Proteomic analysis of the periodontal pathogen Prevotella intermedia secretomes in biofilm and planktonic lifestyles

Karched, Maribasappa; Bhardwaj, Radhika G.; Qudeimat, Muawia A.; Al-Khabbaz, Areej K.; Ellepola, A. N. B.

doi:10.1038/s41598-022-09085-0

Cited by 13 publications

(12 citation statements)

References 52 publications

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“…The virulence factors mediating the contribution of P. intermedia to malignant transformation may be secreted proteins given that the proteinase K treatment of the conditioned medium eliminated these biological activities. In a recent report, an analysis of the functional protein association network of P. intermedia secretomes revealed that carbohydrate metabolism constitutes one of the three major groups in the network [45]. Among the components of the sugar metabolism network, glucose-6-phosphate isomerase (GPI), also known as autocrine motility factor (AMF), was identified.…”

Section: Discussionmentioning

confidence: 99%

Enrichment of Prevotella intermedia in human colorectal cancer and its additive effects with Fusobacterium nucleatum on the malignant transformation of colorectal adenomas

Jao

et al. 2022

J Biomed Sci

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Background Owing to the heterogeneity of microbiota among individuals and populations, only Fusobacterium nucleatum and Bacteroides fragilis have been reported to be enriched in colorectal cancer (CRC) in multiple studies. Thus, the discovery of additional bacteria contributing to CRC development in various populations can be expected. We aimed to identify bacteria associated with the progression of colorectal adenoma to carcinoma and determine the contribution of these bacteria to malignant transformation in patients of Han Chinese origin. Methods Microbiota composition was determined through 16S rRNA V3–V4 amplicon sequencing of autologous adenocarcinomas, adenomatous polyps, and non-neoplastic colon tissue samples (referred to as “tri-part samples”) in patients with CRC. Enriched taxa in adenocarcinoma tissues were identified through pairwise comparison. The abundance of candidate bacteria was quantified through genomic quantitative polymerase chain reaction (qPCR) in tissue samples from 116 patients. Associations of candidate bacteria with clinicopathological features and genomic and genetic alterations were evaluated through odds ratio tests. Additionally, the effects of candidate bacteria on CRC cell proliferation, migration, and invasion were evaluated through the co-culture of CRC cells with bacterial cells or with conditioned media from bacteria. Results Prevotella intermedia was overrepresented in adenocarcinomas compared with paired adenomatous polyps. Furthermore, co-abundance of P. intermedia and F. nucleatum was observed in tumor tissues. More notably, the coexistence of these two bacteria in adenocarcinomas was associated with lymph node involvement and distant metastasis. These two bacteria also exerted additive effects on the enhancement of the migration and invasion abilities of CRC cells. Finally, conditioned media from P. intermedia promoted the migration and invasion of CRC cells. Conclusion This report is the first to demonstrate that P. intermedia is enriched in colorectal adenocarcinoma tissues and enhances the migration and invasion abilities of CRC cells. Moreover, P. intermedia and F. nucleatum exert additive effects on the malignant transformation of colorectal adenomas into carcinomas. These findings can be used to identify patients at a high risk of malignant transformation of colorectal adenomas or metastasis of CRC, and they can accordingly be provided optimal clinical management.

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Section: Discussionmentioning

confidence: 99%

Enrichment of Prevotella intermedia in human colorectal cancer and its additive effects with Fusobacterium nucleatum on the malignant transformation of colorectal adenomas

Jao

et al. 2022

J Biomed Sci

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“…Other up-regulated surface proteins with a potential pathogenic role, identified in the periodontitis state, were the BspA of T. forsynthia ( Sharma et al, 1998 ; Mahalakshmi et al, 2018 ), the s-layer homology protein of Fretibacterium , and a lipoprotein cluster of Tannerella. Prevotella is known to secrete proteins in both planktonic and biofilm lifestyles ( Karched et al, 2022 ) and the increased transcription of the type VI secretion system protein Hcp suggests an important role of the Prevotella secretome in periodontitis. Elongation factor thermal unstable (EF-Tu) is one of the most abundant proteins in bacteria, with an important role in protein synthesis.…”

Section: Discussionmentioning

confidence: 99%

Microbial signatures in human periodontal disease: a metatranscriptome meta-analysis

Ovsepian,

Kardaras,

Skoulakis

et al. 2024

Front. Microbiol.

