Abstract
BackgroundPostnatal development of early life microbiota influences immunity, metabolism, neurodevelopment, and infant health. Microbiome development occurs at multiple body sites, with distinct community compositions and functions. Associations between microbiota at multiple sites represent an unexplored influence on the infant microbiome. Here, we examined co-occurrence patterns of gut and respiratory microbiota in pre- and full-term infants over the first year of life, a period critical to neonatal development.ResultsGut and respiratory microbiota collected as longitudinal rectal, throat, and nasal samples from 38 pre-term and 44 full-term infants were first clustered into community state types (CSTs) on the basis of their compositional profiles. Multiple methods were used to relate the occurrence of CSTs to temporal microbiota development and measures of infant maturity, including gestational age (GA) at birth, week of life (WOL), and post-menstrual age (PMA). Manifestation of CSTs followed one of three patterns with respect to infant maturity: (1) chronological, with CST occurrence frequency solely a function of post-natal age (WOL), (2) idiosyncratic to maturity at birth, with the interval of CST occurrence dependent on infant post-natal age but the frequency of occurrence dependent on GA at birth, and (3) convergent, in which CSTs appear first in infants of greater maturity at birth, with occurrence frequency in pre-terms converging after a post-natal interval proportional to pre-maturity. The composition of CSTs was highly dissimilar between different body sites, but the CST of any one body site was highly predictive of the CSTs at other body sites. There were significant associations between the abundance of individual taxa at each body site and the CSTs of the other body sites, which persisted after stringent control for the non-linear effects of infant maturity. Canonical correlations exist between the microbiota composition at each pair of body sites, with the strongest correlations between proximal locations.ConclusionThese findings suggest that early microbiota is shaped by neonatal innate and adaptive developmental responses. Temporal progression of CST occurrence is influenced by infant maturity at birth and post-natal age. Significant associations of microbiota across body sites reveal distal connections and coordinated development of the infant microbial ecosystem.
Highlights
Postnatal development of early life microbiota influences immunity, metabolism, neurodevelopment, and infant health
Our results suggest that similar to the longitudinal progression of community state type (CST), specific functional pathways emerge in the initial early life CSTs, with expansion and diversification of microbial communities in later CSTs occurring as a result of contact with environmental sources and adaptation to changes in energy substrates
Correlations between community state type and post-menstrual age (PMA) in pre- and full-term infants In order to elucidate the relationship between the temporal components of host maturity and the progression of community types at each body site, we further examined the associations between CSTs and maturity (GA) at birth and age, which can be measured developmentally as PMA or postnatally with week of life (WOL)
Summary
Postnatal development of early life microbiota influences immunity, metabolism, neurodevelopment, and infant health. Interactions that occur between members of the microbial community and between microbes and their human host are responsible for features of postnatal development that influence future health [2,3,4,5]. Little has been reported about longitudinal microbiota development or compositional differentiation across multiple body sites during this period. This is true for high-risk pre-term infants, who because of immature mucosal and skin barriers, as well as underdeveloped immunity and suboptimal nutrition, are at increased risk for invasive infection and dysregulated inflammation of critical systems, namely the respiratory and gastrointestinal tracts. Serious perinatal complications in these pre-term infants result in prolonged hospitalization, treatment with antibiotics, and delays in enteral feeding that influence interactions with microbes and inhibit microbial colonization characteristic of full-term infants [11]
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