The Evolution of Cosmetic Preservation and the Microbiological Challenges Posed by Sustainability

503 Evolution and Challenges of Sustainability
their gene/RNA sequences. The archaea are not known to cause skin infections, disease, or
product contamination consequently, they are not discussed in detail in this review.
In 2018, Byrd, Belkaid, and Segre studied bacteria on different anatomical sites using 16S
rRNA sequencing methodology.74 They reported the 10 most abundant bacteria found
in dry sites (e.g., hypothenar palm and volar forearm), moist sites (e.g., nares, antecubital
fossa, inguinal crease, interdigital web, and popliteal fossa), sebaceous sites (e.g., alar crease,
cheek, glabella, external auditory canal, manubrium, retroauricular crease, occiput, and
back), and the foot (e.g., toe web space, toenail, and plantar heel). The species identified are
listed in Table VI.
Fungi are also members of the skin microbiome and generally comprise members of the
Ascomycota and Basidiomycota phyla.74 The predominant genus is Malassezia spp. (formerly
Pityrosporum spp.), which grow in sebum rich regions of the skin, such as the scalp, face and
upper back) and have been associated with dandruff and seborrheic dermatitis. Byrd and
coworkers reported that the highest level of fungal diversity occurs on the feet, which
frequently are colonized by Aspergillus, Cryptococccus, Rhodotorula, and Epicoccum genera.
Byrd and coworkers also studied fungi on different anatomical sites and identified them
using the internal transcribed spacer 1 (ITS1) region of the eukaryotic ribosomal gene for
sequencing. They reported the 10 most abundant fungi found in the same four skin sites
as were used for the bacteria (above). The 10 most abundant fungal species identified are
listed in Table VII. The differences in the findings between Grice and coworkers and Byrd
and coworkers may be due to factors including different panelists, demographics, season of
the year, and methodology.
Most viruses on skin are bacteriophages (i.e., phages), which are viruses that infect and
replicate within bacteria and archaea. Natarelli, Gahoonia, and Sivamani observed that
viral diversity present in chronic wounds is increased compared to healthy skin.75 A study
conducted using an atopic mouse model showed favorable results for the use of phage
Table VI
Top 10 Abundant Bacterial on Various Skin Sites
Dry Moist Sebaceous Foot
Cutibacterium acnes Corynebacterium
tuberculostericum
Cutibacterium acnes Corynebacterium
tuberculostericum
Corynebacterium
tuberculostericum
Staphylococcus hominis Staphylococcal epidermidis Staphylococcus
hominis
Streptococcus mitis Cutibacterium acnes Corynebacterium
tuberculostericum
Staphylococcus
warneri
Streptococcus oralis Staphylococcus epidermidis Staphylococcus capitis Staphylococcus
epidermidis
Streptococcus pseudopneumoniae Staphylococcus capitis Corynebacterium stimulans Staphylococcus capitis
Streptococcus sanguinis Corynebacterium fastidiosum Streptococcus mitis Staphylococcus
haemolyticus
Micrococcus luteus Corynebacterium afermentans Staphylococcus hominis Micrococcus luteus
Staphylococcus epidermidis Micrococcus luteus Corynebacterium aurimucosum Corynebacterium
afermentans
Staphylococcus capitis Enhydrobacter aerosaccus Corynebacterium kroppenstedtii Corynebacterium
simulans
Veillonella parvula Corynebacterium simulans Corynebacterium amycolatum Corynebacterium
resistens
*Table adapted from Byrd, Belkaid, and Segre.74

504 JOURNAL OF COSMETIC SCIENCE
in controlling S. aureus growth on skin.76 Barnard et al.77 found that there was a greater
relative abundance of C. acnes phages in healthy skin compared to lesional skin of acne
test subjects. Natarelli and coworkers noted that phage-based therapeutic strategies appear
promising for the treatment of a variety of dermatological conditions.75
MICROBIAL INTERACTIONS WITH THE SKIN
Many researchers have considered the dominant skin bacteria to be commensals.66,68,78
However, information gained over the past several years indicates that some members of
the skin microflora benefit from the nutrients and environment provided by the skin and
the skin benefits by having improved barrier function, an activated SIS, and protection
from colonization by transients and pathogens.79,80 Although “commensalism” describes
the biological interaction in which members of one species gain benefits while other
species neither benefit nor are harmed and “mutualism” describes the biological interaction
between two or more organisms in which each organism has a net benefit, this review
considers commensals to be microorganisms that are either neutral or beneficial to skin.
