Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitis
Antibiotic therapy is the primary treatment for bovine mastitis, but the drawbacks of this strategy include poor cure rate and economic losses from the need to discard milk with antibiotic residues. Unfortunately, few other treatment options are currently available for mastitis. Failure of antibioti...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-12-01
|
| Series: | Biofilm |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2590207523000461 |
| _version_ | 1827578619260567552 |
|---|---|
| author | Wen-Chun Lin Kai-Chen Hsu Ming-Feng You Kuo-Hua Lee Chau-Hwa Chi Jyh-Yih Chen |
| author_facet | Wen-Chun Lin Kai-Chen Hsu Ming-Feng You Kuo-Hua Lee Chau-Hwa Chi Jyh-Yih Chen |
| author_sort | Wen-Chun Lin |
| collection | DOAJ |
| description | Antibiotic therapy is the primary treatment for bovine mastitis, but the drawbacks of this strategy include poor cure rate and economic losses from the need to discard milk with antibiotic residues. Unfortunately, few other treatment options are currently available for mastitis. Failure of antibiotic treatments is often attributed to formation of bacterial biofilms and abscesses in the mammary gland tissue, which lead to chronic infections that are difficult to eradicate and drive recurrent disease. A major mastitis-causing pathogen (MCP) associated with biofilms in bovine mastitis is Staphylococcus aureus. In this study, we demonstrate that octanoic acid has broad-spectrum microbicidal activity against MCPs and effectively inhibits S. aureus biofilm formation in milk (>50% inhibition at 3.13 mM). Octanoic acid effectively clears biofilms (95% eradication at 1X minimum bactericidal concentration, MBC) and infrequently induces S. aureus small colony variants (SCVs) that may cause recurrent mastitis. Additionally, octanoic acid rapidly kills persistent biofilm cells and cells with antibiotic tolerance (within 4 h). In contrast, antibiotics treated at >100X MBC cannot eradicate biofilms but do induce SCVs and antibiotic-tolerant cells. These effects may accelerate the transition from biofilm to chronic infection. Thus, octanoic acid exhibits bactericidal action against S. aureus biofilms, and it is less likely than antibiotic therapy to induce persistent cells and pathogen tolerance. Moreover, octanoic acid acts additively with antibiotics against S. aureus, and it attenuates tetracycline-induced virulence factor gene expression in S. aureus cells. According to these data, octanoic acid may prevent the pathological progression of bovine mastitis and offer a new strategy for treating the condition. |
| first_indexed | 2024-03-08T21:49:07Z |
| format | Article |
| id | doaj.art-654ecdf99ffe4a6bba44985d18682aa9 |
| institution | Directory Open Access Journal |
| issn | 2590-2075 |
| language | English |
| last_indexed | 2024-03-08T21:49:07Z |
| publishDate | 2023-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Biofilm |
| spelling | doaj.art-654ecdf99ffe4a6bba44985d18682aa92023-12-20T07:36:43ZengElsevierBiofilm2590-20752023-12-016100149Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitisWen-Chun Lin0Kai-Chen Hsu1Ming-Feng You2Kuo-Hua Lee3Chau-Hwa Chi4Jyh-Yih Chen5Marine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, 23-10 Dahuen Road, Jiaushi, Ilan, 262, TaiwanDepartment of Veterinary Medicine, National Taiwan University, Taipei, TaiwanMarine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, 23-10 Dahuen Road, Jiaushi, Ilan, 262, TaiwanHsin-Chu Branch Station, COA- TRI, Hsin-Chu, Taiwan; Corresponding author. No. 207-5, Bi-tou-mian, Wu-hoo village, Si-hoo Township, Miaoli County, Taiwan.Department of Veterinary Medicine, National Taiwan University, Taipei, Taiwan; Corresponding author. No. 1, Sec. 4, Roosevelt Road, Taipei City, Taiwan.Marine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, 23-10 Dahuen Road, Jiaushi, Ilan, 262, Taiwan; The iEGG and Animal Biotechnology Center and the Rong Hsing Research Center for Translational Medicine, National Chung Hsing University, Taichung, 402, Taiwan; Corresponding author. Marine Research