{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T04:14:24Z","timestamp":1788408864148,"version":"build-2803163510"},"reference-count":47,"publisher":"American Chemical Society (ACS)","issue":"2","license":[{"start":{"date-parts":[[2020,1,21]],"date-time":"2020-01-21T00:00:00Z","timestamp":1579564800000},"content-version":"vor","delay-in-days":39,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_termsofuse.html"}],"funder":[{"DOI":"10.13039\/100011102","name":"Seventh Framework Programme","doi-asserted-by":"publisher","award":["305340"],"award-info":[{"award-number":["305340"]}],"id":[{"id":"10.13039\/100011102","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004359","name":"Vetenskapsr\u00e5det","doi-asserted-by":"publisher","award":["NA"],"award-info":[{"award-number":["NA"]}],"id":[{"id":"10.13039\/501100004359","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,2,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Necrotizing soft-tissue infections (NSTIs) have multiple causes, risk factors, anatomical locations, and pathogenic mechanisms. In patients with NSTI, circulating metabolites may serve as a substrate having impact on bacterial adaptation at the site of infection. Metabolic signatures associated with NSTI may reveal the potential to be useful as diagnostic and prognostic markers and novel targets for therapy. This study used untargeted metabolomics analyses of plasma from NSTI patients (n = 34) and healthy (noninfected) controls (n = 24) to identify the metabolic signatures and connectivity patterns among metabolites associated with NSTI. Metabolite\u2013metabolite association networks were employed to compare the metabolic profiles of NSTI patients and noninfected surgical controls. Out of 97 metabolites detected, the abundance of 33 was significantly altered in NSTI patients. Analysis of metabolite\u2013metabolite association networks showed a more densely connected network: specifically, 20 metabolites differentially connected between NSTI and controls. A selected set of significantly altered metabolites was tested in vitro to investigate potential influence on NSTI group A streptococcal strain growth and biofilm formation. Using chemically defined media supplemented with the selected metabolites, ornithine, ribose, urea, and glucuronic acid, revealed metabolite-specific effects on both bacterial growth and biofilm formation. This study identifies for the first time an NSTI-specific metabolic signature with implications for optimized diagnostics and therapies.<\/jats:p>","DOI":"10.1021\/acs.jproteome.9b00565","type":"journal-article","created":{"date-parts":[[2019,12,13]],"date-time":"2019-12-13T05:26:22Z","timestamp":1576214782000},"page":"688-698","source":"Crossref","is-referenced-by-count":21,"title":["Integrated Univariate,\nMultivariate, and Correlation-Based\nNetwork Analyses Reveal Metabolite-Specific Effects on Bacterial Growth\nand Biofilm Formation in Necrotizing Soft Tissue Infections"],"prefix":"10.1021","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5552-7200","authenticated-orcid":true,"given":"Muhammad","family":"Afzal","sequence":"first","affiliation":[{"name":"Karolinska University Hospital , , Alfred Nobels Alle\u0301 8 , ,","place":["Huddinge, Sweden, 141 52"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8284-4829","authenticated-orcid":true,"given":"Edoardo","family":"Saccenti","sequence":"additional","affiliation":[{"name":"Wageningen University & Research , , Stippeneng 4 , ,","place":["Wageningen, The Netherlands, 6708 WE"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5832-2262","authenticated-orcid":true,"given":"Martin Bruun","family":"Madsen","sequence":"additional","affiliation":[{"name":"Copenhagen University Hospital, Rigshospitalet , , ,","place":["Copenhagen, Denmark, 2100"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5695-6728","authenticated-orcid":true,"given":"Marco Bo","family":"Hansen","sequence":"additional","affiliation":[{"name":"Rigshospitalet, University