Infant Mode of Delivery Shapes the Skin Mycobiome of Prepubescent Children

Abstract

ABSTRACT Characterizing the skin mycobiome is necessary to define its association with the host immune system, particularly in children. In this study, we describe the skin mycobiome on the face, ventral forearm, and calf of 72 prepubescent children (aged 1 to 10 years) and their mothers, based on internal transcribed spacer (ITS) amplicon sequencing. The age and delivery mode at birth are the most influential factors shaping the skin mycobiome. Compared with that of the vaginally born children, the skin mycobiome of caesarean-born children is assembled by predominantly deterministic niche-based processes and exhibits a more fragile microbial network at all three sampling sites. Moreover, vaginal delivery leads to clearer intra- and interindividual specialization of fungal structures with increasing age; this phenomenon is not observed in caesarean-born children. The maternal correlation with children also differs based on the mode of delivery; specifically, the mycobiomes of vaginally born children at younger ages are more strongly correlated with vagina-associated fungal genera (Candida and Rhodotorula), whereas those of caesarean-delivered children at elder age include more skin-associated and airborne fungal genera (Malassezia and Alternaria). Based on this ecological framework, our results suggest that the delivery mode is significantly associated with maturation of the skin fungal community in children. IMPORTANCE Human skin is permanently colonized by microbes starting at birth. The hygiene hypothesis suggests that a lack of early-life immune imprinting weakens the body’s resilience against atopic disorders later in life. To better understand fungal colonization following early-life periods affected by interruption, we studied the skin mycobiomes of 73 children and their mothers. Our results suggest a differentiation of the skin mycobiomes between caesarean-born and vaginally born children. Caesarean-born children exhibit a mycobiome structure with more fitted deterministic niche-based processes, a fragile network, and an unchanged microbial dissimilarity over time. In vaginally born children, this dissimilarity increases with age. The results indicate that initial microbial colonization has a long-term impact on a child’s skin mycobiome. We believe that these findings will inspire further investigations of the “hygiene hypothesis” in the human microbiome, especially in providing novel insights into influences on the development of the early-life microbiome.

Keywords

• skin mycobiome
• fungi
• prepubescent children
• delivery mode