Station, Institute of Cellular and Organismic Biology, Academia Sinica, 23-10 Dahuen Rd. Jiaushi, Ilan, 262, Taiwan.Antibiotic therapy is the primary treatment for bovine mastitis, but the drawbacks of this strategy include poor cure rate and economic losses from the need to discard milk with antibiotic residues. Unfortunately, few other treatment options are currently available for mastitis. Failure of antibiotic treatments is often attributed to formation of bacterial biofilms and abscesses in the mammary gland tissue, which lead to chronic infections that are difficult to eradicate and drive recurrent disease. A major mastitis-causing pathogen (MCP) associated with biofilms in bovine mastitis is Staphylococcus aureus. In this study, we demonstrate that octanoic acid has broad-spectrum microbicidal activity against MCPs and effectively inhibits S. aureus biofilm formation in milk (>50% inhibition at 3.13 mM). Octanoic acid effectively clears biofilms (95% eradication at 1X minimum bactericidal concentration, MBC) and infrequently induces S. aureus small colony variants (SCVs) that may cause recurrent mastitis. Additionally, octanoic acid rapidly kills persistent biofilm cells and cells with antibiotic tolerance (within 4 h). In contrast, antibiotics treated at >100X MBC cannot eradicate biofilms but do induce SCVs and antibiotic-tolerant cells. These effects may accelerate the transition from biofilm to chronic infection. Thus, octanoic acid exhibits bactericidal action against S. aureus biofilms, and it is less likely than antibiotic therapy to induce persistent cells and pathogen tolerance. Moreover, octanoic acid acts additively with antibiotics against S. aureus, and it attenuates tetracycline-induced virulence factor gene expression in S. aureus cells. According to these data, octanoic acid may prevent the pathological progression of bovine mastitis and offer a new strategy for treating the condition.http://www.sciencedirect.com/science/article/pii/S2590207523000461Octanoic acidStaphylococcus aureus biofilmsPersistence cellsAntibiotic tolerance cellsRecurrent mastitis |
| spellingShingle | Wen-Chun Lin Kai-Chen Hsu Ming-Feng You Kuo-Hua Lee Chau-Hwa Chi Jyh-Yih Chen Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitis Biofilm Octanoic acid Staphylococcus aureus biofilms Persistence cells Antibiotic tolerance cells Recurrent mastitis |
| title | Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitis |
| title_full | Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitis |
| title_fullStr | Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitis |
| title_full_unstemmed | Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitis |
| title_short | Octanoic acid promotes clearance of antibiotic-tolerant cells and eradicates biofilms of Staphylococcus aureus isolated from recurrent bovine mastitis |
| title_sort | octanoic acid promotes clearance of antibiotic tolerant cells and eradicates biofilms of staphylococcus aureus isolated from recurrent bovine mastitis |
| topic | Octanoic acid Staphylococcus aureus biofilms Persistence cells Antibiotic tolerance cells Recurrent mastitis |
| url | http://www.sciencedirect.com/science/article/pii/S2590207523000461 |
| work_keys_str_mv | AT wenchunlin octanoicacidpromotesclearanceofantibiotictolerantcellsanderadicatesbiofilmsofstaphylococcusaureusisolatedfromrecurrentbovinemastitis AT kaichenhsu octanoicacidpromotesclearanceofantibiotictolerantcellsanderadicatesbiofilmsofstaphylococcusaureusisolatedfromrecurrentbovinemastitis AT mingfengyou octanoicacidpromotesclearanceofantibiotictolerantcellsanderadicatesbiofilmsofstaphylococcusaureusisolatedfromrecurrentbovinemastitis AT kuohualee octanoicacidpromotesclearanceofantibiotictolerantcellsanderadicatesbiofilmsofstaphylococcusaureusisolatedfromrecurrentbovinemastitis AT chauhwachi octanoicacidpromotesclearanceofantibiotictolerantcellsanderadicatesbiofilmsofstaphylococcusaureusisolatedfromrecurrentbovinemastitis AT jyhyihchen octanoicacidpromotesclearanceofantibiotictolerantcellsanderadicatesbiofilmsofstaphylococcusaureusisolatedfromrecurrentbovinemastitis |