of Copenhagen , , Blegdamsvej 9 , ,","place":["Copenhagen, Denmark, DK-2100"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1147-379X","authenticated-orcid":true,"given":"Ole","family":"Hyldegaard","sequence":"additional","affiliation":[{"name":"Copenhagen University Hospital, Rigshospitalet , , ,","place":["Copenhagen, Denmark, 2100"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1615-4453","authenticated-orcid":true,"given":"Steinar","family":"Skrede","sequence":"additional","affiliation":[{"name":"Haukeland University Hospital , , ,","place":["Bergen, Norway, N-5021"]},{"name":"University of Bergen , , ,","place":["Bergen, Norway, N-5020"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2352-9017","authenticated-orcid":true,"given":"Vitor A. P.","family":"Martins dos Santos","sequence":"additional","affiliation":[{"name":"Wageningen University & Research , , Stippeneng 4 , ,","place":["Wageningen, The Netherlands, 6708 WE"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9372-1795","authenticated-orcid":true,"given":"Anna","family":"Norrby-Teglund","sequence":"additional","affiliation":[{"name":"Karolinska University Hospital , , Alfred Nobels Alle\u0301 8 , ,","place":["Huddinge, Sweden, 141 52"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1695-7934","authenticated-orcid":true,"given":"Mattias","family":"Svensson","sequence":"additional","affiliation":[{"name":"Karolinska University Hospital , , Alfred Nobels Alle\u0301 8 , ,","place":["Huddinge, Sweden, 141 52"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2019,12,13]]},"reference":[{"key":"2026090223352201000_cit1","doi-asserted-by":"publisher","first-page":"2253","DOI":"10.1056\/NEJMra1600673","article-title":"Necrotizing Soft-Tissue\nInfections","volume":"377","author":"Stevens","year":"2017","journal-title":"N. Engl. J. Med."},{"key":"2026090223352201000_cit2","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1001\/archsurg.140.2.151","article-title":"Predictors of Mortality and Limb Loss in Necrotizing\nSoft Tissue Infections","volume":"140","author":"Anaya","year":"2005","journal-title":"Arch. Surg."},{"key":"2026090223352201000_cit3","doi-asserted-by":"publisher","first-page":"1241","DOI":"10.1007\/s00134-019-05730-x","article-title":"Patient\u2019s\nCharacteristics and Outcomes\nin Necrotising Soft-Tissue Infections: Results from a Scandinavian,\nMulticentre, Prospective Cohort Study","volume":"45","author":"Madsen","year":"2019","journal-title":"Intensive\nCare Med."},{"key":"2026090223352201000_cit4","doi-asserted-by":"publisher","first-page":"E545","DOI":"10.1111\/1469-0691.12276","article-title":"Necrotizing\nSoft Tissue Infections Caused by Streptococcus Pyogenes and Streptococcus\nDysgalactiae Subsp. Equisimilis of Groups C and G in Western Norway","volume":"19","author":"Bruun","year":"2013","journal-title":"Clin. Microbiol. Infect."},{"key":"2026090223352201000_cit5","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/S0002-9343(97)00160-5","article-title":"Population-Based Surveillance for Group A Streptococcal\nNecrotizing Fasciitis: Clinical Features, Prognostic Indicators, and\nMicrobiologic Analysis of Seventy-Seven Cases","volume":"103","author":"Kaul","year":"1997","journal-title":"Am. J. Med."},{"key":"2026090223352201000_cit6","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1086\/653116","article-title":"Getting under\nthe Skin: The Immunopathogenesis of Streptococcus Pyogenes Deep Tissue\nInfections","volume":"51","author":"Johansson","year":"2010","journal-title":"Clin. Infect. 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Proteome\nRes."},{"key":"2026090223352201000_cit10","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1021\/pr501075r","article-title":"Probabilistic\nNetworks of Blood Metabolites in Healthy Subjects As Indicators of\nLatent Cardiovascular Risk","volume":"14","author":"Saccenti","year":"2015","journal-title":"J. Proteome Res."