Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureus
ABSTRACT Cutibacterium acnes is a human skin-resident bacterium. Although C. acnes maintains skin health by inhibiting invasion from pathogens like Staphylococcus aureus, it also contributes to several diseases, including acne. Studies suggest that differences in genetic background may explain the d...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2021-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/Spectrum.00562-21 |
| _version_ | 1818940063311986688 |
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| author | Ayano Tsuru Yumi Hamazaki Shuta Tomida Mohammad Shaokat Ali Tomomi Komura Yoshikazu Nishikawa Eriko Kage-Nakadai |
| author_facet | Ayano Tsuru Yumi Hamazaki Shuta Tomida Mohammad Shaokat Ali Tomomi Komura Yoshikazu Nishikawa Eriko Kage-Nakadai |
| author_sort | Ayano Tsuru |
| collection | DOAJ |
| description | ABSTRACT Cutibacterium acnes is a human skin-resident bacterium. Although C. acnes maintains skin health by inhibiting invasion from pathogens like Staphylococcus aureus, it also contributes to several diseases, including acne. Studies suggest that differences in genetic background may explain the diverse phenotypes of C. acnes strains. In this study, we investigated the effects of C. acnes strains on the Caenorhabditis elegans life span and observed that some strains shortened the life span, whereas other strains, such as strain HL110PA4, did not alter it. Next, we assessed the effects of C. acnes HL110PA4 on host resistance against S. aureus. The survival time of C. acnes HL110PA4-fed wild-type animals was significantly longer than that of Escherichia coli OP50 control bacterium-fed worms upon infection with S. aureus. Although the survival times of worms harboring mutations at the daf-16/FoxO and skn-1/Nrf2 loci were similar to those of wild-type worms after S. aureus infection, administration of C. acnes failed to improve survival times of tir-1/SARM1, nsy-1/mitogen-activated protein kinase kinase kinase (MAPKKK), sek-1/mitogen-activated protein kinase kinase (MAPKK), and pmk-1/p38 mitogen-activated protein kinase (MAPK) mutants. These results suggest that the TIR-1 and p38 MAPK pathways are involved in conferring host resistance against S. aureus in a C. acnes-mediated manner. IMPORTANCE Cutibacterium acnes is one of the most common bacterial species residing on the human skin. Although the pathogenic properties of C. acnes, such as its association with acne vulgaris, have been widely described, its beneficial aspects have not been well characterized. Our study classifies C. acnes strains based on its pathogenic potential toward the model host C. elegans and reveals that the life span of C. elegans worms fed on C. acnes was consistent with the clinical association of C. acnes ribotypes with acne or nonacne. Furthermore, nonpathogenic C. acnes confers host resistance against the opportunistic pathogen Staphylococcus aureus. Our study provides insights into the impact of C. acnes on the host immune system and its potential roles in the ecosystem of skin microbiota. |
| first_indexed | 2024-12-20T06:33:41Z |
| format | Article |
| id | doaj.art-9eebc85a16934c0581338fe785578080 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-20T06:33:41Z |
| publishDate | 2021-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-9eebc85a16934c0581338fe7855780802022-12-21T19:50:03ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-10-019210.1128/Spectrum.00562-21Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureusAyano Tsuru0Yumi Hamazaki1Shuta Tomida2Mohammad Shaokat Ali3Tomomi Komura4Yoshikazu Nishikawa5Eriko Kage-Nakadai6Graduate School of Human Life Science, Osaka City University, Osaka, JapanGraduate School of Human Life Science, Osaka City University, Osaka, JapanCenter for Comprehensive Genomic Medicine, Okayama University Hospital, Okayama, JapanGraduate School of Human Life Science, Osaka City University, Osaka, JapanGraduate School of Human Life Science, Osaka City University, Osaka, JapanGraduate School of Human Life Science, Osaka City University, Osaka, JapanGraduate School of Human Life Science, Osaka City University, Osaka, JapanABSTRACT Cutibacterium acnes is a human skin-resident bacterium. Although C. acnes maintains skin health by inhibiting invasion from pathogens like Staphylococcus aureus, it also contributes to several diseases, including acne. Studies suggest that differences in genetic background may explain the diverse phenotypes of C. acnes strains. In this study, we investigated the effects of C. acnes strains on the Caenorhabditis elegans life span and observed that some strains shortened the life span, whereas other strains, such as strain HL110PA4, did not alter it. Next, we assessed the effects of C. acnes HL110PA4 on host resistance against S. aureus. The survival time of C. acnes HL110PA4-fed wild-type animals was significantly longer than that of Escherichia coli OP50 control bacterium-fed worms upon infection with S. aureus. Although the survival times of worms harboring mutations at the daf-16/FoxO and skn-1/Nrf2 loci were similar to those of wild-type worms after S. aureus infection, administration of C. acnes failed to improve survival times of tir-1/SARM1, nsy-1/mitogen-activated protein kinase kinase kinase (MAPKKK), sek-1/mitogen-activated protein kinase kinase (MAPKK), and pmk-1/p38 mitogen-activated protein kinase (MAPK) mutants. These results suggest that the TIR-1 and p38 MAPK pathways are involved in conferring host resistance against S. aureus in a C. acnes-mediated manner. IMPORTANCE Cutibacterium acnes is one of the most common bacterial species residing on the human skin. Although the pathogenic properties of C. acnes, such as its association with acne vulgaris, have been widely described, its beneficial aspects have not been well characterized. Our study classifies C. acnes strains based on its pathogenic potential toward the model host C. elegans and reveals that the life span of C. elegans worms fed on C. acnes was consistent with the clinical association of C. acnes ribotypes with acne or nonacne. Furthermore, nonpathogenic C. acnes confers host resistance against the opportunistic pathogen Staphylococcus aureus. Our study provides insights into the impact of C. acnes on the host immune system and its potential roles in the ecosystem of skin microbiota.https://journals.asm.org/doi/10.1128/Spectrum.00562-21Caenorhabditis elegansCutibacterium acnesp38 MAPKStaphylococcus aureustir-1 |
| spellingShingle | Ayano Tsuru Yumi Hamazaki Shuta Tomida Mohammad Shaokat Ali Tomomi Komura Yoshikazu Nishikawa Eriko Kage-Nakadai Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureus Microbiology Spectrum Caenorhabditis elegans Cutibacterium acnes p38 MAPK Staphylococcus aureus tir-1 |
| title | Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureus |
| title_full | Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureus |
| title_fullStr | Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureus |
| title_full_unstemmed | Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureus |
| title_short | Nonpathogenic Cutibacterium acnes Confers Host Resistance against Staphylococcus aureus |
| title_sort | nonpathogenic cutibacterium acnes confers host resistance against staphylococcus aureus |
| topic | Caenorhabditis elegans Cutibacterium acnes p38 MAPK Staphylococcus aureus tir-1 |
| url | https://journals.asm.org/doi/10.1128/Spectrum.00562-21 |
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