Orth observed that skin microflora may confer some of the same benefits to skin as
probiotics do in the GI tract.78,81 These benefits are achieved by “colonization resistance”
which helps maintain homeostasis of the skin/skin microbiome ecosystem. Colonization
resistance involves:
1. Growth of commensal microorganisms on skin and mucous membranes lowers the pH,
which makes it more difficult for competing microorganisms (transients and pathogens)
to grow.
2. Commensal skin microflora compete with transients and pathogens for nutrients, which
makes it more difficult for them to grow.
3. Commensal skin microflora compete with transients and pathogens for epidermal
receptor sites and may block their colonization on skin.
4. Association of commensal skin microflora with immunologically competent cells in the
skin, such as keratinocytes and Langerhans cells, may stimulate the SIS so that it is a state
of readiness when stimulated by transients and potentially harmful microorganisms.
5. Crosstalk between the commensal skin microflora and keratinocytes enhances
antimicrobial peptide (AMP) expression by keratinocytes including human β-defensin
2 (HBD2), cathelicidin LL-37, ribonuclease-7, psoriasin (S100A7), and dermicidin.80-83
Table VII
Top 10 Abundant Fungi on Various Skin Sites
Dry Moist Sebaceous Foot
Malassezia restricta Malassezia globosa Malassezia restricta Malassezia restricta
Malassezia globosa Malassezia restricta Malassezia globosa Tricophyton rubrum
Aspergillus tubingensis Tielleti walkeri Malassezia sympodialis Malassezia globosa
Candida parapsilosis Malassezia sympodialis Aureoumbra lagunensis Pyramimonas parkeae
Zymoseptoria tritici Pyramimonas parkeae Tielleti walkeri Trychophyton mentogrophytes
Malassezia sympodialis Parachlorella kessleri Pycnococcus provosolii Parachlorella kessleri
Epidermophyton floccosum Aspergillus tubingensis Gracilaria tenuistipitata Aspergillus tubingensis
Pyramimonas parkeae Zymoseptoria tritici Pyramimonas parkeae Zymoseptoria tritici
Nannizzia nana Nephroselmis olivacea Parachlorella kessleri Gracilaria tenuistipitata
Parachlorella kessleri Cyanophora paradoxa Leucocytozoon majoris Nephroselmis olivacea
*Table adapted from Byrd, Belkaid, and Segre.74

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503 Evolution and Challenges of Sustainability
their gene/RNA sequences. The archaea are not known to cause skin infections, disease, or
product contamination consequently, they are not discussed in detail in this review.
In 2018, Byrd, Belkaid, and Segre studied bacteria on different anatomical sites using 16S
rRNA sequencing methodology.74 They reported the 10 most abundant bacteria found
in dry sites (e.g., hypothenar palm and volar forearm), moist sites (e.g., nares, antecubital
fossa, inguinal crease, interdigital web, and popliteal fossa), sebaceous sites (e.g., alar crease,
cheek, glabella, external auditory canal, manubrium, retroauricular crease, occiput, and
back), and the foot (e.g., toe web space, toenail, and plantar heel). The species identified are
listed in Table VI.
Fungi are also members of the skin microbiome and generally comprise members of the
Ascomycota and Basidiomycota phyla.74 The predominant genus is Malassezia spp. (formerly
Pityrosporum spp.), which grow in sebum rich regions of the skin, such as the scalp, face and
upper back) and have been associated with dandruff and seborrheic dermatitis. Byrd and
coworkers reported that the highest level of fungal diversity occurs on the feet, which
frequently are colonized by Aspergillus, Cryptococccus, Rhodotorula, and Epicoccum genera.
