Acyl-CoA reductase PGN_0723 utilizes succinyl-CoA to generate succinate semialdehyde in a butyrate-producing pathway of Porphyromonas gingivalis

Yamaguchi, Yasuo; Sato, Mitsunari; Kezuka, Yuichiro; Hasegawa, Yoshinori; Nagano, Keiji; Takebe, Jun; Yoshimura, Fuminobu

doi:10.1016/j.abb.2016.03.014

Cited by 8 publications

(10 citation statements)

References 43 publications

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“…The majority of these 52 proteins are related to transcription and protein production, including 30S proteins, 50S proteins, translation initiation factors, and tRNA ligases. Some are enzymes involved in energy metabolism, such as PGN_1367 /NAD‐specific glutamate dehydrogenase, the protein that converts glutamate into 2‐oxoglutarate, and PGN_0723 /succinate‐semialdehyde dehydrogenase, whose role is to release succinate from succinate semialdehyde based on its enzymology, but in P gingivalis , it was demonstrated to produce succinate semialdehyde from succinyl‐CoA which regulates succinylation . Some of the other proteins had identifiable functions, such as PGN_1019 /PorX, which regulates the type IX secretion system and PGN_1451 /groEL co‐chaperone.…”

Section: Resultsmentioning

confidence: 99%

Global analysis of lysine succinylome in the periodontal pathogen Porphyromonas gingivalis

Gong

Zhou

et al. 2019

Molecular Oral Microbiology

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The gram-negative anaerobe Porphyromonas gingivalis is not only a keystone periodontal pathogen but also an emerging systemic pathogen. Although the newly discovered protein post-translational modification (PTM), lysine succinylation (Ksuc), appears to play an important role in modulating metabolic processes in bacteria, this PTM has not been investigated in P gingivalis. In this study, we used a highly sensitive proteomics approach combining affinity enrichment with high-resolution liquid chromatography coupled with tandem mass spectrometry to examine Ksuc in P gingivalis.In total, 345 Ksuc sites in 233 proteins were identified and determined to be involved in a variety of cellular processes. In the region surrounding Ksuc sites, lysine residues were drastically overrepresented and sequence motifs with succinyl-lysine flanked by a lysine at the +3 or +6 positions appear to be unique to this pathogen. Additionally, our results suggest a crosstalk between Ksuc and glycosylation, but the overlap between Ksuc and acetylation in P gingivalis is quite different from that observed in other organisms. Notably, Ksuc was observed in proteins associated with established virulence factors, including gingipains, fimbriae, RagB, and PorR. Moreover, products of the factors necessary for P gingivalis in vitro survival (18.5%) were found to be succinylated at lysine sites and the same was observed in products of fitness factors for P gingivalis survival in both abscess and epithelial cell colonization environments (12%). Collectively, these results suggest that Ksuc may be a new mechanism in modulating the virulence, adaptation, and fitness of P gingivalis. K E Y W O R D S fitness factors, lysine succinylation, necessary factors, Porphyromonas gingivalis, proteomics | 75 WU et al.

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Section: Resultsmentioning

confidence: 99%

Global analysis of lysine succinylome in the periodontal pathogen Porphyromonas gingivalis

Gong

Zhou

et al. 2019

Molecular Oral Microbiology

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“…The pathway for GABA degradation is shared with succinate degradation via succinate semialdehyde and 4‐hydroxybutyrate (Fig. ), and butyrate production from succinate via this pathway has been demonstrated in Porphyromonas gingivalis and Clostridioides difficile (Ferreyra et al ., ; Yoshida et al ., ).…”

Section: Butyrate and Propionate Formation From Proteins And Amino Acidsmentioning

confidence: 97%

Formation of propionate and butyrate by the human colonic microbiota

Louis

Flint

2016

Environmental Microbiology

1,760

1,353

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SummaryThe human gut microbiota ferments dietary nondigestible carbohydrates into short-chain fatty acids (SCFA). These microbial products are utilized by the host and propionate and butyrate in particular exert a range of health-promoting functions. Here an overview of the metabolic pathways utilized by gut microbes to produce these two SCFA from dietary carbohydrates and from amino acids resulting from protein breakdown is provided. This overview emphasizes the important role played by crossfeeding of intermediary metabolites (in particular lactate, succinate and 1,2-propanediol) between different gut bacteria. The ecophysiology, including growth requirements and responses to environmental factors, of major propionate and butyrate producing bacteria are discussed in relation to dietary modulation of these metabolites. A detailed understanding of SCFA metabolism by the gut microbiota is necessary to underpin effective strategies to optimize SCFA supply to the host.

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“…Tan et al [22] showed that P. gingivalis W50 increased the rate of hydrolysis of glycine- The metabolic genes and pathway reactions of P. gingivalis W83 were sourced from KEGG with reference to Yoshida et al [44,45] and Sato et al [46]. Gene products with their gene expression fold changes are listed in red for each gene that showed upregulation during P. gingivalis W50 growth in OB: CM relative to OBGM.…”

Section: Proteases Required For Hydrolysis Of Glycine-containing Peptmentioning

confidence: 99%

Metabolic cooperativity between Porphyromonas gingivalis and Treponema denticola

Kin

Butler

Slakeski

et al. 2020

Journal of Oral Microbiology

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Background: Porphyromonas gingivalis and Treponema denticola are proteolytic periodontopathogens that co-localize in polymicrobial subgingival plaque biofilms, display in vitro growth symbiosis and synergistic virulence in animal models of disease. These symbioses are underpinned by a range of metabolic interactions including cooperative hydrolysis of glycine-containing peptides to produce free glycine, which T. denticola uses as a major energy and carbon source. Objective: To characterize the P. gingivalis gene products essential for these interactions. Methods: The P. gingivalis transcriptome exposed to cell-free T. denticola conditioned medium was determined using RNA-seq. P. gingivalis proteases potentially involved in hydrolysis of glycine-containing peptides were identified using a bioinformatics approach. Results: One hundred and thirty-twogenes displayed differential expression, with the pattern of gene expression consistent with succinate cross-feeding from T. denticola to P. gingivalis and metabolic shifts in the P. gingivalis folate-mediated one carbon superpathway. Interestingly, no P. gingivalis proteases were significantly up-regulated. Three P. gingivalis proteases were identified as candidates and inactivated to determine their role in the release of free glycine. P. gingivalis PG0753 and PG1788 but not PG1605 are involved in the hydrolysis of glycine-containing peptides, making free glycine available for T. denticola utilization. Conclusion: Collectively these metabolic interactions help to partition resources and engage synergistic interactions between these two species.

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Acyl-CoA reductase PGN_0723 utilizes succinyl-CoA to generate succinate semialdehyde in a butyrate-producing pathway of Porphyromonas gingivalis

Cited by 8 publications

References 43 publications

Global analysis of lysine succinylome in the periodontal pathogen Porphyromonas gingivalis

Global analysis of lysine succinylome in the periodontal pathogen Porphyromonas gingivalis

Formation of propionate and butyrate by the human colonic microbiota

Metabolic cooperativity between Porphyromonas gingivalis and Treponema denticola

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