{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T20:00:06Z","timestamp":1792872006932,"version":"4.5.0"},"reference-count":92,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,11,30]],"date-time":"2022-11-30T00:00:00Z","timestamp":1669766400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"California Table Grape Commission"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antioxidants"],"abstract":"<jats:p>Over three million Americans are affected by skin cancer each year, largely as a result of exposure to sunlight. The purpose of this study was to determine the potential of grape consumption to modulate UV-induced skin erythema. With 29 human volunteers, we report that nine demonstrated greater resistance to UV irradiation of the skin after consuming the equivalent of three servings of grapes per day for two weeks. We further explored any potential relationship to the gut\u2013skin axis. Alpha- and beta-diversity of the gut microbiome were not altered, but grape consumption modulated microbiota abundance, enzyme levels, and KEGG pathways. Striking differences in the microbiome and metabolome were discerned when comparing the nine individuals showing greater UV resistance with the 20 non-responders. Notably, three urinary metabolites, 2\u2032-deoxyribonic acid, 3-hydroxyphenyl acetic and scyllo-inositol, were depressed in the UV-resistant group. A ROC curve revealed a 71.8% probability that measurement of urinary 2\u2032-deoxyribonic acid identifies a UV skin non-responder. 2\u2032-Deoxyribonic acid is cleaved from the DNA backbone by reactive oxygen species. Three of the nine subjects acquiring UV resistance following grape consumption showed a durable response, and these three demonstrated unique microbiomic and metabolomic profiles. Variable UV skin sensitivity was likely due to glutathione S-transferase polymorphisms. We conclude that a segment of the population is capable of demonstrating greater resistance to a dermal response elicited by UV irradiation as a result of grape consumption. It is uncertain if modulation of the gut-skin axis leads to enhanced UV resistance, but there is correlation. More broadly, it is reasonable to expect that these mechanisms relate to other health outcomes anticipated to result from grape consumption.<\/jats:p>","DOI":"10.3390\/antiox11122372","type":"journal-article","created":{"date-parts":[[2022,11,30]],"date-time":"2022-11-30T05:45:22Z","timestamp":1669787122000},"page":"2372","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Short-Term Grape Consumption Diminishes UV-Induced Skin Erythema"],"prefix":"10.3390","volume":"11","author":[{"given":"John M.","family":"Pezzuto","sequence":"first","affiliation":[{"name":"College of Pharmacy and Health Sciences, Western New England University, Springfield, MA 01119, USA"},{"name":"Department of Medicine, UMass Chan Medical School\u2014Baystate, Springfield, MA 01199, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asim","family":"Dave","sequence":"additional","affiliation":[{"name":"Immunology Program, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eun-Jung","family":"Park","sequence":"additional","affiliation":[{"name":"Division of Pharmaceutical Sciences, Arnold & Marie Schwartz College of Pharmacy and Health Sciences, Long Island University, Brooklyn, NY 11201, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diren","family":"Beyo\u011flu","sequence":"additional","affiliation":[{"name":"College of Pharmacy and Health Sciences, Western New England University, Springfield, MA 01119, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6143-1520","authenticated-orcid":false,"given":"Jeffrey R.","family":"Idle","sequence":"additional","affiliation":[{"name":"College of Pharmacy and Health Sciences, Western New England University, Springfield, MA 01119, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,30]]},"reference":[{"key":"ref_1","unstructured":"(2022, November 14). Healthy Diet. Available online: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/healthy-diet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1126\/science.275.5297.218","article-title":"Cancer chemopreventive activity of resveratrol, a natural product derived from grapes","volume":"275","author":"Jang","year":"1997","journal-title":"Science"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1016\/j.bbadis.2015.01.014","article-title":"The pharmacology of resveratrol in animals and humans","volume":"1852","author":"Park","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"6777","DOI":"10.1021\/jf800898p","article-title":"Grapes and human health: A perspective","volume":"56","author":"Pezzuto","year":"2008","journal-title":"J. Agric. Food Chem."