Cell Proteins Obtained by Peptic Shaving of Two Phenotypically Different Strains of Streptococcus thermophilus as a Source of Anti-Inflammatory Peptides
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cells, Chemicals, and Materials
2.2. Bacterial Strains and Growth Conditions
2.3. Enzymatic Shaving of Surface Proteins
2.4. LC-MS/MS Analysis
2.5. Cell Lines, Culture Conditions, Toxicity, Anti-Inflammatory Assay, and ELISA Analysis
2.6. Western Blot Analysis
2.7. Statistical Analyses
3. Results
3.1. Analysis of Peptides Recovered after Proteolytic Shaving of S. thermophilus LMD-9 and CNRZ-21N
3.2. Anti-Inflammatory Effect on THP-1 Macrophages of Peptide Hydrolysates
3.3. Anti-Inflammatory Effect on HT-29 Cells of Peptide Hydrolysates
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Delorme, C. Safety Assessment of Dairy Microorganisms: Streptococcus thermophilus. Int. J. Food Microbiol. 2008, 126, 274–277. [Google Scholar] [CrossRef] [PubMed]
- Hols, P.; Hancy, F.; Fontaine, L.; Grossiord, B.; Prozzi, D.; Leblond-Bourget, N.; Decaris, B.; Bolotin, A.; Delorme, C.; Ehrlich, D.S.; et al. New Insights in the Molecular Biology and Physiology of Revealed by Comparative Genomics. FEMS Microbiol. Rev. 2005, 29, 435–463. [Google Scholar] [CrossRef] [PubMed]
- Uriot, O.; Denis, S.; Junjua, M.; Roussel, Y.; Dary-Mourot, A.; Blanquet-Diot, S. Streptococcus thermophilus: From Yogurt Starter to a New Promising Probiotic Candidate? J. Funct. Foods 2017, 37, 74–89. [Google Scholar] [CrossRef]
- Boulay, M.; Metton, C.; Mézange, C.; Correia, L.O.; Meylheuc, T.; Monnet, V.; Gardan, R.; Juillard, V. Three Distinct Proteases Are Responsible for Overall Cell Surface Proteolysis in Streptococcus thermophilus. Appl. Environ. Microbiol. 2021, 87, e01292-21. [Google Scholar] [CrossRef]
- Dandoy, D.; Fremaux, C.; de Frahan, M.H.; Horvath, P.; Boyaval, P.; Hols, P.; Fontaine, L. The Fast Milk Acidifying Phenotype of Streptococcus thermophilus Can Be Acquired by Natural Transformation of the Genomic Island Encoding the Cell-Envelope Proteinase PrtS. Microb. Cell. Fact. 2011, 10, S21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Delorme, C.; Bartholini, C.; Bolotine, A.; Ehrlich, S.D.; Renault, P. Emergence of a Cell Wall Protease in the Streptococcus thermophilus Population. Appl. Environ. Microbiol. 2010, 76, 451–460. [Google Scholar] [CrossRef] [Green Version]
- Galia, W.; Perrin, C.; Genay, M.; Dary, A. Variability and Molecular Typing of Streptococcus thermophilus Strains Displaying Different Proteolytic and Acidifying Properties. Int. Dairy J. 2009, 19, 89–95. [Google Scholar] [CrossRef]
- Hafeez, Z.; Cakir-Kiefer, C.; Roux, E.; Perrin, C.; Miclo, L.; Dary-Mourot, A. Strategies of Producing Bioactive Peptides from Milk Proteins to Functionalize Fermented Milk Products. Food Res. Int. 2014, 63, 71–80. [Google Scholar] [CrossRef]
- Miclo, L.; Roux, É.; Genay, M.; Brusseaux, É.; Poirson, C.; Jameh, N.; Perrin, C.; Dary, A. Variability of Hydrolysis of β-, αs1-, and α s2 -Caseins by 10 Strains of Streptococcus thermophilus and Resulting Bioactive Peptides. J. Agric. Food Chem. 2012, 60, 554–565. [Google Scholar] [CrossRef]
