{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T23:10:41Z","timestamp":1788909041381,"version":"build-2803163510"},"reference-count":96,"publisher":"American Chemical Society (ACS)","issue":"1","license":[{"start":{"date-parts":[[2020,12,3]],"date-time":"2020-12-03T00:00:00Z","timestamp":1606953600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_ccby_termsofuse.html"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["AI125529"],"award-info":[{"award-number":["AI125529"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000152","name":"Division of Molecular and Cellular Biosciences","doi-asserted-by":"publisher","award":["MCB1837877"],"award-info":[{"award-number":["MCB1837877"]}],"id":[{"id":"10.13039\/100000152","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,1,8]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Bacteria depend on a well-regulated iron homeostasis to survive adverse environments. A key component of the iron homeostasis machinery is the compartmentalization of Fe3+ in bacterioferritin and its subsequent mobilization as Fe2+ to satisfy metabolic requirements. In Pseudomonas aeruginosa Fe3+ is compartmentalized in bacterioferritin (BfrB), and its mobilization to the cytosol requires binding of a ferredoxin (Bfd) to reduce the stored Fe3+ and release the soluble Fe2+. Blocking the BfrB-Bfd complex in P.\u00a0aeruginosa by deletion of the bfd gene triggers an irreversible accumulation of Fe3+ in BfrB, concomitant cytosolic iron deficiency and significant impairment of biofilm development. Herein we report that small molecules developed to bind BfrB at the Bfd binding site block the BfrB-Bfd complex, inhibit the mobilization of iron from BfrB in P.\u00a0aeruginosa cells, elicit a bacteriostatic effect on planktonic cells, and are bactericidal to cells embedded in mature biofilms.<\/jats:p>","DOI":"10.1021\/acsinfecdis.0c00669","type":"journal-article","created":{"date-parts":[[2020,12,3]],"date-time":"2020-12-03T11:09:11Z","timestamp":1606993751000},"page":"123-140","source":"Crossref","is-referenced-by-count":38,"title":["Small Molecule Inhibitors of the Bacterioferritin\n(BfrB)\u2013Ferredoxin (Bfd) Complex Kill Biofilm-Embedded\n                    <i>Pseudomonas aeruginosa<\/i>\n                    Cells"],"prefix":"10.1021","volume":"7","author":[{"given":"Anabel","family":"Soldano","sequence":"first","affiliation":[{"name":"Louisiana State University , , 232 Choppin Hall , , ,","place":["Baton Rouge, Louisiana, United States, 70803"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huili","family":"Yao","sequence":"additional","affiliation":[{"name":"Louisiana State University , , 232 Choppin Hall , , ,","place":["Baton Rouge, Louisiana, United States, 70803"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Achala N. D.","family":"Punchi Hewage","sequence":"additional","affiliation":[{"name":"University of Kansas , , 2030 Becker Drive , , ,","place":["Lawrence, Kansas, United States, 66047"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin","family":"Meraz","sequence":"additional","affiliation":[{"name":"Oklahoma State University , , , ,","place":["Stillwater, Oklahoma, United States, 74078"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joel K.","family":"Annor-Gyamfi","sequence":"additional","affiliation":[{"name":"Oklahoma State University , , , ,","place":["Stillwater, Oklahoma, United States, 74078"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard A.","family":"Bunce","sequence":"additional","affiliation":[{"name":"Oklahoma State University , , , ,","place":["Stillwater, Oklahoma, United States, 74078"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0833-3259","authenticated-orcid":true,"given":"Kevin P.","family":"Battaile","sequence":"additional","affiliation":[{"name":"New York Structural Biology Center , , , ,","place":["Upton, New York, United States, 11973"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott","family":"Lovell","sequence":"additional","affiliation":[{"name":"University of Kansas , , 2034 Becker Drive , , ,","place":["Lawrence, Kansas, United States, 