},{"key":"2026090223352201000_cit11","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1021\/acs.jproteome.7b00404","article-title":"Age and Sex Effects\non Plasma Metabolite Association Networks in Healthy Subjects","volume":"17","author":"Vignoli","year":"2018","journal-title":"J. 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Immun."},{"key":"2026090223352201000_cit25","article-title":"Static Biofilm\nCultures of Gram-Positive Pathogens Grown in a Microtiter Format Used\nfor Anti-Biofilm Drug Discovery","volume-title":"Current\nProtocols in Pharmacology","author":"Kwasny","year":"2010"},{"key":"2026090223352201000_cit26","doi-asserted-by":"publisher","first-page":"708","DOI":"10.1038\/nrc3124","article-title":"Aminoacyl-TRNA Synthetases and Tumorigenesis: More\nthan Housekeeping","volume":"11","author":"Kim","year":"2011","journal-title":"Nat. Rev. Cancer"},{"key":"2026090223352201000_cit27","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/0006-291X(66)90415-3","article-title":"Enzymatic\nSynthesis of Diadenosine Tetraphosphate and Diadenosine Triphosphate\nwith a Purified Lysyl-SRNA Synthetase","volume":"24","author":"Zamecnik","year":"1966","journal-title":"Biochem.\nBiophys. Res. Commun."},{"key":"2026090223352201000_cit28","doi-asserted-by":"publisher","first-page":"6102","DOI":"10.1046\/j.1432-1327.2000.01701.x","article-title":"Physiological Functions\nof Thioredoxin and Thioredoxin\nReductase","volume":"267","author":"Arne\u0301r","year":"2000","journal-title":"Eur. J. Biochem."},{"key":"2026090223352201000_cit29","doi-asserted-by":"publisher","first-page":"39968","DOI":"10.1074\/jbc.M402260200","article-title":"Cytosolic\nNADP+-Dependent Isocitrate Dehydrogenase\nPlays a Key Role in Lipid Metabolism","volume":"279","author":"Koh","year":"2004","journal-title":"J. Biol.\nChem."},{"key":"2026090223352201000_cit30","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1056\/NEJM199608223350803","article-title":"Invasive\nGroup A Streptococcal Infections\nin Ontario, Canada","volume":"335","author":"Davies","year":"1996","journal-title":"N. Engl. J. Med."},{"key":"2026090223352201000_cit31","doi-asserted-by":"publisher","first-page":"1155","DOI":"10.1128\/JCM.02155-08","article-title":"Clinical and Microbiological\nCharacteristics of Severe Streptococcus Pyogenes Disease in Europe","volume":"47","author":"Luca-Harari","year":"2009","journal-title":"J. Clin. Microbiol."},{"key":"2026090223352201000_cit32","doi-asserted-by":"publisher","first-page":"3646","DOI":"10.1128\/JB.00088-08","article-title":"Regulation of Gene Expression in a Mixed-Genus Community:\nStabilized Arginine Biosynthesis in Streptococcus Gordonii by Coaggregation\nwith Actinomyces Naeslundii","volume":"190","author":"Jakubovics","year":"2008","journal-title":"J. Bacteriol."},{"key":"2026090223352201000_cit33","doi-asserted-by":"publisher","first-page":"6016","DOI":"10.1128\/jb.185.20.6016-6024.2003","article-title":"Rgg Coordinates\nVirulence Factor Synthesis and Metabolism in Streptococcus Pyogenes","volume":"185","author":"Chaussee","year":"2003","journal-title":"J. Bacteriol."},{"key":"2026090223352201000_cit34","doi-asserted-by":"publisher","first-page":"1829","DOI":"10.1099\/13500872-140-8-1829","article-title":"Analysis of a Ribose Transport Operon from Bacillus\nSubtilis","volume":"140","author":"Woodson","year":"1994","journal-title":"Microbiol."},{"key":"2026090223352201000_cit35","doi-asserted-by":"publisher","first-page":"6327","DOI":"10.1016\/j.bmc.2006.05.057","article-title":"Ribokinase\nfrom E. Coli: Expression, Purification, and Substrate Specificity","volume":"14","author":"Chuvikovsky","year":"2006","journal-title":"Bioorg. Med. 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Biotechnol."