- Sánchez, A.; Vázquez, A. Bioactive Peptides: A Review. Food Qual. Saf. 2017, 1, 29–46. [Google Scholar] [CrossRef]
- Dave, L.A.; Hayes, M.; Montoya, C.A.; Rutherfurd, S.M.; Moughan, P.J. Human Gut Endogenous Proteins as a Potential Source of Angiotensin-I-Converting Enzyme (ACE-I)-, Renin Inhibitory and Antioxidant Peptides. Peptides 2016, 76, 30–44. [Google Scholar] [CrossRef] [PubMed]
- Guha, S.; Majumder, K. Structural-Features of Food-Derived Bioactive Peptides with Anti-Inflammatory Activity: A Brief Review. J. Food Biochem. 2019, 43, e12531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jia, L.; Wang, L.; Liu, C.; Liang, Y.; Lin, Q. Bioactive Peptides from Foods: Production, Function, and Application. Food Funct. 2021, 12, 7108–7125. [Google Scholar] [CrossRef] [PubMed]
- Chakrabarti, S.; Guha, S.; Majumder, K. Food-Derived Bioactive Peptides in Human Health: Challenges and Opportunities. Nutrients 2018, 10, 1738. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fernández-Tomé, S.; Hernández-Ledesma, B.; Chaparro, M.; Indiano-Romacho, P.; Bernardo, D.; Gisbert, J.P. Role of Food Proteins and Bioactive Peptides in Inflammatory Bowel Disease. Trends Food Sci. Technol. 2019, 88, 194–206. [Google Scholar] [CrossRef]
- Dargahi, N.; Johnson, J.C.; Apostolopoulos, V. Immune Modulatory Effects of Probiotic Streptococcus thermophilus on Human Monocytes. Biologics 2021, 1, 23. [Google Scholar] [CrossRef]
- Han, F.; Wu, G.; Zhang, Y.; Zheng, H.; Han, S.; Li, X.; Cai, W.; Liu, J.; Zhang, W.; Zhang, X.; et al. Streptococcus thermophilus Attenuates Inflammation in Septic Mice Mediated by Gut Microbiota. Front. Microbiol. 2020, 11, 598010. [Google Scholar] [CrossRef]
- Piqué, N.; Berlanga, M.; Miñana-Galbis, D. Health Benefits of Heat-Killed (Tyndallized) Probiotics: An Overview. Int. J. Mol. Sci. 2019, 20, 2534. [Google Scholar] [CrossRef] [Green Version]
- Junjua, M.; Kechaou, N.; Chain, F.; Awussi, A.A.; Roussel, Y.; Perrin, C.; Roux, E.; Langella, P.; Bermúdez-Humarán, L.G.; Le Roux, Y.; et al. A Large Scale In vitro Screening of Streptococcus thermophilus Strains Revealed Strains with a High Anti-Inflammatory Potential. LWT Food Sci. Technol. 2016, 70, 78–87. [Google Scholar] [CrossRef]
- Li, P.; Yu, Q.; Ye, X.; Wang, Z.; Yang, Q. Lactobacillus S-Layer Protein Inhibition of Salmonella-Induced Reorganization of the Cytoskeleton and Activation of MAPK Signalling Pathways in Caco-2 Cells. Microbiology 2011, 157, 2639–2646. [Google Scholar] [CrossRef]
- do Carmo, F.L.R.; Rabah, H.; Cordeiro, B.F.; da Silva, S.H.; Pessoa, R.M.; Fernandes, S.O.A.; Cardoso, V.N.; Gagnaire, V.; Deplanche, M.; Savassi, B.; et al. Probiotic Propionibacterium freudenreichii Requires SlpB Protein to Mitigate Mucositis Induced by Chemotherapy. Oncotarget 2019, 10, 7198–7219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Siciliano, R.A.; Lippolis, R.; Mazzeo, M.F. Proteomics for the Investigation of Surface-Exposed Proteins in Probiotics. Front. Nutr. 2019, 6, 52. [Google Scholar] [CrossRef] [PubMed]
- Tjalsma, H.; Lambooy, L.; Hermans, P.W.; Swinkels, D.W. Shedding & Shaving: Disclosure of Proteomic Expressions on a Bacterial Face. Proteomics 2008, 8, 1415–1428. [Google Scholar] [CrossRef] [PubMed]