66047"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5692-5497","authenticated-orcid":true,"given":"Mario","family":"Rivera","sequence":"additional","affiliation":[{"name":"Louisiana State University , , 232 Choppin Hall , , ,","place":["Baton Rouge, Louisiana, United States, 70803"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,12,3]]},"reference":[{"key":"2026090114144864300_cit1","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1016\/S1473-3099(17)30753-3","article-title":"Discovery, research, and development\nof new antibiotics: the WHO priority list of antibiotic-resistant\nbacteria and tuberculosis","volume":"18","author":"Tacconelli","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"2026090114144864300_cit2","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1038\/nrd1008","article-title":"Understanding\nbiofilm resistance to antibacterial agents","volume":"2","author":"Davies","year":"2003","journal-title":"Nat. Rev. Drug Discovery"},{"key":"2026090114144864300_cit3","doi-asserted-by":"publisher","first-page":"6558","DOI":"10.1128\/JB.173.20.6558-6567.1991","article-title":"Optical sectioning of microbial biofilms","volume":"173","author":"Lawrence","year":"1991","journal-title":"J. Bacteriol."},{"key":"2026090114144864300_cit4","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1099\/00221287-147-1-3","article-title":"Biofilm exopolysaccharides:\na strong and sticky framework","volume":"147","author":"Sutherland","year":"2001","journal-title":"Microbiology"},{"key":"2026090114144864300_cit5","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1128\/iai.28.2.546-556.1980","article-title":"Production\nof Mucoid Microcolonies by Pseudomonas aeruginosa Within Infected Lungs in Cystic Fibrosis","volume":"28","author":"Lam","year":"1980","journal-title":"Infect. Immun."},{"key":"2026090114144864300_cit6","doi-asserted-by":"publisher","first-page":"1318","DOI":"10.1126\/science.284.5418.1318","article-title":"Bacterial Biofilms: A Common Cause\nof Persistent Infection","volume":"284","author":"Costerton","year":"1999","journal-title":"Science"},{"key":"2026090114144864300_cit7","doi-asserted-by":"publisher","first-page":"677","DOI":"10.1146\/annurev.micro.57.030502.090720","article-title":"Bacterial biofilms:\nan emerging link to disease pathogenesis","volume":"57","author":"Parsek","year":"2003","journal-title":"Annu.\nRev. 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Dis."},{"key":"2026090114144864300_cit13","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1111\/j.1524-475X.2007.00321.x","article-title":"Biofilms in chronic\nwounds","volume":"16","author":"James","year":"2008","journal-title":"Wound Repair Regen"},{"key":"2026090114144864300_cit14","doi-asserted-by":"publisher","first-page":"35","DOI":"10.3390\/biomedicines7020035","article-title":"Recent Advances\nin Non-Conventional Antimicrobial Approaches for Chronic Wound Biofilms:\nHave We Found the \u2018Chink in the Armor\u2019?","volume":"7","author":"Kadam","year":"2019","journal-title":"Biomedicines"},{"key":"2026090114144864300_cit15","doi-asserted-by":"publisher","first-page":"850","DOI":"10.1016\/j.tim.2019.05.003","article-title":"Antimicrobial Tolerance\nand Metabolic Adaptations in Microbial Biofilms","volume":"27","author":"Crabbe","year":"2019","journal-title":"Trends Microbiol."},{"key":"2026090114144864300_cit16","doi-asserted-by":"publisher","first-page":"1771","DOI":"10.1128\/JCM.37.6.1771-1776.1999","article-title":"The Calgary Biofilm Device: new technology\nfor rapid determination\nof antibiotic susceptibilities of bacterial biofilms","volume":"37","author":"Ceri","year":"1999","journal-title":"J. Clin. Microbiol."