Byrd and coworkers also studied fungi on different anatomical sites and identified them
using the internal transcribed spacer 1 (ITS1) region of the eukaryotic ribosomal gene for
sequencing. They reported the 10 most abundant fungi found in the same four skin sites
as were used for the bacteria (above). The 10 most abundant fungal species identified are
listed in Table VII. The differences in the findings between Grice and coworkers and Byrd
and coworkers may be due to factors including different panelists, demographics, season of
the year, and methodology.
Most viruses on skin are bacteriophages (i.e., phages), which are viruses that infect and
replicate within bacteria and archaea. Natarelli, Gahoonia, and Sivamani observed that
viral diversity present in chronic wounds is increased compared to healthy skin.75 A study
conducted using an atopic mouse model showed favorable results for the use of phage
Table VI
Top 10 Abundant Bacterial on Various Skin Sites
Dry Moist Sebaceous Foot
Cutibacterium acnes Corynebacterium
tuberculostericum
Cutibacterium acnes Corynebacterium
tuberculostericum
Corynebacterium
tuberculostericum
Staphylococcus hominis Staphylococcal epidermidis Staphylococcus
hominis
Streptococcus mitis Cutibacterium acnes Corynebacterium
tuberculostericum
Staphylococcus
warneri
Streptococcus oralis Staphylococcus epidermidis Staphylococcus capitis Staphylococcus
epidermidis
Streptococcus pseudopneumoniae Staphylococcus capitis Corynebacterium stimulans Staphylococcus capitis
Streptococcus sanguinis Corynebacterium fastidiosum Streptococcus mitis Staphylococcus
haemolyticus
Micrococcus luteus Corynebacterium afermentans Staphylococcus hominis Micrococcus luteus
Staphylococcus epidermidis Micrococcus luteus Corynebacterium aurimucosum Corynebacterium
afermentans
Staphylococcus capitis Enhydrobacter aerosaccus Corynebacterium kroppenstedtii Corynebacterium
simulans
Veillonella parvula Corynebacterium simulans Corynebacterium amycolatum Corynebacterium
resistens
*Table adapted from Byrd, Belkaid, and Segre.74

504 JOURNAL OF COSMETIC SCIENCE
in controlling S. aureus growth on skin.76 Barnard et al.77 found that there was a greater
relative abundance of C. acnes phages in healthy skin compared to lesional skin of acne
test subjects. Natarelli and coworkers noted that phage-based therapeutic strategies appear
promising for the treatment of a variety of dermatological conditions.75
MICROBIAL INTERACTIONS WITH THE SKIN
Many researchers have considered the dominant skin bacteria to be commensals.66,68,78
However, information gained over the past several years indicates that some members of
the skin microflora benefit from the nutrients and environment provided by the skin and
the skin benefits by having improved barrier function, an activated SIS, and protection
from colonization by transients and pathogens.79,80 Although “commensalism” describes
the biological interaction in which members of one species gain benefits while other
species neither benefit nor are harmed and “mutualism” describes the biological interaction
between two or more organisms in which each organism has a net benefit, this review
considers commensals to be microorganisms that are either neutral or beneficial to skin.
Orth observed that skin microflora may confer some of the same benefits to skin as
probiotics do in the GI tract.78,81 These benefits are achieved by “colonization resistance”
which helps maintain homeostasis of the skin/skin microbiome ecosystem. Colonization
resistance involves:
1. Growth of commensal microorganisms on skin and mucous membranes lowers the pH,
which makes it more difficult for competing microorganisms (transients and pathogens)
to grow.
2. Commensal skin microflora compete with transients and pathogens for nutrients, which
makes it more difficult for them to grow.
3. Commensal skin microflora compete with transients and pathogens for epidermal
receptor sites and may block their colonization on skin.
4. Association of commensal skin microflora with immunologically competent cells in the
skin, such as keratinocytes and Langerhans cells, may stimulate the SIS so that it is a state
of readiness when stimulated by transients and potentially harmful microorganisms.
