{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T20:19:48Z","timestamp":1788466788889,"version":"build-2803163510"},"reference-count":69,"publisher":"American Chemical Society (ACS)","issue":"18","license":[{"start":{"date-parts":[[2019,10,15]],"date-time":"2019-10-15T00:00:00Z","timestamp":1571097600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_termsofuse.html"}],"funder":[{"DOI":"10.13039\/501100001412","name":"Council of Scientific and Industrial Research","doi-asserted-by":"publisher","award":["09\/143(0857)\/2014-EMR-I"],"award-info":[{"award-number":["09\/143(0857)\/2014-EMR-I"]}],"id":[{"id":"10.13039\/501100001412","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,10,29]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The recalcitrant biofilm formed by fungus Cryptococcus neoformans is a life-threatening pathogenic condition responsible for further intensifying cryptococcosis. Considering the enhanced biofilm resistance and toxicity of synthetic antifungal drugs, the search for efficient, nontoxic, and cost-effective natural therapeutics has received a major boost. Phenolic (thymol and carvacrol) and aldehydic (citral) terpenes are natural and safe alternatives capable of efficient microbial biofilm inhibition. However, the biofilm inhibition mechanism of these terpenes still remains unclear. In this study, we adopted an integrative biophysical and biochemical approach to elucidate the hierarchy of their action against C. neoformans biofilm cells. The microscopic analysis revealed disruption of the biofilm cell surface with elevation in surface roughness and reduction in cell height. Although all terpenes acted through ergosterol biosynthesis inhibition, the phenolic terpenes also selectively interacted via ergosterol binding. Further, the alterations in the fatty acid profile in response to terpenes attenuated the cell membrane fluidity with enhanced permeability, resulting in pore formation and efflux of the K+\/intracellular content. Additionally, mitochondrial depolarization caused higher levels of reactive oxygen species, which led to increased lipid peroxidation and activation of the antioxidant defense system. Indeed, the oxidative stress caused a significant decline in the amount of extracellular polymeric matrix and capsule sugars (mannose, xylose, and glucuronic acid), leading to a reduced capsule size and an overall negative charge on the cell surface. This comprehensive data revealed the mechanistic insights into the mode of action of terpenes on biofilm inhibition, which could be exploited for formulating novel anti-biofilm agents.<\/jats:p>","DOI":"10.1021\/acsomega.9b01482","type":"journal-article","created":{"date-parts":[[2019,10,15]],"date-time":"2019-10-15T08:49:10Z","timestamp":1571129350000},"page":"17634-17648","source":"Crossref","is-referenced-by-count":48,"title":["Delineating the Biofilm Inhibition Mechanisms of Phenolic and Aldehydic\nTerpenes against\n                    <i>Cryptococcus neoformans<\/i>"],"prefix":"10.1021","volume":"4","author":[{"given":"Poonam","family":"Kumari","sequence":"first","affiliation":[{"name":"Indian Institute of Technology Roorkee , , , ,","place":["Roorkee, Uttarakhand, India, 247677"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neha","family":"Arora","sequence":"additional","affiliation":[{"name":"Indian Institute of Technology Roorkee , , , ,","place":["Roorkee, Uttarakhand, India, 247677"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Apurva","family":"Chatrath","sequence":"additional","affiliation":[{"name":"Indian Institute of Technology Roorkee , , , ,","place":["Roorkee, Uttarakhand, India, 247677"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rashmi","family":"Gangwar","sequence":"additional","affiliation":[{"name":"Indian Institute of Technology Roorkee , , , ,","place":["Roorkee, Uttarakhand, India, 247677"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vikas","family":"Pruthi","sequence":"additional","affiliation":[{"name":"Indian Institute of Technology Roorkee , , , ,","place":["Roorkee, Uttarakhand, India, 247677"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3801-7134","authenticated-orcid":true,"given":"Krishna Mohan","family":"Poluri","sequence":"additional","affiliation":[{"name":"Indian Institute of Technology Roorkee , , , ,","place":["Roorkee, Uttarakhand, India, 247677"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7341-2346","authenticated-orcid":true,"given":"Ramasare","family":"Prasad","sequence":"additional","affiliation":[{"name":"Indian Institute of Technology Roorkee , , , ,","place":["Roorkee, Uttarakhand, India, 247677"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2019,10,15]]},"reference":[{"key":"2026090315571490400_cit1","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1016\/s1473-3099(17)30243-8","article-title":"Global burden of disease of HIV-associated\ncryptococcal meningitis: an updated analysis","volume":"17","author":"Rajasingham","year":"2017","journal-title":"Lancet Infect. 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Case Rep."