},{"key":"2026090114144864300_cit17","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1016\/S0140-6736(01)05321-1","article-title":"Antibiotic\nresistance of bacteria in biofilms","volume":"358","author":"Stewart","year":"2001","journal-title":"Lancet"},{"key":"2026090114144864300_cit18","doi-asserted-by":"publisher","first-page":"1666","DOI":"10.1128\/AAC.34.9.1666","article-title":"Enhanced\nactivity of combination of tobramycin and\npiperacillin for eradication of sessile biofilm cells of Pseudomonas aeruginosa","volume":"34","author":"Anwar","year":"1990","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090114144864300_cit19","doi-asserted-by":"publisher","first-page":"6600","DOI":"10.1002\/anie.201506818","article-title":"Targeting\nAntibiotic Resistance","volume":"55","author":"Chellat","year":"2016","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090114144864300_cit20","doi-asserted-by":"publisher","first-page":"14440","DOI":"10.1002\/anie.201804971","article-title":"Thinking\nOutside the Box-Novel Antibacterials To Tackle the Resistance Crisis","volume":"57","author":"Lakemeyer","year":"2018","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090114144864300_cit21","doi-asserted-by":"publisher","first-page":"824","DOI":"10.3389\/fchem.2019.00824","article-title":"Bacterial Biofilm Eradication Agents:\nA Current Review","volume":"7","author":"Verderosa","year":"2019","journal-title":"Front. Chem."},{"key":"2026090114144864300_cit22","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1016\/j.femsim.2004.11.010","article-title":"Iron and Infection:\nThe Heart of the Matter","volume":"43","author":"Bullen","year":"2005","journal-title":"FEMS Immunol. Med.\nMicrobiol."},{"key":"2026090114144864300_cit23","doi-asserted-by":"publisher","first-page":"646","DOI":"10.1039\/C7MT00042A","article-title":"Inhibiting the BfrB:Bfd Interaction in Pseudomonas aeruginosa Causes Irreversible Iron Accumulation in Bacterioferritin\nand Iron Deficiency in the Bacterial Cell","volume":"9","author":"Eshelman","year":"2017","journal-title":"Metallomics"},{"key":"2026090114144864300_cit24","doi-asserted-by":"publisher","first-page":"13635","DOI":"10.1073\/pnas.93.24.13635","article-title":"Superoxide Accelerates\nDNA-Damage by Elevating Free-Iron\nLevels","volume":"93","author":"Keyer","year":"1996","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026090114144864300_cit25","doi-asserted-by":"publisher","first-page":"8171","DOI":"10.1021\/jacs.9b00394","article-title":"Small Molecule Inhibitors of the\nBfrB-Bfd Interaction Decrease Pseudomonas aeruginosa Fitness and Potentiate Fluoroquinolone Activity","volume":"141","author":"Punchi Hewage","year":"2019","journal-title":"J. Am. Chem. Soc."},{"key":"2026090114144864300_cit26","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1021\/acsinfecdis.9b00398","article-title":"Inhibiting Iron Mobilization from\nBacterioferritin in Pseudomonas aeruginosa Impairs\nBiofilm Formation Irrespective of Environmental Iron Availability","volume":"6","author":"Soldano","year":"2020","journal-title":"ACS Infect. Dis."},{"key":"2026090114144864300_cit27","doi-asserted-by":"publisher","first-page":"5236","DOI":"10.1021\/bi2004119","article-title":"Two Disctinct Ferritin-Like Molecules\nin P.\u00a0aeruginosa: The Product of the bfrA Gene is a Bacterial Ferritin (FtnA) not a bacterioferritin\n(Bfr)","volume":"50","author":"Yao","year":"2011","journal-title":"Biochemistry"},{"key":"2026090114144864300_cit28","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1021\/acs.accounts.6b00514","article-title":"Bacterioferritin:\nStructure, Dynamics and Protein-Protein Interactions at Play in Iron\nStorage and Mobilization","volume":"50","author":"Rivera","year":"2017","journal-title":"Acc. Chem. Res."},{"key":"2026090114144864300_cit29","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1021\/bi9015204","article-title":"Structural\nStudies of Bacterioferritin\nB (BfrB) from Pseudomonas aeruginosa Suggest a Gating\nMechanism for Iron Uptake via the Ferroxidase Center","volume":"49","author":"Weeratunga","year":"2010","journal-title":"Biochemistry"},{"key":"2026090114144864300_cit30","doi-asserted-by":"publisher","first-page":"13470","DOI":"10.1021\/ja305180n","article-title":"The Structure of the\nBfrB-Bfd Complex Reveals Protein-Protein Interactions Enabling Iron\nRelease from Bacterioferritin","volume":"134","author":"Yao","year":"2012","journal-title":"J. Am. Chem.\nSoc."