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Control of Staphylococcus aureus infection by biosurfactant derived from Bacillus rugosus HH2: Strain isolation, structural characterization, and mechanistic insights
Novel antimicrobials are urgently needed to combat methicillin-resistant Staphylococcus aureus (MRSA) infections. This study explores the potential of biosurfactants derived from Bacillus rugosus HH2 as a novel antibacterial agent against MRSA. The biosurfactant, identified as surfactin, demonstrate...
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Published in: | Journal of hazardous materials 2024-12, Vol.480, p.136402, Article 136402 |
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creator | Jeong, Geum-Jae Kim, Do-Kyun Park, Dong-Joo Cho, Kyung-Jin Kim, Min-Ung Oh, Do Kyung Tabassum, Nazia Jung, Won-Kyo Khan, Fazlurrahman Kim, Young-Mog |
description | Novel antimicrobials are urgently needed to combat methicillin-resistant Staphylococcus aureus (MRSA) infections. This study explores the potential of biosurfactants derived from Bacillus rugosus HH2 as a novel antibacterial agent against MRSA. The biosurfactant, identified as surfactin, demonstrated surface-active properties, reducing surface tension to 37.63 mN/m and lowering contact angles in a concentration-dependent manner. It remained stable across a wide range of pH (4−10), temperatures (30–80 °C), and salinity levels (3–18 %). The biosurfactant inhibited the growth of both methicillin-sensitive S. aureus and MRSA, with minimum inhibitory concentrations ranging from 128 to 256 μg/mL. Additionally, it showed anti-biofilm activity, preventing biofilm formation and dispersing established biofilms. Field-emission scanning electron microscopy revealed that the biosurfactant disrupted bacterial cell membranes, leading to leakage. Furthermore, it reduced the production of virulence factors in S. aureus, including hemolysin and lipase. Transcriptomic analysis indicated downregulation of genes associated with quorum sensing and cell adhesion in MRSA. Molecular docking studies showed strong interactions between surfactin and key MRSA proteins, underscoring its potential to overcome antibiotic resistance. Biocompatibility was confirmed through in vitro cytotoxicity and in vivo phytotoxicity tests. In summary, this study presents surfactin as a promising novel antibacterial agent against MRSA, providing insights into its mechanisms of action.
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•B. rugosus HH2 produces biosurfactants identified as surfactin.•The biosurfactants showed excellent surface activity and stability.•The biosurfactants exhibited anti-S. aureus activity.•RT-PCR and molecular docking analyses revealed the mechanism of action in S. aureus.•The biosurfactants demonstrated biocompatibility at both in vitro and in vivo levels. |
doi_str_mv | 10.1016/j.jhazmat.2024.136402 |
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[Display omitted]