5. Crosstalk between the commensal skin microflora and keratinocytes enhances
antimicrobial peptide (AMP) expression by keratinocytes including human β-defensin
2 (HBD2), cathelicidin LL-37, ribonuclease-7, psoriasin (S100A7), and dermicidin.80-83
Table VII
Top 10 Abundant Fungi on Various Skin Sites
Dry Moist Sebaceous Foot
Malassezia restricta Malassezia globosa Malassezia restricta Malassezia restricta
Malassezia globosa Malassezia restricta Malassezia globosa Tricophyton rubrum
Aspergillus tubingensis Tielleti walkeri Malassezia sympodialis Malassezia globosa
Candida parapsilosis Malassezia sympodialis Aureoumbra lagunensis Pyramimonas parkeae
Zymoseptoria tritici Pyramimonas parkeae Tielleti walkeri Trychophyton mentogrophytes
Malassezia sympodialis Parachlorella kessleri Pycnococcus provosolii Parachlorella kessleri
Epidermophyton floccosum Aspergillus tubingensis Gracilaria tenuistipitata Aspergillus tubingensis
Pyramimonas parkeae Zymoseptoria tritici Pyramimonas parkeae Zymoseptoria tritici
Nannizzia nana Nephroselmis olivacea Parachlorella kessleri Gracilaria tenuistipitata
Parachlorella kessleri Cyanophora paradoxa Leucocytozoon majoris Nephroselmis olivacea
*Table adapted from Byrd, Belkaid, and Segre.74

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501 Evolution and Challenges of Sustainability
Oxidoreductive enzymes catalyze reactions to produce products that frequently are
cytotoxic and have antimicrobial activity. The use of natural oxidoreductive enzyme
systems including lactoperoxidase plus glucose oxidase for product preservation have been
developed to achieve mild preservation in response to the perceived consumer need for
products that do not contain traditional preservatives.63 In the presence of glucose substrate
and oxygen, glucose oxidase produces hydrogen peroxide, which then becomes a substrate
for lactoperoxidase. Lactoperoxidase uses hydrogen peroxide and an oxidizable anion such as
thiocyanate as a substrate to produce hypothiocyanate, which is believed to target exposed
sulfhydryl groups in the bacterial cell membrane and inhibit bacterial metabolism.63
Although this is an elegant biochemical system for achieving antimicrobial action, it does
not seem to have gained wide acceptance for use in the cosmetic industry.
In recent years, there has been an increase in the promotion of fermented ingredients for use
as safe and natural preservatives. Leucidal® Liquid is a natural preservative derived from
radishes fermented with Leuconostoc kimchii, a lactic acid bacterium that has traditionally
been used to make kimchi. Promotional material indicates that Leucidal® Liquid consists
of an isolated peptide that is secreted by the bacteria during the fermentation process. It is
likely that the peptide is a bacteriocin—a peptide antibiotic that may kill Gram-positive
bacteria by disrupting cell wall production and cell membrane functions.64 Leuconostoc spp.
are heterofermentative lactic acid bacteria, which produce lactic acid and lesser amounts of
acetic acid, ethanol, and carbon dioxide during fermentation. It is believed that the primary
antimicrobial action of this ferment would be due to the short-chain fatty acids, ethanol, and
bacteriocins. Leuconostoc/radish root ferment filtrate is a natural ingredient derived from
the fermentation of radish roots with Leuconostoc spp., resulting in a natural preservative with
antimicrobial peptides that are reported to target bacteria and fungi. The radish roots may
provide somewhat different substrates than radishes used for the Leucidal® Liquid, and this
may result in different fermentation products. However, it is likely that the antimicrobial
action of the Leuconostoc/radish root ferment filtrate would be like that of the Leucidal®
Liquid. Water/punica granatum fruit extract/Lactobacillus ferment is a preservative obtained
from Lactobacillus spp. fermentation of pomegranate (Punica granatum). The Lactobacillus spp.
used may be homofermentative, which means that it produces virtually only lactic acid
during fermentation, or it may be heterofermentative. The strain used may also produce
bacteriocins. It is likely that short-chain fatty acids and bacteriocins (if present) would be
responsible for preservative action at recommended use levels up to10% in formulations.
