Abstract

ABSTRACTCutibacterium 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.

Highlights

  • Cutibacterium acnes is a human skin-resident bacterium

  • To examine the effects of C. acnes strains with diverse genetic backgrounds on the life span of C. elegans, we tested a series of C. acnes strains, namely, ATCC 6919, HL063PA1, SK137, HL038PA1, HL110PA1, HL030PA2, HL030PA1, HL082PA2, and HL110PA4 (Table 1)

  • Because nonpathogenic C. acnes HL110PA4 induced the expression of genes involved in defense against Gram-positive bacteria, we examined the effect of C. acnes HL110PA4 on host resistance to S. aureus, which is a Gram-positive, opportunistic pathogen and a human skinresident microbe

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Summary

Introduction

Cutibacterium acnes is a human skin-resident bacterium. C. acnes maintains skin health by inhibiting invasion from pathogens like Staphylococcus aureus, it contributes to several diseases, including acne. Cutibacterium acnes, a Gram-positive, aerotolerant anaerobic bacterium [2], is one of the most common and abundant bacterial species residing on the human skin [3, 4], in sebaceous areas [1]. It is associated with acne vulgaris, a chronic inflammatory disease of the pilosebaceous unit, affecting more than 85% of adolescents and young adults [5]. The clinical association of C. acnes strains with disease or health has been corroborated experimentally in vitro and in a murine model, in which the application of acne-associated C. acnes strains (type IA2, RT4/5) led to the development of moderate-to-severe skin pathology and induced the production of proinflammatory cytokines compared with the application of health-associated type II (RT2/6) C. acnes strains [14]

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