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Pezzuto, J.M. (2016). Grapes and Health, Springer.","DOI":"10.1007\/978-3-319-28995-3"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1992","DOI":"10.1210\/en.2017-03230","article-title":"How UV light touches the brain and endocrine system through skin, and why","volume":"159","author":"Slominski","year":"2018","journal-title":"Endocrinology"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1002\/ijc.32921","article-title":"Cutaneous melanomas attributable to ultraviolet radiation exposure by state","volume":"147","author":"Islami","year":"2020","journal-title":"Int. J. Cancer"},{"key":"ref_8","unstructured":"(2022, October 15). Skin Cancer. Available online: https:\/\/www.aad.org\/media\/stats-skin-cancer."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4062\/biomolther.2018.176","article-title":"Resveratrol: Twenty years of growth, development and controversy","volume":"27","author":"Pezzuto","year":"2019","journal-title":"Biomol. Ther."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/j.jid.2018.09.028","article-title":"Chemoprotective effects of dietary grape powder on UVB radiation-mediated skin carcinogenesis in SKH-1 hairless mice","volume":"139","author":"Singh","year":"2019","journal-title":"J. Investig. Dermatol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3741","DOI":"10.1021\/acs.jproteome.9b00442","article-title":"Identification of molecular targets of dietary grape-mediated chemoprevention of ultraviolet B skin carcinogenesis: A comparative quantitative proteomics analysis","volume":"18","author":"Mintie","year":"2019","journal-title":"J. Proteome Res."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Mintie, C.A., Musarra, A.K., Singh, C.K., Ndiaye, M.A., Sullivan, R., Eickhoff, J.C., and Ahmad, N. (2020). Protective effects of dietary grape on UVB-mediated cutaneous damages and skin tumorigenesis in SKH-1 mice. Cancers, 12.","DOI":"10.3390\/cancers12071751"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1016\/j.jaad.2021.01.035","article-title":"Dietary table grape protects against ultraviolet photodamage in humans: 1. Clinical evaluation","volume":"85","author":"Oak","year":"2021","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1016\/j.jaad.2021.01.036","article-title":"Dietary table grape protects against ultraviolet photodamage in humans: 2. Molecular biomarker studies","volume":"85","author":"Oak","year":"2021","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_15","unstructured":"Pezzuto, J.M. (2016). Standardized Grape powder for basic and clinical research. Grapes and Health, Springer International Publishing."},{"key":"ref_16","unstructured":"Dave, A., Beyo\u011flu, D., Park, E.-J., Idle, J.R., and Pezzuto, J.M. Influence of grape consumption on the human microbiome, submitted."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"8489","DOI":"10.1039\/D2FO00961G","article-title":"Addition of grapes to both a standard and a high-fat Western pattern diet modifies hepatic and urinary metabolite profiles in the mouse","volume":"13","author":"Park","year":"2022","journal-title":"Food Funct."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Dave, A., Park, E.-J., Kumar, A., Parande, F., Beyo\u011flu, D., Idle, J.R., and Pezzuto, J.M. (2022). Consumption of grapes modulates gene expression, reduces non-alcoholic fatty liver disease, and extends longevity in female C57BL\/6J mice provided with a high-fat Western-pattern diet. Foods, 11.","DOI":"10.3390\/foods11131984"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1007\/s11306-014-0642-1","article-title":"A statistical analysis of the effects of urease pre-treatment on the measurement of the urinary metabolome by gas chromatography-mass spectrometry","volume":"10","author":"Kim","year":"2014","journal-title":"Metabolomics"},{"key":"ref_20","first-page":"21","article-title":"Estimating the size of treatment effects","volume":"6","author":"McGough","year":"2009","journal-title":"Psychiatry"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1111\/srt.12199","article-title":"Skin colour, skin redness and melanin biometric measurements: Comparison study between Antera\u00ae 3D, Mexameter\u00ae and Colorimeter\u00ae","volume":"21","author":"Matias","year":"2015","journal-title":"Skin Res. Technol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Vacca, M., Celano, G., Calabrese, F.M., Portincasa, P., Gobbetti, M., and De Angelis, M. (2020). The Controversial role of human gut Lachnospiraceae. Microorganisms, 8.","DOI":"10.3390\/microorganisms8040573"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Barrett, H.L., Gomez-Arango, L.F., Wilkinson, S.A., McIntyre, H.D., Callaway, L.K., Morrison, M., and Dekker Nitert, M. (2018). A vegetarian diet is a major determinant of gut microbiota composition in early pregnancy. Nutrients, 10.","DOI":"10.3390\/nu10070890"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/s13073-020-00758-x","article-title":"High-resolution temporal profiling of the human gut microbiome reveals consistent and cascading alterations in response to dietary glycans","volume":"12","author":"Creswell","year":"2020","journal-title":"Genome Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1038\/s41396-019-0363-6","article-title":"Genomic insights from Monoglobus pectinilyticus: A pectin-degrading specialist bacterium in the human colon","volume":"13","author":"Kim","year":"2019","journal-title":"ISME J."