Saccharomyces/rice ferment filtrate is advertised to balance the skin’s microbiome, strengthen
the skin barrier, and improve moisture retention. Saccharomyces spp. is yeast. This ferment
is reported to contain essential minerals, amino acids, β-glucan and vitamins. The amino
acids may provide nutrients for the skin microflora. Yeast (1→3)-β-glucan is a biological
response regulator that is involved with activation of various immune cells, including
macrophages and neutrophils, resulting in increased production of interleukins, cytokines,
and antibodies that stimulate the immune system to prepare the body to better fight
against infection.65 Promotional materials indicate that it works by preserving the skin’s
natural microbiome balance.
THE SKIN MICROBIOME
The skin is the largest organ in the human body, and it provides an epithelial interface that
separates the body from the external environment. The skin helps maintain homeostasis

502 JOURNAL OF COSMETIC SCIENCE
by regulating temperature, preventing water loss from the body, reducing irritation/
injury due to harsh chemicals and harmful radiation, enabling touch and pain sensations,
supporting vitamin D synthesis, and preventing infection. The skin surface and appendages
are colonized by a diverse community of microorganisms, the “skin microbiome,” and
these microorganisms are involved with maintaining the skin ecosystem with their lipid
metabolism, colonization resistance to transient and pathogenic organisms, regulation of
the skin immune system (SIS), and creation of acid mantle condition of skin.66-69
The skin microbiome is composed of bacteria, yeasts, fungi, viruses, micro-eukaryotes
(mites), and archaea. Although the average number of microorganisms isolated from skin
using traditional culture methods (e.g., plating on agar media) ranges from 103–104 cfu/cm2,
humid places on the body, such as armpits, groin, and nostrils, may have microbial counts
exceeding 106 cfu/cm2. The microbial counts on the scalp, forehead and around the ears are
about 106 cfu/cm2, while microbial counts on the upper back, chest and arms range from
104–105 cfu/cm2.67,69,70 In 2016, Patra. Byrne and Wolf reported that 23–100% of healthy
people have dust mites, which generally are found on the face, around sebaceous glands,
and in hair follicles.71 Consequently, they are part of the normal microflora. Demodex mites
(Demodex folliculorum and Demodex brevis) are present on skin and may be associated with
rosacea and blepharitis.71
In the 2009 landmark publication by Grice et al., it was reported that skin sustains
microorganisms that influence human health and disease.72 They observed that traditional
culture-based characterizations of the skin microflora are biased toward species that readily
grow under standard laboratory conditions, such as the staphylococci, and that molecular
approaches have revealed a greater diversity of skin microflora in distinct topographical
regions of the skin. This provided the basis for examining multiple skin sites with the use
of genomic techniques.
Grice and coworkers analyzed 16S ribosomal RNA (rRNA) gene sequences from 20 distinct
skin sites of 10 healthy human test subjects and found that comparable sites on different
people harbor similar bacterial communities. Although the number of people being tested
was rather small, it was determined that 90% of the bacteria on skin could be classified
into four types (phyla): Actinobacteria (52% Gram positive bacteria with high (55%)
guanosine plus cytosine (G+C) DNA that include Corynebacterium, Actinomyces, Arthrobacter,
Micrococcus, Mycobacterium, Nocardia, Propionibacterium (Cutibacterium) and Rhodococcus
genera), Firmicutes (24% Gram positive bacteria with low G+C DNA content that include
Staphylococcus, Lactobacillus, Streptococcus, Clostridium and Bacillus genera), Proteobacteria
(16% Gram-negative bacteria that include Escherichia, Pseudomonas, Salmonella, Vibrio and
Helicobacter genera) and Bacteroidetes (6% Gram-negative rod-shaped bacteria that include
Bacteroides and Porphyromonas genera). Grice and coworkers found that coagulase negative
staphylococci (CNS) such as Staphylococcus epidermidis, along with Cutibacterium acnes
(formerly Propionibacterium acnes), Corynebacterium spp., Micrococcus spp., Streptococcus spp.,
and Acinetobacter spp. were the dominant genera present on skin.72 Many of bacteria in these
genera were found in studies of skin microflora reported by Samaras and Hoptroff in which
they estimated that Cutibacterium, Staphylococcus, and Corynebacterium genera constituted up
to 80% of the entire skin microbiome.73
Grice and coworkers noted that about 4% of the skin microbiome is represented by the
archaea, based on 16S rRNA sequencing.72 Archaea is a domain of single-celled organisms
that lack cell nuclei and are therefore prokaryotic like bacteria. However, most archaea have
not been isolated by traditional microbiological methods and have been detected only by

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505 Evolution and Challenges of Sustainability
These AMPs help protect the skin from colonization and infection by transient
microorganisms and pathogens.
