription Regulator Essential for Porphyromonas gingivalis Virulence

PgRsp Is a Novel Redox-Sensing Transcription Regulator Essential for Porphyromonas gingivalis Virulence

Hemophore-like proteins of the HmuY family in the oral and gut microbiome: unraveling the mystery of their evolution

Comparative analysis of Porphyromonas gingivalis A7436 and ATCC 33277 strains reveals differences in the expression of heme acquisition systems

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