},{"key":"2026090315571490400_cit5","doi-asserted-by":"publisher","first-page":"290","DOI":"10.3389\/fmicb.2016.00290","article-title":"Virulence of Cryptococcus sp. Biofilms\nIn Vitro and In Vivo using Galleria mellonella as an Alternative Model","volume":"7","author":"Benaducci","year":"2016","journal-title":"Front. Microbiol."},{"key":"2026090315571490400_cit6","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1038\/nrmicro2415","article-title":"The Biofilm\nMatrix","volume":"8","author":"Flemming","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"2026090315571490400_cit7","doi-asserted-by":"publisher","first-page":"6350","DOI":"10.1128\/iai.73.10.6350-6362.2005","article-title":"Specific antibody can prevent fungal biofilm formation\nand this effect correlates with protective efficacy","volume":"73","author":"Martinez","year":"2005","journal-title":"Infect. 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Agric.\nFood Chem."},{"key":"2026090315571490400_cit24","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/s1471-4914(02)02280-3","article-title":"Molecular basis of resistance to\nazole antifungals","volume":"8","author":"Lupetti","year":"2002","journal-title":"Trends Mol. Med."},{"key":"2026090315571490400_cit25","doi-asserted-by":"publisher","first-page":"913","DOI":"10.1007\/s10495-007-0756-2","article-title":"Mitochondria,\noxidative stress and cell death","volume":"12","author":"Ott","year":"2007","journal-title":"Apoptosis"},{"key":"2026090315571490400_cit26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2012\/528521","article-title":"Fungal biofilm resistance","volume":"2012","author":"Ramage","year":"2012","journal-title":"Internet J. 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Microbiol."},{"key":"2026090315571490400_cit29","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005828","article-title":"Fungal super glue: The biofilm matrix and its composition,\nassembly, and functions","volume":"12","author":"Mitchell","year":"2016","journal-title":"PLoS Pathog."},{"key":"2026090315571490400_cit30","doi-asserted-by":"publisher","first-page":"1435","DOI":"10.3390\/molecules22091435","article-title":"Cytotoxic\nactivity of Origanum vulgare L. on hepatocellular carcinoma cell line\nHepG2 and evaluation of its biological activity","volume":"22","author":"Elshafie","year":"2017","journal-title":"Molecules"},{"key":"2026090315571490400_cit31","doi-asserted-by":"publisher","first-page":"3234","DOI":"10.1021\/acs.langmuir.6b00600","article-title":"Mechanism of Action of Thymol on\nCell Membranes Investigated through Lipid Langmuir Monolayers at the\nAir-Water Interface and Molecular Simulation","volume":"32","author":"Ferreira","year":"2016","journal-title":"Langmuir"},{"key":"2026090315571490400_cit32","doi-asserted-by":"publisher","first-page":"1","DOI":"10.9734\/ijtdh\/2016\/21423","article-title":"Antifungal activity of citral by disruption of ergosterol biosynthesis\nin fluconazole resistant Candida tropicalis","volume":"11","author":"Sousa","year":"2016","journal-title":"Int. J. Trop. Dis."},{"key":"2026090315571490400_cit33","doi-asserted-by":"publisher","first-page":"5806","DOI":"10.1039\/c7ra12191a","article-title":"Antifungal mechanism of cinnamaldehyde\nand citral combination against Penicillium expansum based on FT-IR\nfingerprint, plasma membrane, oxidative stress and volatile profile","volume":"8","author":"Wang","year":"2018","journal-title":"RSC Adv."},{"key":"2026090315571490400_cit34","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1007\/s10096-010-1050-8","article-title":"Fungicidal\nactivity of thymol and carvacrol by disrupting ergosterol biosynthesis\nand membrane integrity against Candida","volume":"30","author":"Ahmad","year":"2011","journal-title":"Eur.\nJ. Clin. Microbiol. Infect. Dis."},{"key":"2026090315571490400_cit35","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1016\/j.foodchem.2015.02.136","article-title":"Effects of\nsub-lethal concentrations of thyme and oregano essential oils, carvacrol,\nthymol, citral and trans-2-hexenal on membrane fatty acid composition\nand volatile molecule profile of Listeria monocytogenes, Escherichia\ncoli and Salmonella enteritidis","volume":"182","author":"Siroli","year":"2015","journal-title":"Food Chem."},{"key":"2026090315571490400_cit36","doi-asserted-by":"publisher","first-page":"1508","DOI":"10.1016\/j.bbamem.2009.04.002","article-title":"The role of fatty acid\nunsaturation in minimizing biophysical changes on the structure and\nlocal effects of bilayer membranes","volume":"1788","author":"Leekumjorn","year":"2009","journal-title":"Biochim.\nBiophys. 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Food Chem."},{"key":"2026090315571490400_cit40","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0089122","article-title":"A vanillin derivative causes mitochondrial dysfunction\nand triggers oxidative stress in Cryptococcus neoformans","volume":"9","author":"Kim","year":"2014","journal-title":"PLoS One"},{"key":"2026090315571490400_cit41","doi-asserted-by":"publisher","first-page":"2421","DOI":"10.3389\/fmicb.2017.02421","article-title":"Antimicrobial potential of carvacrol\nagainst uropathogenic Escherichia coli via membrane disruption, depolarization,\nand reactive oxygen species generation","volume":"8","author":"Khan","year":"2017","journal-title":"Front.