- Allouche, R.; Hafeez, Z.; Papier, F.; Dary-Mourot, A.; Genay, M.; Miclo, L. In Vitro Anti-Inflammatory Activity of Peptides Obtained by Tryptic Shaving of Surface Proteins of Streptococcus thermophilus LMD-9. Foods 2022, 11, 1157. [Google Scholar] [CrossRef] [PubMed]
- Terzaghi, B.E.; Sandine, W.E. Improved Medium for Lactic Streptococci and Their Bacteriophages. Appl. Microbiol. 1975, 29, 807–813. [Google Scholar] [CrossRef] [PubMed]
- Lecomte, X.; Gagnaire, V.; Briard-Bion, V.; Jardin, J.; Lortal, S.; Dary, A.; Genay, M. The Naturally Competent Strain Streptococcus thermophilus LMD-9 as a New Tool to Anchor Heterologous Proteins on the Cell Surface. Microb. Cell Factories 2014, 13, 82. [Google Scholar] [CrossRef] [Green Version]
- Serhan, C.N.; Savill, J. Resolution of Inflammation: The Beginning Programs the End. Nat. Immunol. 2005, 6, 1191–1197. [Google Scholar] [CrossRef]
- Wang, B.; Gong, X.; Wan, J.; Zhang, L.; Zhang, Z.; Li, H.; Min, S. Resolvin D1 Protects Mice from LPS-Induced Acute Lung Injury. Pulm. Pharmacol. Ther. 2011, 24, 434–441. [Google Scholar] [CrossRef]
- Gao, X.; Wang, F.; Zhao, P.; Zhang, R.; Zeng, Q. Effect of Heat-Killed Streptococcus thermophilus on Type 2 Diabetes Rats. PeerJ 2019, 7, e7117. [Google Scholar] [CrossRef] [Green Version]
- Sanchón, J.; Fernández-Tomé, S.; Miralles, B.; Hernández-Ledesma, B.; Tomé, D.; Gaudichon, C.; Recio, I. Protein Degradation and Peptide Release from Milk Proteins in Human Jejunum. Comparison with in Vitro Gastrointestinal Simulation. Food Chem. 2018, 239, 486–494. [Google Scholar] [CrossRef]
- Samtiya, M.; Acharya, S.; Pandey, K.K.; Aluko, R.E.; Udenigwe, C.C.; Dhewa, T. Production, Purification, and Potential Health Applications of Edible Seeds’ Bioactive Peptides: A Concise Review. Foods 2021, 10, 2696. [Google Scholar] [CrossRef] [PubMed]
- Keil, B. Specificity of Proteolysis; Springer: Berlin/Heidelberg, Germany, 1992; p. 335. ISBN 978-3-642-48382-0. [Google Scholar]
- Mahvi, D.A.; Mahvi, D.M. Stomach. In Sabiston Textbook of Surgery; Elsevier: Philadelphia, PA, USA, 2021; pp. 1196–1239. ISBN 978-0-323-64062-6. [Google Scholar]
- Olsen, J.V.; Ong, S.-E.; Mann, M. Trypsin Cleaves Exclusively C-Terminal to Arginine and Lysine Residues. Mol. Cell. Proteom. 2004, 3, 608–614. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olaya-Abril, A.; Jiménez-Munguía, I.; Gómez-Gascón, L.; Rodríguez-Ortega, M.J. Surfomics: Shaving Live Organisms for a Fast Proteomic Identification of Surface Proteins. J. Proteom. 2014, 97, 164–176. [Google Scholar] [CrossRef] [PubMed]
- Chhatwal, G.S. Anchorless Adhesins and Invasins of Gram-Positive Bacteria: A New Class of Virulence Factors. Trends Microbiol. 2002, 10, 205–208. [Google Scholar] [CrossRef]
- Henderson, B.; Martin, A. Bacterial Virulence in the Moonlight: Multitasking Bacterial Moonlighting Proteins Are Virulence Determinants in Infectious Disease. Infect. Immun. 2011, 79, 3476–3491. [Google Scholar] [CrossRef] [Green Version]
- Jeffery, C.J. Moonlighting Proteins—An Update. Mol. BioSyst. 2009, 5, 345. [Google Scholar] [CrossRef]
- Wang, W.; Jeffery, C.J. An Analysis of Surface Proteomics Results Reveals Novel Candidates for Intracellular/Surface Moonlighting Proteins in Bacteria. Mol. BioSyst. 2016, 12, 1420–1431. [Google Scholar] [CrossRef]