6. Commensal skin microflora may promote immunological quiescence by up-regulating
production of IL-10 (an anti-inflammatory cytokine) by dendritic cells.
Each microorganism in any environment—including the skin—is in a constant, life-
and-death struggle with other organisms in this environment as they compete for the
available nutrients needed for survival and growth. Microorganisms can make free fatty
acids, enzymes, and virulence factors including toxins, bacteriocins, AMPs, and antibiotics
that help them compete and survive, as illustrated by the following examples. C. acnes,
S. epidermidis, S. aureus, and Malassezia spp. secrete lipases that hydrolyze triglycerides in
sebum to produce free fatty acids that lower the pH of the skin surface and make it more
difficult for non-acid-tolerant microorganisms to grow, and stimulate epithelial cells and
neutrophils to express HBD2, which has antimicrobial activity against Gram-negative
bacteria and Candida spp.84-86 Many fatty acids upregulate AMPs and cytokines in sebaceous
glands, and sebaceous-gland-rich sites have higher levels of AMPs (e.g., psoriasin S100A7,
HBD2, and lipocalin than sebum-poor sites.87-90 Most Corynebacterium spp. contain mycolic
acid in the cell envelope. Mycolic acid can promote γδTcell accumulation with release of
IL-23, an inflammatory cytokine. Some strains of C. acnes produce cutimycin, a thiopeptide
antibiotic that limits S. aureus colonization.89,91 Staphylococcus lugdunensis produces lugdunin,
an antimicrobial peptide that induces keratinocytes to produce AMPs (cathelicidin LL-37
and CXCL8). CXCL8 is a neutrophil chemoattractant produced through the TLR-myeloid
differentiation response protein 88 (TLR-Myd88) pathway.92 S. epidermidis produces
bacteriocins, several types of AMPs, and stimulates keratinocytes and Langerhans cells
to produce AMPs to prevent the growth of other microorganisms. S. epidermidis produces
succinic acid (from fermentation of glycerol) which inhibits some strains of C. acnes.87,93-95
S. epidermidis also produces a serine protease, Esp, that is able to inhibit S. aureus biofilm
formation and colonization.96 Biofilm is involved in the pathogenicity and antimicrobial
susceptibility of C. acnes,97and it is likely that Esp produced by S. epidermidis, or proteases
produced by other microorganisms, may help control biofilm formation of C. acnes, which
in turn decreases C. acnes colonization to decrease the severity of acne.
Skin colonization with commensal microorganisms shapes immunity through activation
of cellular pattern recognition receptors, with distinct activation signatures defining skin
physiology.98 Commensal S. epidermidis, induces IL-17A+ CD8+ T cells that home to the
epidermis, enhance innate barrier immunity, and help prevent pathogen attachment and
colonization.99 Commensals also trigger activation of cellular Toll-like receptors (TLRs)
to enhance immunity and facilitate wound repair.100 Keratinocytes express TLRs and
other immunomodulatory proteins, such as nucleotide-binding oligomerization domain-
containing protein 2 (NOD2), that can recognize pathogenic substances, such as pathogen-
associated molecular patterns including bacterial cell wall peptidoglycans, and stimulate an
immune reaction to them.101,102 Immune response pathways are activated in a TLR-specific
process, which causes the release of cytokines, chemokines, and AMPs to attract circulating
immune cells (e.g., neutrophils and Langerhans cells). Keratinocytes constitutively express
certain AMPs, such as HBD1, while other AMPs are induced in response to injury or
infection.103-105 The Firmicutes and Actinobacteria produce lipoteichoic acid (LTA), which
is a major constituent of Gram-positive bacterial cell walls. LTA is a Toll-like receptor 2
(TLR2) ligand that down-regulates skin inflammation, which in turn, supports barrier
function.82,106

506 JOURNAL OF COSMETIC SCIENCE
Up-regulation of HBD2 is believed to play an important role in cutaneous immune
defense, and expression of this AMP appears to be localized to the upper Malpighian layer
of the epidermis and stratum corneum.107,108 S. epidermidis is a good inducer of HBD2 and
is tolerant to it, which enables S. epidermis to colonize skin. Streptococcus pyogenes is known to
be a poor/variable inducer of HBD2, which means that S. pyogenes can reside on skin and
mucous membranes without stimulating skin cells to release substantial amounts of HBD2.
