{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,1]],"date-time":"2025-07-01T04:11:54Z","timestamp":1751343114569,"version":"3.41.0"},"reference-count":35,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2025,6,30]],"date-time":"2025-06-30T00:00:00Z","timestamp":1751241600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100007161","name":"Secretar\u00eda de Investigaci\u00f3n y Posgrado, Instituto Polit\u00e9cnico Nacional","doi-asserted-by":"publisher","award":["2021-0392"],"award-info":[{"award-number":["2021-0392"]}],"id":[{"id":"10.13039\/501100007161","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007161","name":"Secretar\u00eda de Investigaci\u00f3n y Posgrado, Instituto Polit\u00e9cnico Nacional","doi-asserted-by":"publisher","award":["2022-0660"],"award-info":[{"award-number":["2022-0660"]}],"id":[{"id":"10.13039\/501100007161","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007161","name":"Secretar\u00eda de Investigaci\u00f3n y Posgrado, Instituto Polit\u00e9cnico Nacional","doi-asserted-by":"publisher","award":["2023-0831"],"award-info":[{"award-number":["2023-0831"]}],"id":[{"id":"10.13039\/501100007161","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007161","name":"Secretar\u00eda de Investigaci\u00f3n y Posgrado, Instituto Polit\u00e9cnico Nacional","doi-asserted-by":"publisher","award":["2024-0117"],"award-info":[{"award-number":["2024-0117"]}],"id":[{"id":"10.13039\/501100007161","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS One"],"abstract":"<jats:p>The genus <jats:italic>Burkholderia<\/jats:italic> is currently recognized for producing several antimicrobial compounds with potential applications in developing novel treatments for infectious diseases, including those caused by multidrug-resistant (MDR) bacteria. This study aimed to investigate the ability of <jats:italic>Burkholderia orbicola<\/jats:italic> TAtl-371<jats:sup>T<\/jats:sup> and CACua-24 to inhibit the growth of MDR human pathogens and to analyze the chemical composition of active extracts from cultures of these strains to identify putative compounds associated with their activity. The double-layer agar technique was used to evaluate the antimicrobial activity of <jats:italic>B. orbicola<\/jats:italic> strains. Sequential solvent extraction with hexane, dichloromethane, ethyl acetate, and methanol was conducted on <jats:italic>B. orbicola<\/jats:italic> cultures, and the active extract was analyzed by bioautography and fractionated using preparative thin-layer chromatography. Putative antimicrobials in the active fraction were identified through <jats:sup>1<\/jats:sup>H, <jats:sup>13<\/jats:sup>C NMR, and mass spectrometry. <jats:italic>B. orbicola<\/jats:italic> strains inhibited several MDR strains of <jats:italic>Acinetobacter baumannii<\/jats:italic>, <jats:italic>Klebsiella pneumoniae<\/jats:italic>, <jats:italic>Pseudomonas aeruginosa<\/jats:italic>, <jats:italic>Escherichia coli<\/jats:italic>, and <jats:italic>Staphylococcus aureus<\/jats:italic> on double-layer agar probes, displaying inhibition halos ranging from 5 to 41\u2009mm. The hexane extract showed the best inhibitory activity against MDR strains, except for <jats:italic>P. aeruginosa<\/jats:italic> strains. Analysis through thin-layer chromatography and bioautography revealed a tailing spot with antimicrobial activity. The spectroscopic analysis of this tailing spot revealed the presence of the siderophore fragin. This fragin-containing fraction inhibited the MDR <jats:italic>A. baumannii<\/jats:italic> (1024 \u00b5g\/mL), <jats:italic>K. pneumoniae<\/jats:italic> 903137 (128 \u00b5g\/mL), <jats:italic>E. coli<\/jats:italic> (256 \u00b5g\/mL), and <jats:italic>S. aureus<\/jats:italic> (128 \u00b5g\/mL), but no effect was observed against <jats:italic>P. aeruginosa<\/jats:italic>. This fraction also inhibited yeasts of the species <jats:italic>Candida albicans<\/jats:italic> and <jats:italic>Nakaseomyces glabratus<\/jats:italic>, suggesting an antimicrobial spectrum that extends beyond MDR bacteria. The genomic sequence analysis of strains TAtl-371<jats:sup>T<\/jats:sup> and CACua-24 revealed a cluster of 7 genes, resulting in the same organization and over 99% similarity to the fragin genes reported for <jats:italic>Burkholderia cenocepacia<\/jats:italic> H111. This study highlights the potential of <jats:italic>B. orbicola<\/jats:italic> to produce fragin and its potential activity against MDR bacteria that affect human health worldwide.<\/jats:p>","DOI":"10.1371\/journal.pone.0326906","type":"journal-article","created":{"date-parts":[[2025,6,30]],"date-time":"2025-06-30T17:41:17Z","timestamp":1751305277000},"page":"e0326906","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":0,"title":["Dissecting the inhibitory activity of Burkholderia orbicola against Gram-positive and - negative multidrug-resistant 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electrophoresis and thin layer chromatography","volume":"90","author":"AK Utal","year":"1999","journal-title":"J Neurosci Methods"},{"issue":"6","key":"pone.0326906.ref031","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1002\/bmc.1130080615","article-title":"TLC studies on certain aminoglycoside antibiotics","volume":"8","author":"R Bhushan","year":"1994","journal-title":"Biomed Chromatogr"},{"issue":"1","key":"pone.0326906.ref032","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/0005-2795(76)90288-9","article-title":"Structural studies on a glycoprotein isolated from alveoli of patients with alveolar proteinosis","volume":"427","author":"SN Bhattacharyya","year":"1976","journal-title":"Biochim Biophys Acta"},{"issue":"2","key":"pone.0326906.ref033","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/j.aca.2004.11.044","article-title":"Improved detection limit for ammonium\/ammonia achieved by Berthelot\u2019s reaction by use of solid-phase 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