Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants

ABSTRACT The purpose of this study was to evaluate the composition and richness of bacterial communities associated with low-birthweight (LBW) infants in relation to host body site, individual, and age. Bacterial 16S rRNA genes from saliva samples, skin swabs, and stool samples collected on postnata...

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Autores principales: Elizabeth K. Costello, Erica M. Carlisle, Elisabeth M. Bik, Michael J. Morowitz, David A. Relman
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Publicado: American Society for Microbiology 2013
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spelling oai:doaj.org-article:3107c27332464f88b3ea0f5d9b860ebc2021-11-15T15:42:32ZMicrobiome Assembly across Multiple Body Sites in Low-Birthweight Infants10.1128/mBio.00782-132150-7511https://doaj.org/article/3107c27332464f88b3ea0f5d9b860ebc2013-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00782-13https://doaj.org/toc/2150-7511ABSTRACT The purpose of this study was to evaluate the composition and richness of bacterial communities associated with low-birthweight (LBW) infants in relation to host body site, individual, and age. Bacterial 16S rRNA genes from saliva samples, skin swabs, and stool samples collected on postnatal days 8, 10, 12, 15, 18, and 21 from six LBW (five premature) infants were amplified, pyrosequenced, and analyzed within a comparative framework that included analogous data from normal-birthweight (NBW) infants and healthy adults. We found that body site was the primary determinant of bacterial community composition in the LBW infants. However, site specificity depended on postnatal age: saliva and stool compositions diverged over time but were not significantly different until the babies were 15 days old. This divergence was primarily driven by progressive temporal turnover in the distal gut, which proceeded at a rate similar to that of age-matched NBW infants. Neonatal skin was the most adult-like in microbiota composition, while saliva and stool remained the least so. Compositional variation among infants was marked and depended on body site and age. Only the smallest, most premature infant received antibiotics during the study period; this heralded a coexpansion of Pseudomonas aeruginosa and a novel Mycoplasma sp. in the oral cavity of this vaginally delivered, intubated patient. We conclude that concurrent molecular surveillance of multiple body sites in LBW neonates reveals a delayed compositional differentiation of the oral cavity and distal gut microbiota and, in the case of one infant, an abundant, uncultivated oral Mycoplasma sp., recently detected in human vaginal samples. IMPORTANCE Complications of premature birth are the most common cause of neonatal mortality. Colonization by the indigenous microbiota, which begins at delivery, may predispose some high-risk newborns to invasive infection or necrotizing enterocolitis (NEC), and protect others, yet neonatal microbiome dynamics are poorly understood. Here, we present the first cultivation-independent time series tracking microbiota assembly across multiple body sites in a synchronous cohort of hospitalized low-birthweight (LBW) neonates. We take advantage of archived samples and publically available sequence data and compare our LBW infant findings to those from normal-birthweight (NBW) infants and healthy adults. Our results suggest potential windows of opportunity for the dispersal of microbes within and between hosts and support recent findings of substantial baseline spatiotemporal variation in microbiota composition among high-risk newborns.Elizabeth K. CostelloErica M. CarlisleElisabeth M. BikMichael J. MorowitzDavid A. RelmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 6 (2013)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Elizabeth K. Costello
Erica M. Carlisle
Elisabeth M. Bik
Michael J. Morowitz
David A. Relman
Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants
description ABSTRACT The purpose of this study was to evaluate the composition and richness of bacterial communities associated with low-birthweight (LBW) infants in relation to host body site, individual, and age. Bacterial 16S rRNA genes from saliva samples, skin swabs, and stool samples collected on postnatal days 8, 10, 12, 15, 18, and 21 from six LBW (five premature) infants were amplified, pyrosequenced, and analyzed within a comparative framework that included analogous data from normal-birthweight (NBW) infants and healthy adults. We found that body site was the primary determinant of bacterial community composition in the LBW infants. However, site specificity depended on postnatal age: saliva and stool compositions diverged over time but were not significantly different until the babies were 15 days old. This divergence was primarily driven by progressive temporal turnover in the distal gut, which proceeded at a rate similar to that of age-matched NBW infants. Neonatal skin was the most adult-like in microbiota composition, while saliva and stool remained the least so. Compositional variation among infants was marked and depended on body site and age. Only the smallest, most premature infant received antibiotics during the study period; this heralded a coexpansion of Pseudomonas aeruginosa and a novel Mycoplasma sp. in the oral cavity of this vaginally delivered, intubated patient. We conclude that concurrent molecular surveillance of multiple body sites in LBW neonates reveals a delayed compositional differentiation of the oral cavity and distal gut microbiota and, in the case of one infant, an abundant, uncultivated oral Mycoplasma sp., recently detected in human vaginal samples. IMPORTANCE Complications of premature birth are the most common cause of neonatal mortality. Colonization by the indigenous microbiota, which begins at delivery, may predispose some high-risk newborns to invasive infection or necrotizing enterocolitis (NEC), and protect others, yet neonatal microbiome dynamics are poorly understood. Here, we present the first cultivation-independent time series tracking microbiota assembly across multiple body sites in a synchronous cohort of hospitalized low-birthweight (LBW) neonates. We take advantage of archived samples and publically available sequence data and compare our LBW infant findings to those from normal-birthweight (NBW) infants and healthy adults. Our results suggest potential windows of opportunity for the dispersal of microbes within and between hosts and support recent findings of substantial baseline spatiotemporal variation in microbiota composition among high-risk newborns.
format article
author Elizabeth K. Costello
Erica M. Carlisle
Elisabeth M. Bik
Michael J. Morowitz
David A. Relman
author_facet Elizabeth K. Costello
Erica M. Carlisle
Elisabeth M. Bik
Michael J. Morowitz
David A. Relman
author_sort Elizabeth K. Costello
title Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants
title_short Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants
title_full Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants
title_fullStr Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants
title_full_unstemmed Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants
title_sort microbiome assembly across multiple body sites in low-birthweight infants
publisher American Society for Microbiology
publishDate 2013
url https://doaj.org/article/3107c27332464f88b3ea0f5d9b860ebc
work_keys_str_mv AT elizabethkcostello microbiomeassemblyacrossmultiplebodysitesinlowbirthweightinfants
AT ericamcarlisle microbiomeassemblyacrossmultiplebodysitesinlowbirthweightinfants
AT elisabethmbik microbiomeassemblyacrossmultiplebodysitesinlowbirthweightinfants
AT michaeljmorowitz microbiomeassemblyacrossmultiplebodysitesinlowbirthweightinfants
AT davidarelman microbiomeassemblyacrossmultiplebodysitesinlowbirthweightinfants
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