},{"key":"2026090114144864300_cit31","doi-asserted-by":"publisher","first-page":"7420","DOI":"10.1021\/bi900561a","article-title":"Binding of Pseudomonas aeruginosa Apobacterioferritin-Associated\nFerredoxin to Bacterioferritin B Promotes Heme Mediation of Electron\nDelivery and Mobilization of Core Mineral Iron","volume":"48","author":"Weeratunga","year":"2009","journal-title":"Biochemistry"},{"key":"2026090114144864300_cit32","doi-asserted-by":"publisher","first-page":"5533","DOI":"10.1021\/acs.biochem.8b00823","article-title":"Bfd, a New\nClass of [2Fe-2S] Protein That Functions in Bacterial Iron Homeostasis,\nRequires a Structural Anion Binding Site","volume":"57","author":"Wijerathne","year":"2018","journal-title":"Biochemistry"},{"key":"2026090114144864300_cit33","doi-asserted-by":"publisher","first-page":"6162","DOI":"10.1021\/acs.biochem.5b00937","article-title":"Characterization\nof the Bacterioferritin\/Bacterioferritin\nAssociated Ferredoxin Potein-Protein Interactions in Solution and\nDetermination of Binding Energy Hot Spots","volume":"54","author":"Wang","year":"2015","journal-title":"Biochemistry"},{"key":"2026090114144864300_cit34","doi-asserted-by":"publisher","first-page":"11076","DOI":"10.1073\/pnas.0504266102","article-title":"Iron and Pseuodomonas aeruginosa biofilm formation","volume":"102","author":"Banin","year":"2005","journal-title":"Proc. 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Microbiol."},{"key":"2026090114144864300_cit36","doi-asserted-by":"publisher","first-page":"552","DOI":"10.1038\/417552a","article-title":"A Component of Innate\nImmunity Prevents Bacterial Biofilm Development","volume":"417","author":"Singh","year":"2002","journal-title":"Nature"},{"key":"2026090114144864300_cit37","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1039\/C9MD00032A","article-title":"Connecting\niron acquisition and biofilm\nformation in the ESKAPE pathogens as a strategy for combatting antibiotic\nresistance","volume":"10","author":"Post","year":"2019","journal-title":"MedChemComm"},{"key":"2026090114144864300_cit38","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1080\/00304948.2018.1462072","article-title":"4,7-Diaminoisoindoline-1,3-dione","volume":"50","author":"Gnanasekaran","year":"2018","journal-title":"Org. Prep. Proced. Int."},{"key":"2026090114144864300_cit39","doi-asserted-by":"publisher","first-page":"1661","DOI":"10.1111\/1462-2920.12013","article-title":"Pyoverdine biosynthesis and secretion\nin Pseudomonas aeruginosa: implications for metal homeostasis","volume":"15","author":"Schalk","year":"2013","journal-title":"Environ. Microbiol."},{"key":"2026090114144864300_cit40","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1111\/j.1574-695X.2010.00690.x","article-title":"An update\non Pseudomonas aeruginosa biofilm formation, tolerance,\nand dispersal","volume":"59","author":"Harmsen","year":"2010","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"2026090114144864300_cit41","doi-asserted-by":"publisher","first-page":"320","DOI":"10.1038\/nrmicro.2016.34","article-title":"Distinguishing between\nresistance, tolerance and persistence to antibiotic treatment","volume":"14","author":"Brauner","year":"2016","journal-title":"Nat. Rev. Microbiol."},{"key":"2026090114144864300_cit42","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1128\/AAC.36.6.1208","article-title":"Dynamic\ninteractions of biofilms of mucoid Pseudomonas aeruginosa with tobramycin and piperacillin","volume":"36","author":"Anwar","year":"1992","journal-title":"Antimicrob.\nAgents Chemother."},{"key":"2026090114144864300_cit43","doi-asserted-by":"publisher","first-page":"1251","DOI":"10.1128\/AAC.47.4.1251-1256.2003","article-title":"Role of nutrient\nlimitation and stationary-phase existence in Klebsiella pneumoniae\nbiofilm resistance to ampicillin and ciprofloxacin","volume":"47","author":"Anderl","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090114144864300_cit44","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1128\/AAC.47.1.317-323.2003","article-title":"Contributions of\nantibiotic penetration,\noxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin","volume":"47","author":"Walters","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090114144864300_cit45","doi-asserted-by":"publisher","first-page":"4035","DOI":"10.1128\/AEM.64.10.4035-4039.1998","article-title":"Spatial\nphysiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability","volume":"64","author":"Xu","year":"1998","journal-title":"Appl. Environ. Microbiol."