•B. rugosus HH2 produces biosurfactants identified as surfactin.•The biosurfactants showed excellent surface activity and stability.•The biosurfactants exhibited anti-S. aureus activity.•RT-PCR and molecular docking analyses revealed the mechanism of action in S. aureus.•The biosurfactants demonstrated biocompatibility at both in vitro and in vivo levels.</description><identifier>ISSN: 0304-3894</identifier><identifier>ISSN: 1873-3336</identifier><identifier>EISSN: 1873-3336</identifier><identifier>DOI: 10.1016/j.jhazmat.2024.136402</identifier><identifier>PMID: 39509879</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Anti-Bacterial Agents - chemistry ; Anti-Bacterial Agents - pharmacology ; Anti-Staphylococcus aureus ; Bacillus - drug effects ; Bacillus - metabolism ; Bacillus rugosus ; Biofilms - drug effects ; Biosurfactant ; Lipopeptides - chemistry ; Lipopeptides - pharmacology ; Methicillin-Resistant Staphylococcus aureus - drug effects ; Microbial Sensitivity Tests ; Molecular Docking Simulation ; Staphylococcal Infections - drug therapy ; Staphylococcal Infections - microbiology ; Staphylococcus aureus - drug effects ; Surface-Active Agents - chemistry ; Surface-Active Agents - pharmacology ; Surfactin</subject><ispartof>Journal of hazardous materials, 2024-12, Vol.480, p.136402, Article 136402</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c1589-58a92dbbd8f9b8aa0d11b4b2ac3c1b031617d7bbc324d96a4dd8094f0dae8d353</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39509879$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jeong, Geum-Jae</creatorcontrib><creatorcontrib>Kim, Do-Kyun</creatorcontrib><creatorcontrib>Park, Dong-Joo</creatorcontrib><creatorcontrib>Cho, Kyung-Jin</creatorcontrib><creatorcontrib>Kim, Min-Ung</creatorcontrib><creatorcontrib>Oh, Do Kyung</creatorcontrib><creatorcontrib>Tabassum, Nazia</creatorcontrib><creatorcontrib>Jung, Won-Kyo</creatorcontrib><creatorcontrib>Khan, Fazlurrahman</creatorcontrib><creatorcontrib>Kim, Young-Mog</creatorcontrib><title>Control of Staphylococcus aureus infection by biosurfactant derived from Bacillus rugosus HH2: Strain isolation, structural characterization, and mechanistic insights</title><title>Journal of hazardous materials</title><addtitle>J Hazard Mater</addtitle><description>Novel antimicrobials are urgently needed to combat methicillin-resistant Staphylococcus aureus (MRSA) infections. This study explores the potential of biosurfactants derived from Bacillus rugosus HH2 as a novel antibacterial agent against MRSA. The biosurfactant, identified as surfactin, demonstrated surface-active properties, reducing surface tension to 37.63 mN/m and lowering contact angles in a concentration-dependent manner. It remained stable across a wide range of pH (4−10), temperatures (30–80 °C), and salinity levels (3–18 %). The biosurfactant inhibited the growth of both methicillin-sensitive S. aureus and MRSA, with minimum inhibitory concentrations ranging from 128 to 256 μg/mL. Additionally, it showed anti-biofilm activity, preventing biofilm formation and dispersing established biofilms. Field-emission scanning electron microscopy revealed that the biosurfactant disrupted bacterial cell membranes, leading to leakage. Furthermore, it reduced the production of virulence factors in S. aureus, including hemolysin and lipase. Transcriptomic analysis indicated downregulation of genes associated with quorum sensing and cell adhesion in MRSA. Molecular docking studies showed strong interactions between surfactin and key MRSA proteins, underscoring its potential to overcome antibiotic resistance. Biocompatibility was confirmed through in vitro cytotoxicity and in vivo phytotoxicity tests. In summary, this study presents surfactin as a promising novel antibacterial agent against MRSA, providing insights into its mechanisms of action.
