Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles

ABSTRACT During the first weeks of life, microbial colonization of the gut impacts human immune system maturation and other developmental processes. In premature infants, aberrant colonization has been implicated in the onset of necrotizing enterocolitis (NEC), a life-threatening intestinal disease....

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Autores principales: Christopher T. Brown, Weili Xiong, Matthew R. Olm, Brian C. Thomas, Robyn Baker, Brian Firek, Michael J. Morowitz, Robert L. Hettich, Jillian F. Banfield
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:45a3dc5d52b944faaf02853bedb6f12a2021-11-15T15:53:26ZHospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles10.1128/mBio.00441-182150-7511https://doaj.org/article/45a3dc5d52b944faaf02853bedb6f12a2018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00441-18https://doaj.org/toc/2150-7511ABSTRACT During the first weeks of life, microbial colonization of the gut impacts human immune system maturation and other developmental processes. In premature infants, aberrant colonization has been implicated in the onset of necrotizing enterocolitis (NEC), a life-threatening intestinal disease. To study the premature infant gut colonization process, genome-resolved metagenomics was conducted on 343 fecal samples collected during the first 3 months of life from 35 premature infants housed in a neonatal intensive care unit, 14 of whom developed NEC, and metaproteomic measurements were made on 87 samples. Microbial community composition and proteomic profiles remained relatively stable on the time scale of a week, but the proteome was more variable. Although genetically similar organisms colonized many infants, most infants were colonized by distinct strains with metabolic profiles that could be distinguished using metaproteomics. Microbiome composition correlated with infant, antibiotics administration, and NEC diagnosis. Communities were found to cluster into seven primary types, and community type switched within infants, sometimes multiple times. Interestingly, some communities sampled from the same infant at subsequent time points clustered with those of other infants. In some cases, switches preceded onset of NEC; however, no species or community type could account for NEC across the majority of infants. In addition to a correlation of protein abundances with organism replication rates, we found that organism proteomes correlated with overall community composition. Thus, this genome-resolved proteomics study demonstrated that the contributions of individual organisms to microbiome development depend on microbial community context. IMPORTANCE Humans are colonized by microbes at birth, a process that is important to health and development. However, much remains to be known about the fine-scale microbial dynamics that occur during the colonization period. We conducted a genome-resolved study of microbial community composition, replication rates, and proteomes during the first 3 months of life of both healthy and sick premature infants. Infants were found to be colonized by similar microbes, but each underwent a distinct colonization trajectory. Interestingly, related microbes colonizing different infants were found to have distinct proteomes, indicating that microbiome function is not only driven by which organisms are present, but also largely depends on microbial responses to the unique set of physiological conditions in the infant gut.Christopher T. BrownWeili XiongMatthew R. OlmBrian C. ThomasRobyn BakerBrian FirekMichael J. MorowitzRobert L. HettichJillian F. BanfieldAmerican Society for Microbiologyarticlehuman microbiomemetaproteomicsmicrobial colonizationmicrobial genomicsnecrotizing enterocolitisneonatesMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution DOAJ
collection DOAJ
language EN
topic human microbiome
metaproteomics
microbial colonization
microbial genomics
necrotizing enterocolitis
neonates
Microbiology
QR1-502
spellingShingle human microbiome
metaproteomics
microbial colonization
microbial genomics
necrotizing enterocolitis
neonates
Microbiology
QR1-502
Christopher T. Brown
Weili Xiong
Matthew R. Olm
Brian C. Thomas
Robyn Baker
Brian Firek
Michael J. Morowitz
Robert L. Hettich
Jillian F. Banfield
Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles
description ABSTRACT During the first weeks of life, microbial colonization of the gut impacts human immune system maturation and other developmental processes. In premature infants, aberrant colonization has been implicated in the onset of necrotizing enterocolitis (NEC), a life-threatening intestinal disease. To study the premature infant gut colonization process, genome-resolved metagenomics was conducted on 343 fecal samples collected during the first 3 months of life from 35 premature infants housed in a neonatal intensive care unit, 14 of whom developed NEC, and metaproteomic measurements were made on 87 samples. Microbial community composition and proteomic profiles remained relatively stable on the time scale of a week, but the proteome was more variable. Although genetically similar organisms colonized many infants, most infants were colonized by distinct strains with metabolic profiles that could be distinguished using metaproteomics. Microbiome composition correlated with infant, antibiotics administration, and NEC diagnosis. Communities were found to cluster into seven primary types, and community type switched within infants, sometimes multiple times. Interestingly, some communities sampled from the same infant at subsequent time points clustered with those of other infants. In some cases, switches preceded onset of NEC; however, no species or community type could account for NEC across the majority of infants. In addition to a correlation of protein abundances with organism replication rates, we found that organism proteomes correlated with overall community composition. Thus, this genome-resolved proteomics study demonstrated that the contributions of individual organisms to microbiome development depend on microbial community context. IMPORTANCE Humans are colonized by microbes at birth, a process that is important to health and development. However, much remains to be known about the fine-scale microbial dynamics that occur during the colonization period. We conducted a genome-resolved study of microbial community composition, replication rates, and proteomes during the first 3 months of life of both healthy and sick premature infants. Infants were found to be colonized by similar microbes, but each underwent a distinct colonization trajectory. Interestingly, related microbes colonizing different infants were found to have distinct proteomes, indicating that microbiome function is not only driven by which organisms are present, but also largely depends on microbial responses to the unique set of physiological conditions in the infant gut.
format article
author Christopher T. Brown
Weili Xiong
Matthew R. Olm
Brian C. Thomas
Robyn Baker
Brian Firek
Michael J. Morowitz
Robert L. Hettich
Jillian F. Banfield
author_facet Christopher T. Brown
Weili Xiong
Matthew R. Olm
Brian C. Thomas
Robyn Baker
Brian Firek
Michael J. Morowitz
Robert L. Hettich
Jillian F. Banfield
author_sort Christopher T. Brown
title Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles
title_short Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles
title_full Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles
title_fullStr Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles
title_full_unstemmed Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles
title_sort hospitalized premature infants are colonized by related bacterial strains with distinct proteomic profiles
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/45a3dc5d52b944faaf02853bedb6f12a
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