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Koliarakis, I., Messaritakis, I., Nikolouzakis, T.K., Hamilos, G., Souglakos, J., and Tsiaoussis, J. (2019). Oral bacteria and intestinal dysbiosis in colorectal cancer. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20174146"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1875796","DOI":"10.1080\/19490976.2021.1875796","article-title":"Blautia\u2014A new functional genus with potential probiotic properties?","volume":"13","author":"Liu","year":"2021","journal-title":"Gut Microbes"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/s12275-018-0577-8","article-title":"Gut microbiomes and their metabolites shape human and animal health","volume":"56","author":"Park","year":"2018","journal-title":"J. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1016\/j.celrep.2018.12.028","article-title":"Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids","volume":"26","author":"Wang","year":"2019","journal-title":"Cell Rep."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1666","DOI":"10.3389\/fmicb.2017.01666","article-title":"Secretome of intestinal Bacilli: A natural guard against pathologies","volume":"8","author":"Ilinskaya","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"27572","DOI":"10.1038\/srep27572","article-title":"Accelerated dysbiosis of gut microbiota during aggravation of DSS-induced colitis by a butyrate-producing bacterium","volume":"6","author":"Zhang","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1412","DOI":"10.1136\/gutjnl-2021-326264","article-title":"Cancer pharmacomicrobiomics: Targeting microbiota to optimise cancer therapy outcomes","volume":"71","author":"Ting","year":"2022","journal-title":"Gut"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Huang, F., Qiao, H., Yin, J., Gao, Y., Ju, Y., and Li, Y. (2015). Early-life exposure to Clostridium leptum causes pulmonary immunosuppression. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0141717"},{"key":"ref_34","first-page":"678","article-title":"Bacteroides dorei dominates gut microbiome prior to autoimmunity in Finnish children at high risk for type 1 diabetes","volume":"5","author":"Ardissone","year":"2014","journal-title":"Front. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1016\/j.immuni.2016.09.009","article-title":"Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects","volume":"45","author":"Waldschmitt","year":"2016","journal-title":"Immunity"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1038\/s41385-020-0296-4","article-title":"Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation","volume":"14","author":"Iljazovic","year":"2021","journal-title":"Mucosal Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"476","DOI":"10.3389\/fcimb.2019.00476","article-title":"The oral microbiota may have influence on oral cancer","volume":"9","author":"Zhang","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"902","DOI":"10.1093\/ibd\/izy318","article-title":"An increased abundance of Clostridiaceae characterizes arthritis in inflammatory bowel disease and rheumatoid arthritis: A cross-sectional study","volume":"25","author":"Chen","year":"2019","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1099\/ijsem.0.003698","article-title":"Reclassification of the Clostridium clostridioforme and Clostridium sphenoides clades as Enterocloster gen. nov. and Lacrimispora gen. nov., including reclassification of 15 taxa","volume":"70","author":"Haas","year":"2020","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"5206","DOI":"10.1038\/s41467-020-18871-1","article-title":"Health and disease markers correlate with gut microbiome composition across thousands of people","volume":"11","author":"Manor","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"598010","DOI":"10.3389\/fmicb.2020.598010","article-title":"Streptococcus thermophilus attenuates inflammation in septic mice mediated by gut microbiota","volume":"11","author":"Han","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1177\/1756283X12454590","article-title":"The intestinal microbiota dysbiosis and Clostridium difficile infection: Is there a relationship with inflammatory bowel disease?","volume":"6","author":"Bien","year":"2013","journal-title":"Therap. Adv. Gastroenterol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1093\/nass\/49.1.179","article-title":"Reactivity of 2\u2032-deoxyuridin-1\u2032-yl radical in various DNA structures","volume":"49","author":"Hasiba","year":"2005","journal-title":"Nucleic Acids Symposium. Ser."