},{"key":"2026090223352201000_cit38","doi-asserted-by":"publisher","first-page":"D111","DOI":"10.1093\/nar\/gkp894","article-title":"RegPrecise:\nA Database of Curated\nGenomic Inferences of Transcriptional Regulatory Interactions in Prokaryotes","volume":"38","author":"Novichkov","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"2026090223352201000_cit39","doi-asserted-by":"publisher","first-page":"e99995","DOI":"10.1371\/journal.pone.0099995","article-title":"Anti-Biofilm\nActivity: A Function of Klebsiella Pneumoniae Capsular Polysaccharide","volume":"9","author":"Dos Santos Goncalves","year":"2014","journal-title":"PLoS One"},{"key":"2026090223352201000_cit40","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1186\/s12866-015-0529-y","article-title":"Autoinducer-2 Regulates\nPseudomonas Aeruginosa PAO1 Biofilm Formation\nand Virulence Production in a Dose-Dependent Manner","volume":"15","author":"Li","year":"2015","journal-title":"BMC Microbiol."},{"key":"2026090223352201000_cit41","doi-asserted-by":"publisher","first-page":"88","DOI":"10.3389\/fmicb.2016.00088","article-title":"Autoinducer-2\nof Streptococcus Mitis as a Target Molecule to Inhibit Pathogenic\nMulti-Species Biofilm Formation In Vitro and in an Endotracheal Intubation\nRat Model","volume":"7","author":"Wang","year":"2016","journal-title":"Front. Microbiol."},{"key":"2026090223352201000_cit42","doi-asserted-by":"publisher","first-page":"1581","DOI":"10.1517\/13543770903222293","article-title":"Quorum Sensing Inhibitors:\nA Patent Overview","volume":"19","author":"Pan","year":"2009","journal-title":"Expert Opin. Ther. Pat."},{"key":"2026090223352201000_cit43","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1186\/1471-2180-8-188","article-title":"Functional\nAnalysis of the Group A Streptococcal LuxS\/AI-2\nSystem in Metabolism, Adaptation to Stress and Interaction with Host\nCells","volume":"8","author":"Siller","year":"2008","journal-title":"BMC Microbiol."},{"key":"2026090223352201000_cit44","doi-asserted-by":"publisher","first-page":"4021","DOI":"10.1128\/IAI.01741-05","article-title":"The Actinobacillus\nActinomycetemcomitans Ribose Binding Protein RbsB Interacts with Cognate\nand Heterologous Autoinducer 2 Signals","volume":"74","author":"James","year":"2006","journal-title":"Infect.\nImmun."},{"key":"2026090223352201000_cit45","doi-asserted-by":"publisher","first-page":"836","DOI":"10.1111\/j.1365-2958.2011.07831.x","article-title":"RbsB (NTHI_0632)\nMediates Quorum\nSignal Uptake in Nontypeable Haemophilus Influenzae Strain 86-028NP","volume":"82","author":"Armbruster","year":"2011","journal-title":"Mol. Microbiol."},{"key":"2026090223352201000_cit46","doi-asserted-by":"publisher","first-page":"304","DOI":"10.1016\/j.archoralbio.2014.11.004","article-title":"Synergistic Inhibition\nof Streptococcal Biofilm by\nRibose and Xylitol","volume":"60","author":"Lee","year":"2015","journal-title":"Arch. Oral Biol."},{"key":"2026090223352201000_cit47","doi-asserted-by":"publisher","first-page":"17183","DOI":"10.1038\/s41598-017-17383-1","article-title":"CiaR Impacts Biofilm Formation by\nRegulating an Arginine Biosynthesis Pathway in Streptococcus Sanguinis\nSK36","volume":"7","author":"Zhu","year":"2017","journal-title":"Sci. Rep."}],"container-title":["Journal of Proteome Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.jproteome.9b00565","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jprobs\/article-pdf\/19\/2\/688\/67116149\/acs.jproteome.9b00565.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jprobs\/article-pdf\/19\/2\/688\/67116149\/acs.jproteome.9b00565.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T03:37:52Z","timestamp":1788406672000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jprobs\/article\/19\/2\/688\/1642685\/Integrated-Univariate-Multivariate-and-Correlation"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,13]]},"references-count":47,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2019,12,13]]},"published-print":{"date-parts":[[2020,2,7]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.jproteome.9b00565","relation":{},"ISSN":["1535-3893","1535-3907"],"issn-type":[{"value":"1535-3893","type":"print"},{"value":"1535-3907","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,13]]}}}