- Weidenmaier, C.; Peschel, A. Teichoic Acids and Related Cell-Wall Glycopolymers in Gram-Positive Physiology and Host Interactions. Nat. Rev. Microbiol. 2008, 6, 276–287. [Google Scholar] [CrossRef]
- Henningham, A.; Chiarot, E.; Gillen, C.M.; Cole, J.N.; Rohde, M.; Fulde, M.; Ramachandran, V.; Cork, A.J.; Hartas, J.; Magor, G.; et al. Conserved Anchorless Surface Proteins as Group A Streptococcal Vaccine Candidates. J. Mol. Med. 2012, 90, 1197–1207. [Google Scholar] [CrossRef] [Green Version]
- Hidalgo-Cantabrana, C.; Moro-García, M.A.; Blanco-Míguez, A.; Fdez-Riverola, F.; Oliván, M.; Royo, L.J.; Riestra, S.; Margolles, A.; Lourenço, A.; Alonso-Arias, R.; et al. The Extracellular Proteins of Lactobacillus acidophilus DSM 20079T Display Anti-Inflammatory Effect in Both in Piglets, Healthy Human Donors and Crohn’s Disease Patients. J. Funct. Foods 2020, 64, 103660. [Google Scholar] [CrossRef]
- Fernandez, E.M.; Valenti, V.; Rockel, C.; Hermann, C.; Pot, B.; Boneca, I.G.; Grangette, C. Anti-Inflammatory Capacity of Selected Lactobacilli in Experimental Colitis Is Driven by NOD2-Mediated Recognition of a Specific Peptidoglycan-Derived Muropeptide. Gut 2011, 60, 1050–1059. [Google Scholar] [CrossRef] [PubMed]
- Kim, E.; Lee, H.G.; Han, S.; Seo, K.-H.; Kim, H. Effect of Surface Layer Proteins Derived from Paraprobiotic Kefir Lactic Acid Bacteria on Inflammation and High-Fat Diet-Induced Obesity. J. Agric. Food Chem. 2021, 69, 15157–15164. [Google Scholar] [CrossRef] [PubMed]
- Ricciotti, E.; FitzGerald, G.A. Prostaglandins and Inflammation. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 986–1000. [Google Scholar] [CrossRef]
- Boonma, P.; Spinler, J.K.; Venable, S.F.; Versalovic, J.; Tumwasorn, S. Lactobacillus rhamnosus L34 and Lactobacillus casei L39 Suppress Clostridium Difficile-Induced IL-8 Production by Colonic Epithelial Cells. BMC Microbiol. 2014, 14, 177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mojica, L.; de Mejía, E.G. Optimization of Enzymatic Production of Anti-Diabetic Peptides from Black Bean (Phaseolus vulgaris L.) Proteins, Their Characterization and Biological Potential. Food Funct. 2016, 7, 713–727. [Google Scholar] [CrossRef] [PubMed]
- Mudgil, P.; Baby, B.; Ngoh, Y.-Y.; Kamal, H.; Vijayan, R.; Gan, C.-Y.; Maqsood, S. Molecular Binding Mechanism and Identification of Novel Anti-Hypertensive and Anti-Inflammatory Bioactive Peptides from Camel Milk Protein Hydrolysates. LWT 2019, 112, 108193. [Google Scholar] [CrossRef]
- Guevarra, R.B.; Barraquio, V.L. Viable Counts of Lactic Acid Bacteria in Philippine Commercial Yogurts. Int. J. Dairy Process. Res. 2015, 2, 24–28. [Google Scholar] [CrossRef]
LMD-9 | CNRZ-21N | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
Protein ID | New Locus Number | Description | MW (kDa) | Location | Nb Specific Sequences Identified | Coverage (%) | Nb Specific Sequences Identified | Coverage (%) | ||
Nucleotide metabolism and transport | ||||||||||
STER_0198|ID:1898877| | STER_RS00970 | 2′:3′-cyclic-nucleotide 2′-phosphodiesterase (modular protein) | 91.21 | CS | 205 | 75.44 | ||||
STER_1118|ID:1899510|fliY| | STER_RS05530 | Cystine transporter subunit; periplasmic-binding component of ABC superfamily | 30.94 | Cyto | 13 | 42.09 | ||||