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1021\/bi00429a016","article-title":"Identification of 2-deoxyribonolactone at the site of neocarzinostatin-induced cytosine release in the sequence d(AGC)","volume":"28","author":"Kappen","year":"1989","journal-title":"Biochemistry"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"953205","DOI":"10.3389\/fphar.2022.953205","article-title":"Best Practice in the chemical characterisation of extracts used in pharmacological and toxicological re-search\u2014The ConPhyMP\u2014Guidelines","volume":"13","author":"Heinrich","year":"2022","journal-title":"Front. Pharmacol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1186\/s12967-017-1175-y","article-title":"Influence of diet on the gut microbiome and implications for human health","volume":"15","author":"Singh","year":"2017","journal-title":"J. Transl. Med."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"47","DOI":"10.3389\/fnut.2019.00047","article-title":"The Effects of vegetarian and vegan diets on gut microbiota","volume":"6","author":"Tomova","year":"2019","journal-title":"Front. Nutr."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"872716","DOI":"10.1155\/2012\/872716","article-title":"Probiotics, prebiotics, and synbiotics: Gut and beyond","volume":"2012","author":"Vyas","year":"2012","journal-title":"Gastroenterol. Res. Pract."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1186\/s40168-019-0620-y","article-title":"A review of 10 years of human microbiome research activities at the US National Institutes of Health, Fiscal Years 2007\u20132016","volume":"7","author":"Proctor","year":"2019","journal-title":"Microbiome"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2096995","DOI":"10.1080\/19490976.2022.2096995","article-title":"Impact of gut microbiome on skin health: Gut-skin axis observed through the lenses of therapeutics and skin diseases","volume":"14","author":"Mahmud","year":"2022","journal-title":"Gut Microbes"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1093\/chromsci\/27.1.23","article-title":"Metabolic profiling of urinary organic acids by single and multicolumn capillary gas chromatography","volume":"27","author":"Lefevere","year":"1989","journal-title":"J. Chromatogr. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1093\/chromsci\/22.5.198","article-title":"Capillary gas chromatographic separation of urinary organic acids. Retention indices of 101 urinary acids on a 5% phenylmethyl silicone capillary column","volume":"22","author":"Tuchman","year":"1984","journal-title":"J. Chromatogr. Sci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"9566","DOI":"10.1021\/bi00451a002","article-title":"A 2-deoxyribonolactone-containing nucleotide: Isolation and characterization of the alkali-sensitive photoproduct of the trideoxyribonucleotide d(ApCpA)","volume":"28","author":"Urata","year":"1989","journal-title":"Biochemistry"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1080\/09553007714551241","article-title":"Isolation of 2-deoxy-d-erythro-pentonic acid from an alkali-labile site in \u03b3-irradiated DNA","volume":"32","author":"Dizdaroglu","year":"1977","journal-title":"Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/14764172.2021.1950767","article-title":"Skin impacts from exposure to ultraviolet, visible, infrared, and artificial lights\u2013a review","volume":"23","author":"Furukawa","year":"2021","journal-title":"J. Cosmet. Laser Ther."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1111\/j.1365-2133.1994.tb13107.x","article-title":"Improved prediction of the minimal phototoxic dose in PUVA therapy","volume":"130","author":"Sakuntabhai","year":"1994","journal-title":"Br. J. Dermatol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"7293","DOI":"10.1073\/pnas.85.19.7293","article-title":"Hereditary differences in the expression of the human glutathione transferase active on trans-stilbene oxide are due to a gene deletion","volume":"85","author":"Vorachek","year":"1988","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1042\/bj3000271","article-title":"Human glutathione S-transferase theta (GSTT1): cDNA cloning and the characterization of a genetic polymorphism","volume":"300","author":"Pemble","year":"1994","journal-title":"Biochem. J."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1111\/1523-1747.ep12335337","article-title":"Deficiency of glutathione S-transferases T1 and M1 as heritable factors of increased cutaneous UV sensitivity","volume":"108","author":"Kerb","year":"1997","journal-title":"J. Investig. Dermatol."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Martinovi\u0107, A., Cocuzzi, R., Arioli, S., and Mora, D. (2020). Streptococcus thermophilus: To survive, or not to survive the gastrointestinal tract, that is the question!. Nutrients, 12.","DOI":"10.3390\/nu12082175"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e00857-19","DOI":"10.1128\/mSystems.00857-19","article-title":"Depletion of Blautia species in the microbiota of obese children relates to intestinal inflammation and metabolic phenotype worsening","volume":"5","author":"Sanz","year":"2020","journal-title":"MSystems"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Bag, S., Ghosh, T.S., and Das, B. (2017). Complete genome sequence of Collinsella aerofaciens isolated from the gut of a healthy Indian subject. Genome Announc., 5.","DOI":"10.1128\/genomeA.01361-17"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1038\/s41588-021-00991-z","article-title":"Combined effects of host genetics and diet on human gut microbiota and incident disease in a single population cohort","volume":"54","author":"Qin","year":"2022","journal-title":"Nat. Genet."