Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates
Abstract
The initial microbiome impacts the health and future development of premature infants. Methodological limitations have led to gaps in our understanding of the habitat range and subpopulation complexity of founding strains, as well as how different body sites support microbial growth. Here, we used metagenomics to reconstruct genomes of strains that colonized the skin, mouth, and gut of two hospitalized premature infants during the first month of life. Seven bacterial populations, considered to be identical given whole-genome average nucleotide identity of >99.9%, colonized multiple body sites, yet none were shared between infants. Gut-associated Citrobacter koseri genomes harbored 47 polymorphic sites that we used to define 10 subpopulations, one of which appeared in the gut after 1 wk but did not spread to other body sites. Differential genome coverage was used to measure bacterial population replication rates in situ. In all cases where the same bacterial population was detected in multiple body sites, replication rates were faster in mouth and skin compared to the gut. The ability of identical strains to colonize multiple body sites underscores the habit flexibility of initial colonists, whereas differences in microbial replication rates between body sites suggest differences in host control and/or resource availability. Population genomicmore »
- Authors:
-
- Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
- Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
- Univ. of Pittsburgh School of Medicine Pittsburgh, PA (United States). Dept. of Surgery
- Children’s Hospital of Pittsburgh and Magee-Womens Hospital of UPMC, Pittsburgh, PA (United States). Division of Newborn Medicine
- Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
- Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
- Univ. of Pittsburgh School of Medicine Pittsburgh, PA (United States). Dept. of Surgery
- Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy, and Management; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1625635
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genome Research
- Additional Journal Information:
- Journal Volume: 27; Journal Issue: 4; Journal ID: ISSN 1088-9051
- Publisher:
- Cold Spring Harbor Laboratory Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology; Biotechnology & Applied Microbiology; Genetics & Heredity
Citation Formats
Olm, Matthew R., Brown, Christopher T., Brooks, Brandon, Firek, Brian, Baker, Robyn, Burstein, David, Soenjoyo, Karina, Thomas, Brian C., Morowitz, Michael, and Banfield, Jillian F. Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates. United States: N. p., 2017.
Web. doi:10.1101/gr.213256.116.
Olm, Matthew R., Brown, Christopher T., Brooks, Brandon, Firek, Brian, Baker, Robyn, Burstein, David, Soenjoyo, Karina, Thomas, Brian C., Morowitz, Michael, & Banfield, Jillian F. Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates. United States. https://doi.org/10.1101/gr.213256.116
Olm, Matthew R., Brown, Christopher T., Brooks, Brandon, Firek, Brian, Baker, Robyn, Burstein, David, Soenjoyo, Karina, Thomas, Brian C., Morowitz, Michael, and Banfield, Jillian F. Tue .
"Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates". United States. https://doi.org/10.1101/gr.213256.116. https://www.osti.gov/servlets/purl/1625635.
@article{osti_1625635,
title = {Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates},
author = {Olm, Matthew R. and Brown, Christopher T. and Brooks, Brandon and Firek, Brian and Baker, Robyn and Burstein, David and Soenjoyo, Karina and Thomas, Brian C. and Morowitz, Michael and Banfield, Jillian F.},
abstractNote = {The initial microbiome impacts the health and future development of premature infants. Methodological limitations have led to gaps in our understanding of the habitat range and subpopulation complexity of founding strains, as well as how different body sites support microbial growth. Here, we used metagenomics to reconstruct genomes of strains that colonized the skin, mouth, and gut of two hospitalized premature infants during the first month of life. Seven bacterial populations, considered to be identical given whole-genome average nucleotide identity of >99.9%, colonized multiple body sites, yet none were shared between infants. Gut-associated Citrobacter koseri genomes harbored 47 polymorphic sites that we used to define 10 subpopulations, one of which appeared in the gut after 1 wk but did not spread to other body sites. Differential genome coverage was used to measure bacterial population replication rates in situ. In all cases where the same bacterial population was detected in multiple body sites, replication rates were faster in mouth and skin compared to the gut. The ability of identical strains to colonize multiple body sites underscores the habit flexibility of initial colonists, whereas differences in microbial replication rates between body sites suggest differences in host control and/or resource availability. Population genomic analyses revealed microdiversity within bacterial populations, implying initial inoculation by multiple individual cells with distinct genotypes. Overall, however, the overlap of strains across body sites implies that the premature infant microbiome can exhibit very low microbial diversity.},
doi = {10.1101/gr.213256.116},
journal = {Genome Research},
number = 4,
volume = 27,
place = {United States},
year = {Tue Jan 10 00:00:00 EST 2017},
month = {Tue Jan 10 00:00:00 EST 2017}
}
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Figure 1: Compositional profile of microbial communities colonizing the mouth, skin, and gut of two premature infants. Each colored box represents the percentage of nonhuman reads mapping to an assembled genome, and the stacked boxes for each sample show the fraction of the reads in that data set accounted formore »
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