Post-translational modification, protein turnover and chaperone function | ||||||||||
STER_0846|ID:1899371| | STER_RS04165 | Exported protein of unknown function (subtilisin-like serine protease PrtS) | 173.05 | CS | 343 | 74.80 | ||||
STER_0253|ID:1898921|groL| | STER_RS01230 | Cpn60 chaperonin GroEL, large subunit of GroESL | 56.89 | Cyto | 14 | 22.78 | 17 | 31.11 | ||
STER_2002|ID:1899687|degP| | STER_RS09790 | Serine endoprotease (protease Do), membrane-associated | 42.77 | CM/M | 14 | 30.10 | ||||
Translation | ||||||||||
STER_0524|ID:1899138|tufB| | STER_RS02570 | Protein chain elongation factor EF-Tu (duplicate of tufA) | 43.84 | Cyto | 14 | 35.34 | ||||
STER_1904|ID:1900567|rplB| | STER_RS09330 | 50S ribosomal subunit protein L2 | 29.91 | Cyto | 8 | 29.50 | ||||
STER_0568|ID:1899173|rplL| | STER_RS02800 | 50S ribosomal subunit protein L7/L12 | 12.35 | Cyto | 21 | 61.79 | ||||
STER_1936|ID:1899661| | STER_RS09470 | 50S ribosomal protein L28 | 6.91 | Cyto | 18 | 96.83 | 8 | 61.91 | ||
STER_1899|ID:1900562|rpmC| | STER_RS09305 | 50S ribosomal subunit protein L29 | 7.90 | Cyto | 12 | 68.12 | ||||
STER_1889|ID:1900552|rpmD| | STER_RS09255 | 50S ribosomal subunit protein L30 | 6.39 | Cyto | 51 | 88.53 | 9 | 44.26 | ||
STER_1953|ID:1899670|rpmF| | STER_RS09555 | 50S ribosomal subunit protein L32 | 6.78 | Cyto | 12 | 83.61 | ||||
STER_1954|ID:1899671|rpmG| | STER_RS09560 | 50S ribosomal subunit protein L33 | 5.92 | Cyto | 19 | 92.00 | ||||
STER_1894|ID:1900557| | STER_RS09280 | 30S ribosomal protein S14 type Z (BS21) | 7.07 | Cyto | 11 | 82.26 | ||||
STER_0850|ID:1899831|rpsT| | STER_RS04185 | 30S ribosomal subunit protein S20 | 8.40 | Cyto | 10 | 82.28 | 10 | 89.87 | ||
STHERMOCNRZ21N_v1_31103|ID:59661243|rplX| | Ribosomal protein L24 (BL23) | 10.86 | Cyto | 16 | 69.61 | |||||
Carbohydrate metabolism and transport | ||||||||||
STER_0684|ID:1899266|eno| | STER_RS03365 | Enolase | 46.95 | CS/M/Cyto | 10 | 22.30 | 8 | 19.08 | ||
STER_1243|ID:1900052| | STER_RS06135 | Phosphocarrier protein HPr (histidine-containing protein) | 8.91 | Cyto | 35 | 98.86 | 17 | 98.86 | ||
STER_1876|ID:1900541|kbaY| | STER_RS09185 | Tagatose 6-phosphate aldolase 1, kbaY subunit | 31.51 | Cyto | 10 | 31.63 | 8 | 30.27 | ||
Cell wall/membrane/envelope biogenesis | ||||||||||
STER_0042|ID:1898743| | STER_RS00210 | Secreted 45 kDa protein precursor | 46.45 | CS | 12 | 28.73 | ||||
Amino acid transport and metabolism | ||||||||||
STER_1411|ID:1900180| | STER_RS06940 | Putative transporter subunit: periplasmic-binding component of ABC superfamily | 72.18 | CS | 14 | 45.59 | ||||
STHERMOCNRZ21N_v1_30588|ID:59660728|amiA| | Oligopeptide-binding protein AmiA | 71.92 | CS/M | 12 | 35.98 | |||||
STHERMOCNRZ21N_v1_30299|ID:59660439| | Polar amino acid ABC uptake transporter substrate binding protein | 30.99 | CS | 8 | 32.73 | |||||
STER_0340|ID:1898987|metQ| | STER_RS01655 | DL-methionine transporter subunit; periplasmic-binding component of ABC superfamily | 3.89 | M | 10 | 33.22 | ||||
Transport | ||||||||||
STER_1539|ID:1900277| | STER_RS07565 | Glutamine-binding protein precursor (GlnBP) | 31.30 | CS | 17 | 44.91 | ||||