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Antezack, A., Boxberger, M., La Scola, B., and Monnet-Corti, V. (2021). Isolation and description of catonella massiliensis sp. nov., a novel catonella species, isolated from a stable periodontitis subject. Pathogens, 10.","DOI":"10.1099\/ijsem.0.005039"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1093\/gbe\/evu050","article-title":"A Phylogenomic View of Ecological Specialization in the Lachnospiraceae, A family of digestive tract-associated bacteria","volume":"6","author":"Meehan","year":"2014","journal-title":"Genome Biol. Evol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1111\/imm.12760","article-title":"The immune response to Prevotella bacteria in chronic inflammatory disease","volume":"151","author":"Larsen","year":"2017","journal-title":"Immunology"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"e2101498118","DOI":"10.1073\/pnas.2101498118","article-title":"Elucidation of an anaerobic pathway for metabolism of l-carnitine\u2013derived \u03b3-butyrobetaine to trimethylamine in human gut bacteria","volume":"118","author":"Rajakovich","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_68","first-page":"325","article-title":"Dysbiosis of fecal microbiota and high frequency of Citrobacter, Klebsiella spp., and Actinomycetes in patients with irritable bowel syndrome and gastroenteritis","volume":"9","author":"Ganji","year":"2016","journal-title":"Gastroenterol. Hepatol. Bed Bench"},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Fakharian, F., Asgari, B., Nabavi-Rad, A., Sadeghi, A., Soleimani, N., Yadegar, A., and Zali, M.R. (2022). The interplay between Helicobacter pylori and the gut microbiota: An emerging driver influencing the immune system homeostasis and gastric carcinogenesis. Front. Cell. Infect. Microbiol., 12, Available online: https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2022.953718.","DOI":"10.3389\/fcimb.2022.953718"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"157","DOI":"10.2217\/fmb-2016-0130","article-title":"Roseburia spp.: A marker of health?","volume":"12","author":"Smida","year":"2017","journal-title":"Future Microbiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.3389\/fmicb.2016.01081","article-title":"The gut microbiota in immune-mediated inflammatory diseases","volume":"7","author":"Forbes","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.ijid.2019.02.001","article-title":"Molecular diagnosis and enrichment culture identified a septic pseudoarthrosis due to an infection with Erysipelatoclostridium ramosum","volume":"81","author":"Zakham","year":"2019","journal-title":"Int. J. Infect. Dis."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"775","DOI":"10.3389\/fphys.2018.00775","article-title":"Understanding the representative gut microbiota dysbiosis in metformin-treated type 2 diabetes patients using genome-scale metabolic modeling","volume":"9","author":"Rosario","year":"2018","journal-title":"Front. Physiol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"e06432","DOI":"10.1016\/j.heliyon.2021.e06432","article-title":"Study of microbiome changes in patients with ulcerative colitis in the Central European part of Russia","volume":"7","author":"Gryaznova","year":"2021","journal-title":"Heliyon"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Bui, T.P.N., Schols, H.A., Jonathan, M., Stams, A.J.M., de Vos, W.M., and Plugge, C.M. (2019). Mutual metabolic interactions in co-cultures of the intestinal Anaerostipes Rhamnosivorans with an acetogen, methanogen, or pectin-degrader affecting butyrate production. Front. Microbiol., 10, Available online: https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2019.02449.","DOI":"10.3389\/fmicb.2019.02449"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/s41467-022-28310-y","article-title":"Gut microbiome of the largest living rodent harbors unprecedented enzymatic systems to degrade plant polysaccharides","volume":"13","author":"Cabral","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"e09102","DOI":"10.1016\/j.heliyon.2022.e09102","article-title":"Peptostreptococcus faecalis sp. nov., new bacterial species isolated from healthy indigenous congolese volunteer","volume":"8","author":"Mekhalif","year":"2022","journal-title":"Heliyon"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1080\/19490976.2017.1406584","article-title":"Low dietary fiber intake increases Collinsella abundance in the gut microbiota of overweight and obese pregnant women","volume":"9","author":"Barrett","year":"2018","journal-title":"Gut Microbes"},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Azad, M., Kalam, A., Sarker, M., Li, T., and