[Display omitted]
•B. rugosus HH2 produces biosurfactants identified as surfactin.•The biosurfactants showed excellent surface activity and stability.•The biosurfactants exhibited anti-S. aureus activity.•RT-PCR and molecular docking analyses revealed the mechanism of action in S. aureus.•The biosurfactants demonstrated biocompatibility at both in vitro and in vivo levels.</description><subject>Animals</subject><subject>Anti-Bacterial Agents - chemistry</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Anti-Staphylococcus aureus</subject><subject>Bacillus - drug effects</subject><subject>Bacillus - metabolism</subject><subject>Bacillus rugosus</subject><subject>Biofilms - drug effects</subject><subject>Biosurfactant</subject><subject>Lipopeptides - chemistry</subject><subject>Lipopeptides - pharmacology</subject><subject>Methicillin-Resistant Staphylococcus aureus - drug effects</subject><subject>Microbial Sensitivity Tests</subject><subject>Molecular Docking Simulation</subject><subject>Staphylococcal Infections - drug therapy</subject><subject>Staphylococcal Infections - microbiology</subject><subject>Staphylococcus aureus - drug effects</subject><subject>Surface-Active Agents - chemistry</subject><subject>Surface-Active Agents - pharmacology</subject><subject>Surfactin</subject><issn>0304-3894</issn><issn>1873-3336</issn><issn>1873-3336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkcuO0zAUhi0EYjoDjwDykgUpduwkDhsEFUORRmIBrK3jS6aunLj4MlLngXhOXLWwZXWkc_6Ljj6EXlGypoT27_br_Q4eZ8jrlrR8TVnPSfsEragYWMMY65-iFWGEN0yM_Apdp7QnhNCh48_RFRs7MophXKHfm7DkGDwOE_6e4bA7-qCD1iVhKNHW4ZbJ6uzCgtURKxdSiRPoDEvGxkb3YA2eYpjxJ9DO-2qI5b6KEt5u2_c1M4JbsEvBwynkLU45Fp1LBI_1DmKNqimPlyMsBs-27heXstO1PLn7XU4v0LMJfLIvL_MG_bz9_GOzbe6-ffm6-XjXaNqJsekEjK1RyohpVAKAGEoVVy1opqkijPZ0MINSmrXcjD1wYwQZ-UQMWGFYx27Qm3PuIYZfxaYsZ5e09R4WG0qSjLaCUdF1Q5V2Z6mOIaVoJ3mIboZ4lJTIEyK5lxdE8oRInhFV3-tLRVGzNf9cf5lUwYezwNZHH5yNMmlnF22Ni5WENMH9p-IPnk6qXA</recordid><startdate>20241205</startdate><enddate>20241205</enddate><creator>Jeong, Geum-Jae</creator><creator>Kim, Do-Kyun</creator><creator>Park, Dong-Joo</creator><creator>Cho, Kyung-Jin</creator><creator>Kim, Min-Ung</creator><creator>Oh, Do Kyung</creator><creator>Tabassum, Nazia</creator><creator>Jung, Won-Kyo</creator><creator>Khan, Fazlurrahman</creator><creator>Kim, Young-Mog</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20241205</creationdate><title>Control of Staphylococcus aureus infection by biosurfactant derived from Bacillus rugosus HH2: Strain isolation, structural characterization, and mechanistic insights</title><author>Jeong, Geum-Jae ; Kim, Do-Kyun ; Park, Dong-Joo ; Cho, Kyung-Jin ; Kim, Min-Ung ; Oh, Do Kyung ; Tabassum, Nazia ; Jung, Won-Kyo ; Khan, Fazlurrahman ; Kim, Young-Mog</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1589-58a92dbbd8f9b8aa0d11b4b2ac3c1b031617d7bbc324d96a4dd8094f0dae8d353</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Anti-Bacterial Agents - chemistry</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Anti-Staphylococcus aureus</topic><topic>Bacillus - drug effects</topic><topic>Bacillus - metabolism</topic><topic>Bacillus rugosus</topic><topic>Biofilms - drug effects</topic><topic>Biosurfactant</topic><topic>Lipopeptides - chemistry</topic><topic>Lipopeptides - pharmacology</topic><topic>Methicillin-Resistant Staphylococcus aureus - drug effects</topic><topic>Microbial Sensitivity Tests</topic><topic>Molecular Docking Simulation</topic><topic>Staphylococcal Infections - drug therapy</topic><topic>Staphylococcal Infections - microbiology</topic><topic>Staphylococcus aureus - drug effects</topic><topic>Surface-Active Agents - chemistry</topic><topic>Surface-Active Agents - pharmacology</topic><topic>Surfactin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jeong, Geum-Jae</creatorcontrib><creatorcontrib>Kim, Do-Kyun</creatorcontrib><creatorcontrib>Park, Dong-Joo</creatorcontrib><creatorcontrib>Cho, Kyung-Jin</creatorcontrib><creatorcontrib>Kim, Min-Ung</creatorcontrib><creatorcontrib>Oh, Do