STHERMOCNRZ21N_v1_10277|ID:59659427|nupN| | Lipoprotein involved in guanosine transport | 37.64 | CS | 12 | 33.33 | |||||
Energy production and conversion | ||||||||||
STER_0519|ID:1899133|atpA| | STER_RS02545 | F1 sector of membrane-bound ATP synthase, alpha subunit | 54.54 | CM | 14 | 27.49 | ||||
STER_0521|ID:1899135|atpD| | STER_RS02555 | F1 sector of membrane-bound ATP synthase, beta subunit | 50.84 | CM | 10 | 24.73 | ||||
Unknown or other function | ||||||||||
STER_1963|ID:1899676| | STER_RS09605 | Conserved protein of unknown function (CsbD family protein) | 7.08 | Cyto | 49 | 97.06 | ||||
STER_1141|ID:1899514| | STER_RS10465 | Exported protein of unknown function | 6.26 | _ | 12 | 71.19 | ||||
STER_0856|ID:1899377| | STER_RS04220 | CD4+ T-cell-stimulating antigen precursor | 37.62 | CS | 25 | 55.18 | 12 | 33.33 | ||
STER_0576|ID:1899177| | STER_RS02840 | Mucus binding protein precursor (fragment) | 108.40 | CS | 58 | 56.17 | ||||
STER_0478|ID:1899094| | STER_RS02350 | Exported protein of unknown function | 50.50 | CS | 21 | 63.00 | ||||
STER_0378|ID:1899011| | STER_RS01835 | Membrane-bound protein LytR (modular protein) | 43.94 | Cyto | 18 | 34.23 | ||||
STER_0715|ID:1899786| | Protein of unknown function | 4.92 | _ | 10 | 81.82 | |||||
STHERMOCNRZ21N_v1_10861|ID:59660011|mapZ| | Mid-cell-anchored protein Z | 66.10 | CM/M | 8 | 15.46 |
LMD-9 | CNRZ-21 | |||||||
---|---|---|---|---|---|---|---|---|
Protein Id | New Locus Number | Description | MW (kDa) | Location | Nb Specific Sequences Identified | Coverage (%) | Nb Specific Sequences Identified | Coverage (%) |
Post-translational modification, protein turnover, chaperone function | ||||||||
STER_0846|ID:1899371| | STER_RS04165 | Exported protein of unknown function (subtilisin-like serine protease PrtS) | 173.05 | CS | 190 | 62.26 | ||
STER_2002|ID:1899687|degP| | STER_RS09790 | Serine endoprotease (protease Do), membrane-associated | 42.77 | CM/M | 19 | 40.05 | ||
STER_0253|ID:1898921|groL| | STER_RS01230 | Cpn60 chaperonin GroEL, large subunit of GroESL | 56.89 | Cyto | 9 | 17.59 | 18 | 34.44 |
STER_0648|ID:1899776|clpA| | STER_RS03195 | ATPase and specificity subunit of ClpA-ClpP ATP-dependent serine protease, chaperone activity | 83.69 | _ | 9 | 5.98 | ||
STER_0163|ID:1898844|dnaK| | STER_RS00790 | Chaperone Hsp70, co-chaperone with DnaJ | 64.76 | Cyto | 10 | 10.86 | 8 | 19.57 |
Nucleotide metabolism and transport | ||||||||
STER_0198|ID:1898877| | STER_RS00970 | 2′:3′-cyclic-nucleotide 2′-phosphodiesterase (modular protein) | 91.21 | CS | 152 | 59.15 | ||
Cell wall/membrane/envelope biogenesis | ||||||||
STER_0042|ID:1898743| | STER_RS00210 | Secreted 45 kDa protein precursor | 46.45 | CM | 25 | 46.05 | ||
Energy production and conversion | ||||||||
STER_0519|ID:1899133|atpA| | STER_RS02545 | F1 sector of membrane-bound ATP synthase, alpha subunit | 54.54 | CM | 14 | 27.49 | 11 | 24.10 |
STER_0521|ID:1899135|atpD| | STER_RS02555 | F1 sector of membrane-bound ATP synthase, beta subunit | 50.84 | CM | 10 | 24.73 | 13 | 34.76 |
Transport | ||||||||
STER_0340|ID:1898987|metQ| | STER_RS01655 | DL-methionine transporter subunit; periplasmic-binding component of ABC superfamily | 32.89 | M | 10 | 33.22 | 9 | 32.23 |
