The Skin Microbiota: Balancing Risk and Reward

Abstract

The skin microbiome is an ecosystem comprised of a multitude of microbial species interacting with their surroundings, including other microbes and host epithelial and immune cells. These interactions are the basis of important roles within the skin microbiome that provide benefit to the host, boosting multiple aspects of barrier function, a critical function of this essential organ. However, with reward always comes risk; resident skin microbes function in a context-dependent manner, set on the backdrop of a dynamic host and microbial milieu. Here, we discuss the reward of hosting a microbial ecosystem on the skin, including protection from pathogens and tuning of the skin microenvironment. We also give consideration to how these skin residents, often termed "commensals" can cause disorder, damage, and promote skin disease.

Keywords: commensal microbes; cutaneous disease; dermatology; microbiome; skin.

Figure 1.. Microbiota-Host Interactions Promote Skin Homeostasis and Immune Response

Multiple microbial species residing in skin promote immune tolerance, elicit pro-inflammatory response, and aid in skin maintenance; in turn, the host provides nutrients to sustain microbial survival. Staphylococcus epidermidis, a model example of the intimate relationship microbiota has with the host, can both stimulate and suppress inflammation. Such microbial-host interactions contribute to stability of the microbial ecosystem and skin integrity. Other species such as Roseomonas mucosa, Malassezia spp., or Corynebacterium accolens can also tune keratinocyte and host immune responses in a context-dependent manner. Lastly, even the often-problematic skin resident microbe, Cutibacterium acnes, has beneficial interactions with the host as it metabolizes sebum secretions, which in turn aides in maintaining an acidic skin pH, making the skin suitable for select organisms.

Figure 2.. Risk: Diseases with Causative Agents from or Associated with Skin Microbiota

Microbiota that are most abundant and commonly found in skin microbiome datasets have been identified as the causative agents of the skin disorders and diseases shown here. The species contributing to disease are often body site dependent, a reflection of microbial niche specificity. For instance, both Malassezia spp. and Cutibacterium acnes prefer sebum rich environments, thus high abundance of these species at sebum rich sites, such as the scalp or the face, can lead to host disease. Unfortunately, many species can cause serious systemic disease if given the opportunity to transit to deeper tissue. This occurs most often in immunocompromised host in the form of bacteremia, surgical site soft tissue infections (SSTI), osteomyelitis, and/or chronic wounds.

Figure 3.. Reward: Microbiota Targeting of Pathogens Associated with Skin Disorders or Disease

Microbial-microbial interactions between the skin microbiome (white circles) and pathogens (pink circles) demonstrate the powerful benefit the skin microbiome can have for the host. CoNs, Corynebacterium spp, and Roseomonas mucosa target (arrows point from the source to the target) Staphylococcus aureus. These bacteria can either directly kill through the secretion of antimicrobial factors or limit the virulence of Staphylococcus aureus through the secretion of an inhibitor or suppressor of a major S. aureus virulence regulator. Other skin microbial species can target and limit Cutibacterium acnes, Streptococcus pyogenes, and Streptococcus pneumoniae.

Figure 4.. Colonization Resistance, a Collective Contribution of the Skin Microbiome

The skin microbiome is composed of a diverse microbial community; as also defined in Figure 1, this diversity spans through domains, from kingdom to strain. A recently recognized essential function of the skin microbiome is to provide protection against pathogens, termed colonization resistance. The skin microbiome achieves this through the capability to directly kill or alter the virulence of pathogens through the secretion of antimicrobial peptides and other molecules. Additionally, as many species are capable of stimulating keratinocytes, the microbiome can signal to the host to mount a protective immune response to invading pathogens. Importantly, the combined microbial-microbial and microbial-host interactions play a critical role in maintaining host health.