},{"key":"2026090114144864300_cit46","doi-asserted-by":"publisher","first-page":"6188","DOI":"10.1128\/AEM.70.10.6188-6196.2004","article-title":"Stratified growth in Pseudomonas aeruginosa biofilms","volume":"70","author":"Werner","year":"2004","journal-title":"Appl. Environ.\nMicrobiol."},{"key":"2026090114144864300_cit47","doi-asserted-by":"publisher","first-page":"3803","DOI":"10.1093\/emboj\/cdg366","article-title":"Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors","volume":"22","author":"Hentzer","year":"2003","journal-title":"EMBO J."},{"key":"2026090114144864300_cit48","doi-asserted-by":"publisher","first-page":"2064","DOI":"10.1128\/AEM.72.3.2064-2069.2006","article-title":"Chelator-induced dispersal and killing\nof Pseudomonas aeruginosa cells in a biofilm","volume":"72","author":"Banin","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"2026090114144864300_cit49","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1111\/j.1365-2958.2008.06152.x","article-title":"Tolerance\nto the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on\nthe pmr and mexAB-oprM genes","volume":"68","author":"Pamp","year":"2008","journal-title":"Mol. Microbiol."},{"key":"2026090114144864300_cit50","doi-asserted-by":"publisher","first-page":"1352","DOI":"10.1128\/AAC.41.6.1352","article-title":"Comparison\nof recalcitrance to ciprofloxacin\nand levofloxacin exhibited by Pseudomonas aeruginosa bofilms displaying rapid-transport characteristics","volume":"41","author":"Vrany","year":"1997","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090114144864300_cit51","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1097\/QCO.0b013e328332e672","article-title":"Colistin in the 21st\ncentury","volume":"22","author":"Nation","year":"2009","journal-title":"Curr. Opin. Infect.\nDis."},{"key":"2026090114144864300_cit52","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1016\/S1473-3099(06)70580-1","article-title":"Colistin: the re-emerging antibiotic\nfor multidrug-resistant Gram-negative bacterial infections","volume":"6","author":"Li","year":"2006","journal-title":"Lancet Infect. Dis."},{"key":"2026090114144864300_cit53","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1128\/JCM.01390-18","article-title":"Antimicrobial Susceptibility\nTesting\nfor Polymyxins: Challenges, Issues, and Recommendations","volume":"57","author":"Ezadi","year":"2019","journal-title":"J. Clin. Microbiol."},{"key":"2026090114144864300_cit54","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1016\/j.ijantimicag.2009.12.011","article-title":"Antibiotic\nresistance of bacterial biofilms","volume":"35","author":"Hoiby","year":"2010","journal-title":"Int. J. Antimicrob.\nAgents"},{"issue":"10","key":"2026090114144864300_cit55","doi-asserted-by":"publisher","first-page":"2395","DOI":"10.1099\/00221287-146-10-2395","article-title":"Quantification of biofilm\nstructures by the novel computer program COMSTAT","volume":"146","author":"Heydorn","year":"2000","journal-title":"Microbiology"},{"key":"2026090114144864300_cit56","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1126\/scitranslmed.aat7520","article-title":"Gallium disrupts bacterial iron metabolism\nand has\ntherapeutic effects in mice and humans with lung infections","volume":"10","author":"Goss","year":"2018","journal-title":"Sci. Transl. Med."},{"key":"2026090114144864300_cit57","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1111\/j.1574-6941.2011.01087.x","article-title":"Trade-off between oxygen\nand iron acquisition in bacterial cells at the air-liquid interface","volume":"77","author":"Yamamoto","year":"2011","journal-title":"FEMS Microbiol. Ecol."},{"key":"2026090114144864300_cit58","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1046\/j.1365-2958.2003.03877.x","article-title":"Genes involved in matrix\nformation in Pseudomonas aeruginosa PA14 biofilms","volume":"51","author":"Friedman","year":"2004","journal-title":"Mol. 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