STHERMOCNRZ21N_v1_10277|ID:59659427|nupN| | Lipoprotein involved in guanosine transport | 37.64 | CS | 12 | 33.33 | 14 | 40.62 | |
STHERMOCNRZ21N_v1_30299|ID:59660439| | Polar amino acid ABC uptake transporter substrate binding protein | 30.99 | CS | 8 | 32.73 | |||
STHERMOCNRZ21N_v1_30588|ID:59660728|amiA| | Oligopeptide-binding protein AmiA | 71.92 | CS | 14 | 43.29 | |||
STHERMOCNRZ21N_v1_10753|ID:59659903|livJ| | Branched-chain amino acid ABC uptake transporter substrate-binding protein | 41.81 | CS/M | 8 | 23.98 | |||
Translation | ||||||||
STER_1889|ID:1900552|rpmD| | STER_RS09255 | 50S ribosomal subunit protein L30 | 6.39 | Cyto | 9 | 44.26 | 10 | 57.38 |
STHERMOCNRZ21N_v1_31096|ID:59661236|rpmD| | Ribosomal protein L30 (BL27) | 6.39 | Cyto | 18 | 81.97 | |||
STER_0639|ID:1899231| | STER_RS03135 | 40S ribosomal protein S1 | 43.88 | Cyto | 8 | 7.48 | ||
STER_1904|ID:1900567|rplB| | STER_RS09330 | 50S ribosomal subunit protein L2 | 29.91 | Cyto | 8 | 29.5 | 9 | 36.33 |
STER_0568|ID:1899173|rplL| | STER_RS02800 | 50S ribosomal subunit protein L7/L12 | 12.35 | Cyto | 8 | 59.35 | 11 | 48.78 |
STER_0850|ID:1899831|rpsT| | STER_RS04185 | 30S ribosomal subunit protein S20 | 8.40 | Cyto | 10 | 89.87 | 9 | 89.87 |
STER_1905|ID:1900568|rplW| | STER_RS09335 | 50S ribosomal subunit protein L23 | 10.78 | Cyto | 8 | 45.46 | ||
STHERMOCNRZ21N_v1_31103|ID:59661243|rplX| | Ribosomal protein L24 (BL23) | 10.86 | Cyto | 16 | 69.61 | 21 | 80.39 | |
Carbohydrate metabolism and transport | ||||||||
STER_1243|ID:1900052| | STER_RS06135 | Phosphocarrier protein HPr (Histidine-containing protein) | 8.91 | Cyto | 11 | 60.23 | 19 | 98.86 |
STER_0684|ID:1899266|eno| | STER_RS03365 | Enolase | 46.95 | CS/M/Cyto | 9 | 26.44 | ||
Unknown or other function | ||||||||
STER_0856|ID:1899377| | STER_RS04220 | CD4+ T-cell-stimulating antigen precursor | 37.62 | CS | 14 | 40.62 | ||
STER_0576|ID:1899177| | STER_RS02840 | Mucus binding protein precursor (fragment) | 108.4 | CS | 66 | 45.24 | ||
STER_0478|ID:1899094| | Exported protein of unknown function | 50.50 | _ | 14 | 42.00 | |||
STER_1317|ID:1899536| | Conserved protein of unknown function | 6.81 | _ | 11 | 80.00 | |||
STHERMOCNRZ21N_v1_10861|ID:59660011|mapZ| | Mid-cell-anchored protein Z | 66.10 | CM/M | 8 | 15.46 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Allouche, R.; Genay, M.; Dary-Mourot, A.; Hafeez, Z.; Miclo, L. Cell Proteins Obtained by Peptic Shaving of Two Phenotypically Different Strains of Streptococcus thermophilus as a Source of Anti-Inflammatory Peptides. Nutrients 2022, 14, 4777. https://doi.org/10.3390/nu14224777
Allouche R, Genay M, Dary-Mourot A, Hafeez Z, Miclo L. Cell Proteins Obtained by Peptic Shaving of Two Phenotypically Different Strains of Streptococcus thermophilus as a Source of Anti-Inflammatory Peptides. Nutrients. 2022; 14(22):4777. https://doi.org/10.3390/nu14224777
Chicago/Turabian StyleAllouche, Rania, Magali Genay, Annie Dary-Mourot, Zeeshan Hafeez, and Laurent Miclo. 2022. "Cell Proteins Obtained by Peptic Shaving of Two Phenotypically Different Strains of Streptococcus thermophilus as a Source of Anti-Inflammatory Peptides" Nutrients 14, no. 22: 4777. https://doi.org/10.3390/nu14224777