Yin, J. (2018). Probiotic species in the modulation of gut microbiota: An overview. Biomed Res. Int., 9478630.","DOI":"10.1155\/2018\/9478630"},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Nie, K., Ma, K., Luo, W., Shen, Z., Yang, Z., Xiao, M., Tong, T., Yang, Y., and Wang, X. (2021). Roseburia intestinalis: A beneficial gut organism from the discoveries in genus and species. Front. Cell. Infect. Microbiol., 11, Available online: https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2021.757718.","DOI":"10.3389\/fcimb.2021.757718"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1830","DOI":"10.3389\/fimmu.2018.01830","article-title":"Aspects of gut microbiota and immune system interactions in infectious diseases, Immunopathology, and Cancer","volume":"9","author":"Lazar","year":"2018","journal-title":"Front Immunol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"104158","DOI":"10.1016\/j.isci.2022.104158","article-title":"Bacteroides ovatus colonization influences the abundance of intestinal short chain fatty acids and neurotransmitters","volume":"25","author":"Horvath","year":"2022","journal-title":"iScience"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Bressa, C., Bail\u00e9n-Andrino, M., P\u00e9rez-Santiago, J., Gonz\u00e1lez-Soltero, R., P\u00e9rez, M., Montalvo-Lominchar, M.G., Mat\u00e9-Mu\u00f1oz, J.L., Dom\u00ednguez, R., Moreno, D., and Larrosa, M. (2017). Differences in gut microbiota profile between women with active lifestyle and sedentary women. PLOS ONE, 12.","DOI":"10.1371\/journal.pone.0171352"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"9351507","DOI":"10.1155\/2017\/9351507","article-title":"Proteobacteria: A common factor in human diseases","volume":"2017","author":"Rizzatti","year":"2017","journal-title":"Biomed Res. Int."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Lai, C.-H., Lin, T.-L., Huang, M.-Z., Li, S.-W., Wu, H.-Y., Chiu, Y.-F., Yang, C.-Y., Chiu, C.-H., and Lai, H.-C. (2022). Gut commensal Parabacteroides goldsteinii mts01 alters gut microbiota composition and reduces cholesterol to mitigate Helicobacter pylori-induced pathogenesis. Front. Immunol., 13, Available online: https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2022.916848.","DOI":"10.3389\/fimmu.2022.916848"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Zamani, S., Taslimi, R., Sarabi, A., Jasemi, S., Sechi, L.A., and Feizabadi, M.M. (2020). Enterotoxigenic Bacteroides fragilis: A possible etiological candidate for bacterially-induced colorectal precancerous and cancerous lesions. Front. Cell. Infect. Microbiol., 9, Available online: https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2019.00449.","DOI":"10.3389\/fcimb.2019.00449"},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Thingholm, L.B., Bang, C., R\u00fchlemann, M.C., Starke, A., Sicks, F., Kaspari, V., Jandowsky, A., Fr\u00f6lich, K., Ismer, G., and Bernhard, A. (2021). Ecology impacts the decrease of Spirochaetes and Prevotella in the fecal gut microbiota of urban humans. BMC Microbiol., 21.","DOI":"10.1186\/s12866-021-02337-5"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"3122","DOI":"10.3892\/etm.2017.4878","article-title":"Phascolarctobacterium faecium abundant colonization in human gastrointestinal tract","volume":"14","author":"Wu","year":"2017","journal-title":"Exp. Ther. Med."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"4672","DOI":"10.1073\/pnas.1000091107","article-title":"Substrate-driven gene expression in Roseburia inulinivorans: Importance of inducible enzymes in the utilization of inulin and starch","volume":"108","author":"Scott","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1093\/molehr\/gav003","article-title":"Amino acid metabolism in intestinal bacteria and its potential implications for mammalian reproduction","volume":"21","author":"Dai","year":"2015","journal-title":"Mol. Hum. Reprod."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1128\/CMR.00008-07","article-title":"Bacteroides: The good, the bad, and the nitty-gritty","volume":"20","author":"Wexler","year":"2007","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"3329","DOI":"10.2147\/NDT.S188340","article-title":"Possible association of Firmicutes in the gut microbiota of patients with major depressive disorder","volume":"14","author":"Huang","year":"2018","journal-title":"Neuropsychiatr. Dis. Treat."}],"container-title":["Antioxidants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3921\/11\/12\/2372\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:30:21Z","timestamp":1760146221000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3921\/11\/12\/2372"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,30]]},"references-count":92,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["antiox11122372"],"URL":"https:\/\/doi.org\/10.3390\/antiox11122372","relation":{},"ISSN":["2076-3921"],"issn-type":[{"value":"2076-3921","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,30]]}}}