<named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty Acids
ABSTRACT Staphylococcus aureus is a major pathogen, which colonizes one in three otherwise healthy humans. This significant spread of S. aureus is largely due to its ability to circumvent innate immune responses, including antimicrobial fatty acids (AFAs) on the skin and in nasal secretions. In resp...
| Main Authors: | , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-10-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00804-20 |
| _version_ | 1818856780162138112 |
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| author | Arnaud Kengmo Tchoupa Andreas Peschel |
| author_facet | Arnaud Kengmo Tchoupa Andreas Peschel |
| author_sort | Arnaud Kengmo Tchoupa |
| collection | DOAJ |
| description | ABSTRACT Staphylococcus aureus is a major pathogen, which colonizes one in three otherwise healthy humans. This significant spread of S. aureus is largely due to its ability to circumvent innate immune responses, including antimicrobial fatty acids (AFAs) on the skin and in nasal secretions. In response to AFAs, S. aureus swiftly induces resistance mechanisms, which have yet to be completely elucidated. Here, we identify membrane vesicle (MV) release as a resistance strategy used by S. aureus to sequester host-specific AFAs. MVs protect S. aureus against a wide array of AFAs. Strikingly, beside MV production, S. aureus modulates MV composition upon exposure to AFAs. MVs purified from bacteria grown in the presence of linoleic acid display a distinct protein content and are enriched in lipoproteins, which strongly activate Toll-like receptor 2 (TLR2). Cumulatively, our findings reveal the protective capacities of MVs against AFAs, which are counteracted by an increased TLR2-mediated innate immune response. IMPORTANCE The nares of one in three humans are colonized by Staphylococcus aureus. In these environments, and arguably on all mucosal surfaces, bacteria encounter fatty acids with antimicrobial properties. Our study uncovers that S. aureus releases membrane vesicles (MVs) that act as decoys to protect the bacterium against antimicrobial fatty acids (AFAs). The AFA-neutralizing effects of MVs were neither strain specific nor restricted to one particular AFA. Hence, MVs may represent “public goods” playing an overlooked role in shaping bacterial communities in AFA-rich environments such as the skin and nose. Intriguingly, in addition to MV biogenesis, S. aureus modulates MV composition in response to exposure to AFAs, including an increased release of lipoproteins. These MVs strongly stimulate the innate immunity via Toll-like receptor 2 (TLR2). TLR2-mediated inflammation, which helps to fight infections, may exacerbate inflammatory disorders like atopic dermatitis. Our study highlights intricate immune responses preventing infections from colonizing bacteria. |
| first_indexed | 2024-12-19T08:29:56Z |
| format | Article |
| id | doaj.art-b1eac4bcc38345f590a43f6dbbd85ae1 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-19T08:29:56Z |
| publishDate | 2020-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-b1eac4bcc38345f590a43f6dbbd85ae12022-12-21T20:29:13ZengAmerican Society for MicrobiologymSphere2379-50422020-10-015510.1128/mSphere.00804-20<named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty AcidsArnaud Kengmo Tchoupa0Andreas Peschel1Department of Infection Biology, Interfaculty Institute for Microbiology and Infection Medicine Tübingen (IMIT), University of Tübingen, Tübingen, GermanyDepartment of Infection Biology, Interfaculty Institute for Microbiology and Infection Medicine Tübingen (IMIT), University of Tübingen, Tübingen, GermanyABSTRACT Staphylococcus aureus is a major pathogen, which colonizes one in three otherwise healthy humans. This significant spread of S. aureus is largely due to its ability to circumvent innate immune responses, including antimicrobial fatty acids (AFAs) on the skin and in nasal secretions. In response to AFAs, S. aureus swiftly induces resistance mechanisms, which have yet to be completely elucidated. Here, we identify membrane vesicle (MV) release as a resistance strategy used by S. aureus to sequester host-specific AFAs. MVs protect S. aureus against a wide array of AFAs. Strikingly, beside MV production, S. aureus modulates MV composition upon exposure to AFAs. MVs purified from bacteria grown in the presence of linoleic acid display a distinct protein content and are enriched in lipoproteins, which strongly activate Toll-like receptor 2 (TLR2). Cumulatively, our findings reveal the protective capacities of MVs against AFAs, which are counteracted by an increased TLR2-mediated innate immune response. IMPORTANCE The nares of one in three humans are colonized by Staphylococcus aureus. In these environments, and arguably on all mucosal surfaces, bacteria encounter fatty acids with antimicrobial properties. Our study uncovers that S. aureus releases membrane vesicles (MVs) that act as decoys to protect the bacterium against antimicrobial fatty acids (AFAs). The AFA-neutralizing effects of MVs were neither strain specific nor restricted to one particular AFA. Hence, MVs may represent “public goods” playing an overlooked role in shaping bacterial communities in AFA-rich environments such as the skin and nose. Intriguingly, in addition to MV biogenesis, S. aureus modulates MV composition in response to exposure to AFAs, including an increased release of lipoproteins. These MVs strongly stimulate the innate immunity via Toll-like receptor 2 (TLR2). TLR2-mediated inflammation, which helps to fight infections, may exacerbate inflammatory disorders like atopic dermatitis. Our study highlights intricate immune responses preventing infections from colonizing bacteria.https://journals.asm.org/doi/10.1128/mSphere.00804-20Staphylococcus aureusToll-like receptorsantimicrobial fatty acidslipoproteinsmembrane vesicles |
| spellingShingle | Arnaud Kengmo Tchoupa Andreas Peschel <named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty Acids mSphere Staphylococcus aureus Toll-like receptors antimicrobial fatty acids lipoproteins membrane vesicles |
| title | <named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty Acids |
| title_full | <named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty Acids |
| title_fullStr | <named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty Acids |
| title_full_unstemmed | <named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty Acids |
| title_short | <named-content content-type="genus-species">Staphylococcus aureus</named-content> Releases Proinflammatory Membrane Vesicles To Resist Antimicrobial Fatty Acids |
| title_sort | named content content type genus species staphylococcus aureus named content releases proinflammatory membrane vesicles to resist antimicrobial fatty acids |
| topic | Staphylococcus aureus Toll-like receptors antimicrobial fatty acids lipoproteins membrane vesicles |
| url | https://journals.asm.org/doi/10.1128/mSphere.00804-20 |
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