Skin dysbiosis in the microbiome in atopic dermatitis is site-specific and involves bacteria, fungus and virus

Abstract

Background Microbial dysbiosis with increased Staphylococcus aureus (S. aureus) colonization on the skin is a hallmark of atopic dermatitis (AD), however most microbiome studies focus on bacteria in the flexures and the microbial composition at other body sites have not been studied systematically. Objectives The aim of the study is to characterize the skin microbiome, including bacteria, fungi and virus, at different body sites in relation to AD, lesional state, and S. aureus colonization, and to test whether the nares could be a reservoir for S. aureus strain colonization. Methods Using shotgun metagenomics we characterized microbial compositions from 14 well defined skin sites from 10 patients with AD and 5 healthy controls. Results We found clear differences in microbial composition between AD and controls at multiple skin sites, most pronounced on the flexures and neck. The flexures exhibited lower alpha-diversity and were colonized by S. aureus, accompanied by S. epidermidis in lesions. Malassezia species were absent on the neck in AD. Virus mostly constituted Propionibacterium and Staphylococcusphages, with increased abundance of Propionibacterium phages PHL041 and PHL092 and Staphylococcus epidermidis phages CNPH82 and PH15 in AD. In lesional samples, both the genus Staphylococcus and Staphylococcus phages were more abundant. S. aureus abundance was higher across all skin sites except from the feet. In samples where S. aureus was highly abundant, lower abundances of S. hominis and Cutibacterium acnes were observed. M. osloensis and M. luteus were more abundant in AD. By single nucleotide variant analysis of S. aureus we found strains to be subject specific. On skin sites some S. aureus strains were similar and some dissimilar to the ones in the nares. Conclusions Our data indicate a global and site-specific dysbiosis in AD, involving both bacteria, fungus and virus. When defining targeted treatment clinicians should both consider the individual and skin site and future research into potential crosstalk between microbiota in AD yields high potential.

The Human Mycobiome: Colonization, Composition and the Role in Health and Disease

“…Inter-kingdom and inter-species microbial interactions can worsen the disease or change relationships from opportunistic to pathogenic [ 131 , 134 , 135 ]. Fungal dysbiosis could be associated with numerous skin diseases often present in a site-specific manner, including atopic dermatitis in the arm and leg creases [ 136 ], psoriasis on the elbows and knees [ 132 ], pityriasis versicolor [ 137 ], seborrheic dermatitis [ 138 ], etc. The prevalence of fungal infections on the skin, hair and nails varies from 20 to 25% worldwide [ 139 ].…”

“…The dysbiosis of the major commensal skin fungi, Malassezia sp., is associated with numerous skin disorders [ 123 , 137 ]. The species Malassezia globosa colonized antecubital flexures at the neck of healthy individuals but was absent in patients with atopic dermatitis [ 136 ]. Similarly, a higher relative abundance of M. globosa in controls was reported by another study [ 140 ].…”

“…Similarly, a higher relative abundance of M. globosa in controls was reported by another study [ 140 ]. This growth restriction could be a consequence of dry skin and insufficient growth conditions usually provided by the bacterium Cutibacterium acnes , which were decreased in patients with atopic dermatitis as well [ 136 ]. Furthermore, Malassezia restricta and Malassezia sympodialis were significantly associated with psoriasis at the back and elbow body sites as shown by LEfSe analysis [ 135 ].…”

Clinical features and tactics of therapy of comorbid dermatoses

“…В этиопатогенезе микробной экземы аллергический компонент считается вторичным по отношению к инфекционному [6,7]. Кожные покровы вокруг первично инфицированного очага сенсибилизируются антигенными структурами и продуктами жизнедеятельности обитаю щих там микроорганизмов [8][9][10]. Для нормобиоты патологических очагов характерны представители грамположительной кокковой флоры (Staphylococcus aureus, Staphylococcus haemolyticus, Staphylococcus epidermidis, Staphylococcus saprophytes, Streptococcus pyogenes), а в отдельных случаях -грибы рода Candida и Trichophyton (при микотической экземе) [11][12][13][14][15][16][17].…”

In vitro and in vivo antimicrobial activity of an active plant-based quadrocomplex for skin hygiene

“…It also alters the proportions of organisms compared to the healthy skin microbiome and may trigger the pathogenic potential of the commensals (Skowron et al, 2021). Nevertheless, the switch can occur when the normal skin flora is disrupted: S. epidermidis, which usually colonizes human skin without any negative health effects, can cause serious illness, including atopic dermatitis and, as proposed, inflammation (Bjerre et al, 2021;Cau et al, 2021;Otto, 2009).…”