\nMicrobiol."},{"key":"2026090315571490400_cit42","doi-asserted-by":"publisher","first-page":"239","DOI":"10.3389\/fmicb.2018.00239","article-title":"A Damaged oxidative\nphosphorylation mechanism is involved in the antifungal activity of\ncitral against Penicillium digitatum","volume":"9","author":"OuYang","year":"2018","journal-title":"Front.\nMicrobiol."},{"key":"2026090315571490400_cit43","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.foodchem.2017.04.172","article-title":"Tea tree oil exhibits antifungal activity against Botrytis cinerea\nby affecting mitochondria","volume":"234","author":"Li","year":"2017","journal-title":"Food Chem."},{"key":"2026090315571490400_cit44","doi-asserted-by":"publisher","first-page":"2419","DOI":"10.3389\/fmicb.2017.02419","article-title":"Eugenol induces\nphenotypic alterations and increases the oxidative burst in Cryptococcus","volume":"8","author":"Alves","year":"2017","journal-title":"Front. Microbiol."},{"key":"2026090315571490400_cit45","doi-asserted-by":"publisher","first-page":"1423","DOI":"10.3389\/fmicb.2017.01423","article-title":"Capsule enlargement in Cryptococcus\nneoformans is dependent on mitochondrial activity","volume":"8","author":"Trevijano-Contador","year":"2017","journal-title":"Front. Microbiol."},{"key":"2026090315571490400_cit46","doi-asserted-by":"publisher","first-page":"1476644","DOI":"10.1080\/20002297.2018.1476644","article-title":"Fluconazole impacts the extracellular matrix of fluconazole-susceptible\nand -resistant Candida albicans and Candida glabrata biofilms","volume":"10","author":"Panariello","year":"2018","journal-title":"J. Oral Microbiol."},{"key":"2026090315571490400_cit47","doi-asserted-by":"publisher","first-page":"4592","DOI":"10.1128\/aem.02506-06","article-title":"Cryptococcus\nneoformans biofilm formation depends on surface support and carbon\nsource and reduces fungal cell susceptibility to heat, cold, and UV\nlight","volume":"73","author":"Martinez","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"2026090315571490400_cit48","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1093\/glycob\/cwy030","article-title":"Unraveling synthesis\nof the cryptococcal cell wall and capsule","volume":"28","author":"Wang","year":"2018","journal-title":"Glycobiology"},{"key":"2026090315571490400_cit49","doi-asserted-by":"crossref","first-page":"1836","DOI":"10.1128\/iai.65.5.1836-1841.1997","article-title":"Cellular charge of Cryptococcus neoformans:\ncontributions from the capsular polysaccharide, melanin, and monoclonal\nantibody binding","volume":"65","author":"Nosanchuk","year":"1997","journal-title":"Infect. Immun."},{"key":"2026090315571490400_cit50","doi-asserted-by":"publisher","first-page":"653","DOI":"10.1111\/1348-0421.12331","article-title":"Correlation between biofilm production,\nantibiotic susceptibility and exopolysaccharide composition inBurkholderia\npseudomalleibpsI,ppk, andrpoS mutant strains","volume":"59","author":"Mongkolrob","year":"2015","journal-title":"Microbiol. Immunol."},{"key":"2026090315571490400_cit51","doi-asserted-by":"publisher","first-page":"154","DOI":"10.4172\/jbb.1000151","article-title":"Carvacrol\nand Thymol for Fresh Food Packaging","volume":"5","author":"Ramos","year":"2013","journal-title":"J. Bioequivalence\nBioavailability"},{"key":"2026090315571490400_cit52","doi-asserted-by":"publisher","first-page":"421","DOI":"10.3109\/13693780903136879","article-title":"Temperature\naffects the susceptibility ofCryptococcus neoformansbiofilms to antifungal\nagents","volume":"48","author":"Pettit","year":"2010","journal-title":"Med. Mycol."},{"key":"2026090315571490400_cit53","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1007\/s11046-012-9575-2","article-title":"Cryptococcus laurentii Biofilms:\nStructure, Development and Antifungal Drug Resistance","volume":"174","author":"Ajesh","year":"2012","journal-title":"Mycopathologia"},{"key":"2026090315571490400_cit54","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1021\/ac60111a017","article-title":"Colorimetric method for determination\nof sugars and related substances","volume":"28","author":"Dubois","year":"1956","journal-title":"Anal. Chem."},{"key":"2026090315571490400_cit55","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1006\/abio.1976.9999","article-title":"A rapid and sensitive method for the quantitation of\nmicrogram quantities of protein utilizing the principle of protein-dye\nbinding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"2026090315571490400_cit56","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1038\/nprot.2006.59","article-title":"Gas chromatography mass spectrometry-based metabolite\nprofiling in plants","volume":"1","author":"Lisec","year":"2015","journal-title":"Nat. Protoc."},{"key":"2026090315571490400_cit57","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1007\/s12010-016-2086-8","article-title":"Boosting TAG accumulation\nwith improved biodiesel production from novel oleaginous microalgae\nScenedesmus sp. IITRIND2 utilizing waste sugarcane bagasse aqueous\nextract (SBAE)","volume":"180","author":"Arora","year":"2016","journal-title":"Appl. Biochem. 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