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The characterization of oral microbial communities and their functional potential has been shaped by metagenomics and metatranscriptomics studies. Here, a meta-analysis of four geographically and technically diverse oral shotgun metatranscriptomics studies of human periodontitis was performed. In total, 54 subgingival plaque samples, 27 healthy and 27 periodontitis, were analyzed. The core microbiota of the healthy and periodontitis group encompassed 40 and 80 species, respectively, with 38 species being common to both microbiota. The differential abundance analysis identified 23 genera and 26 species, that were more abundant in periodontitis. Our results not only validated previously reported genera and species associated with periodontitis with heightened statistical significance, but also elucidated additional genera and species that were overlooked in the individual studies. Functional analysis revealed a significant up-regulation in the transcription of 50 gene families (UniRef-90) associated with transmembrane transport and secretion, amino acid metabolism, surface protein and flagella synthesis, energy metabolism, and DNA supercoiling in periodontitis samples. Notably, the overwhelming majority of the identified gene families did not exhibit differential abundance when examined across individual datasets. Additionally, 4 bacterial virulence factor genes, including TonB dependent receptor from P. gingivalis, surface antigen BspA from T. forsynthia, and adhesin A (PsaA) and Type I glyceraldehyde-3-phosphate dehydrogenase (GAPDH) from the Streptococcus genus, were also found to be significantly more transcribed in periodontitis group. Microbial co-occurrence analysis demonstrated that the periodontitis microbial network was less dense compared to the healthy network, but it contained more positive correlations between the species. Furthermore, there were discernible disparities in the patterns of interconnections between the species in the two networks, denoting the rewiring of the whole microbial network during the transition to the disease state. In summary, our meta-analysis has provided robust insights into the oral active microbiome and transcriptome in both health and disease.

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“…Previous proteomic analysis of P. intermedia compared the subcellular localization of proteins in planktonic and biofilm states (Karched et al, 2022 ). However, OMVs in P. intermedia have yet to be explored.…”

Section: Discussionmentioning

confidence: 99%

Ultrastructural and glycoproteomic characterization of Prevotella intermedia: Insights into O‐glycosylation and outer membrane vesicles

Ye,

Paul,

et al. 2024

MicrobiologyOpen

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Prevotella intermedia, a Gram‐negative bacterium from the Bacteroidota phylum, is associated with periodontitis. Other species within this phylum are known to possess the general O‐glycosylation system. The O‐glycoproteome has been characterized in several species, including Tannerella forsythia, Porphyromonas gingivalis, and Flavobacterium johnsoniae. In our study, we used electron cryotomography (cryoET) and glycoproteomics to reveal the ultrastructure of P. intermedia and characterize its O‐glycoproteome. Our cryoET analysis unveiled the ultrastructural details of the cell envelope and outer membrane vesicles (OMVs) of P. intermedia. We observed an electron‐dense surface layer surrounding both cells and OMVs. The OMVs were often large (>200 nm) and presented two types, with lumens being either electron‐dense or translucent. LC‐MS/MS analyses of P. intermedia fractions led to the identification of 1655 proteins, which included 62 predicted T9SS cargo proteins. Within the glycoproteome, we identified 443 unique O‐glycosylation sites within 224 glycoproteins. Interestingly, the O‐glycosylation motif exhibited a broader range than reported in other species, with O‐glycosylation found at D(S/T)(A/I/L/M/T/V/S/C/G/F/N/E/Q/D/P). We identified a single O‐glycan with a delta mass of 1531.48 Da. Its sequence was determined by MS2 and MS3 analyses using both collision‐induced dissociation and high‐energy collisional dissociation fragmentation modes. After partial deglycosylation with trifluoromethanesulfonic acid, the O‐glycan sequence was confirmed to be dHex‐dHex‐HexNAc (HPO3‐C6H12O5)‐dHex‐Hex‐HexA‐Hex(dHex). Bioinformatic analyses predicted the localization of O‐glycoproteins, with 73 periplasmic proteins, 53 inner membrane proteins, 52 lipoproteins, 26 outer membrane proteins, and 14 proteins secreted by the T9SS.

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Proteomic analysis of the periodontal pathogen Prevotella intermedia secretomes in biofilm and planktonic lifestyles

Cited by 13 publications

References 52 publications

Enrichment of Prevotella intermedia in human colorectal cancer and its additive effects with Fusobacterium nucleatum on the malignant transformation of colorectal adenomas

Enrichment of Prevotella intermedia in human colorectal cancer and its additive effects with Fusobacterium nucleatum on the malignant transformation of colorectal adenomas

Microbial signatures in human periodontal disease: a metatranscriptome meta-analysis

Ultrastructural and glycoproteomic characterization of Prevotella intermedia: Insights into O‐glycosylation and outer membrane vesicles

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