However, S. pyogenes is reported to be significantly more sensitive to killing by HBD2 than
S. epidermidis.107 Consequently, the growth of S. epidermidis on skin up-regulates HBD2
which helps limit S. pyogenes colonization of skin.
Phenol-soluble modulins (PSMs) are AMPs which are small peptides with an amphipathic
α-helical structure and strong surfactant-like properties. PSMs are produced by most
staphylococci and can induce the production of proinflammatory cytokines, recruit, activate,
and lyse neutrophils to help staphylococci evade destruction by these neutrophils. For
example, PSMs facilitate the detachment and dissemination of staphylococcal biofilms.66
PSMα elicits a keratinocyte Myd88 signaling response that drives an IL-17-mediated skin
inflammatory response to S. aureus colonization of skin, and PSMε enhances production
of IL-8—neutrophil chemotactic factor—a proinflammatory mediator that recruits and
activates neutrophils to kill competing microorganisms.109-111
The normally functioning skin microbiome assists the body’s immune barrier however,
dysbiosis (i.e., disruption of the microbiome with changes composition and/or metabolic
activities) may lead to inflammatory skin disorders.112 For example, C. acnes is involved
directly or indirectly in the pathogenesis of acne vulgaris. The free fatty acids and porphyrins
produced by C. acnes cause skin inflammation.68,82,113 S. epidermidis, and to a lesser extent,
S. aureus normally colonize human skin without any negative health effects, but these
bacteria may worsen atopic dermatitis (AD) in some patients. It is not known whether over-
colonization by staphylococci in AD is the cause or the consequence of inflammation.74,114,115
Malassezia yeasts are residents of healthy skin, but Malassezia spp. may cause dandruff
and seborrheic dermatitis in susceptible individuals.116 The microbiome of patients with
psoriasis has higher numbers of Malassezia spp. and Streptococcus spp. and lower numbers of
Cutibacterium spp. compared to healthy individuals.117
The crosstalk between commensals and the skin may involve microbial metabolite-mediated
interactions with cells in the immune system. Mucosal-associated invariant T (MAIT) cells
constitute a subset of αβT lymphocytes characterized by a semi-invariant T cell receptor
alpha (TCRα) chain. MAIT cells have innate, T cell effector-like qualities.118,119 Microbial
exposure that occurs during early life imprints MAIT cell abundance for life. MAIT cells
represent a dominant type-17 effector subset in the skin, they are involved with immune
surveillance, and they defend against microbial infection. MAIT cells require vitamin B2
metabolites that are only produced by bacteria and fungi.86 The major histocompatibility
complex (MHC) class I-like protein, MR1, is responsible for presenting bacterially-produced
riboflavin (vitamin B2) and folic acid (vitamin B9) metabolites to MAIT cells.118,120-122 After
the presentation of foreign antigen by MR1, MAIT cells produce the proinflammatory
cytokines, interferon-γ (IFN-γ) and tumor necrosis factor, and they are cytolytic.118
Most species within the dominant bacterial taxa Corynebacteriaceae, Propionibacteriaceae,
and Staphylococcaceae in the skin microbiome encode Vitamin B2 biosynthesis therefore,
MAIT cell specific immunity through recognition of riboflavin biosynthesis intermediates
produced by the skin microflora is an example of crosstalk between commensals and the
skin that plays an important role in skin barrier immunology.123-127

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