Kyung</creatorcontrib><creatorcontrib>Tabassum, Nazia</creatorcontrib><creatorcontrib>Jung, Won-Kyo</creatorcontrib><creatorcontrib>Khan, Fazlurrahman</creatorcontrib><creatorcontrib>Kim, Young-Mog</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of hazardous materials</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jeong, Geum-Jae</au><au>Kim, Do-Kyun</au><au>Park, Dong-Joo</au><au>Cho, Kyung-Jin</au><au>Kim, Min-Ung</au><au>Oh, Do Kyung</au><au>Tabassum, Nazia</au><au>Jung, Won-Kyo</au><au>Khan, Fazlurrahman</au><au>Kim, Young-Mog</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Control of Staphylococcus aureus infection by biosurfactant derived from Bacillus rugosus HH2: Strain isolation, structural characterization, and mechanistic insights</atitle><jtitle>Journal of hazardous materials</jtitle><addtitle>J Hazard Mater</addtitle><date>2024-12-05</date><risdate>2024</risdate><volume>480</volume><spage>136402</spage><pages>136402-</pages><artnum>136402</artnum><issn>0304-3894</issn><issn>1873-3336</issn><eissn>1873-3336</eissn><abstract>Novel antimicrobials are urgently needed to combat methicillin-resistant Staphylococcus aureus (MRSA) infections. This study explores the potential of biosurfactants derived from Bacillus rugosus HH2 as a novel antibacterial agent against MRSA. The biosurfactant, identified as surfactin, demonstrated surface-active properties, reducing surface tension to 37.63 mN/m and lowering contact angles in a concentration-dependent manner. It remained stable across a wide range of pH (4−10), temperatures (30–80 °C), and salinity levels (3–18 %). The biosurfactant inhibited the growth of both methicillin-sensitive S. aureus and MRSA, with minimum inhibitory concentrations ranging from 128 to 256 μg/mL. Additionally, it showed anti-biofilm activity, preventing biofilm formation and dispersing established biofilms. Field-emission scanning electron microscopy revealed that the biosurfactant disrupted bacterial cell membranes, leading to leakage. Furthermore, it reduced the production of virulence factors in S. aureus, including hemolysin and lipase. Transcriptomic analysis indicated downregulation of genes associated with quorum sensing and cell adhesion in MRSA. Molecular docking studies showed strong interactions between surfactin and key MRSA proteins, underscoring its potential to overcome antibiotic resistance. Biocompatibility was confirmed through in vitro cytotoxicity and in vivo phytotoxicity tests. In summary, this study presents surfactin as a promising novel antibacterial agent against MRSA, providing insights into its mechanisms of action.
[Display omitted]
•B. rugosus HH2 produces biosurfactants identified as surfactin.•The biosurfactants showed excellent surface activity and stability.•The biosurfactants exhibited anti-S. aureus activity.•RT-PCR and molecular docking analyses revealed the mechanism of action in S. aureus.•The biosurfactants demonstrated biocompatibility at both in vitro and in vivo levels.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>39509879</pmid><doi>10.1016/j.jhazmat.2024.136402</doi></addata></record> |
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subjects | Animals Anti-Bacterial Agents - chemistry Anti-Bacterial Agents - pharmacology Anti-Staphylococcus aureus Bacillus - drug effects Bacillus - metabolism Bacillus rugosus Biofilms - drug effects Biosurfactant Lipopeptides - chemistry Lipopeptides - pharmacology Methicillin-Resistant Staphylococcus aureus - drug effects Microbial Sensitivity Tests Molecular Docking Simulation Staphylococcal Infections - drug therapy Staphylococcal Infections - microbiology Staphylococcus aureus - drug effects Surface-Active Agents - chemistry Surface-Active Agents - pharmacology Surfactin |
title | Control of Staphylococcus aureus infection by biosurfactant derived from Bacillus rugosus HH2: Strain isolation, structural characterization, and mechanistic insights |
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