Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates

Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon; Firek, Brian; Baker, Robyn; Burstein, David; Soenjoyo, Karina; Thomas, Brian C.; Morowitz, Michael; Banfield, Jillian F.

doi:10.1101/gr.213256.116

Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates

Journal Article · Mon Jan 09 23:00:00 EST 2017 · Genome Research

DOI:https://doi.org/10.1101/gr.213256.116· OSTI ID:1625635

Olm, Matthew R. ^[1]; Brown, Christopher T. ^[2]; Brooks, Brandon ^[2]; Firek, Brian ^[3]; Baker, Robyn ^[4]; Burstein, David ^[5]; Soenjoyo, Karina ^[2]; Thomas, Brian C. ^[6]; Morowitz, Michael ^[7]; Banfield, Jillian F. ^[8]

Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; DOE/OSTI
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

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625635

Journal Information:: Genome Research, Journal Name: Genome Research Journal Issue: 4 Vol. 27; ISSN 1088-9051

Publisher:: Cold Spring Harbor Laboratory PressCopyright Statement

Country of Publication:: United States

Language:: English

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Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance Keren, Ray; Lawrence, Jennifer E.; Zhuang, Weiqin Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-0786-3	journal	January 2020
Evolutionary dynamics of bacteria in the gut microbiome within and across hosts Garud, Nandita R.; Good, Benjamin H.; Hallatschek, Oskar PLOS Biology, Vol. 17, Issue 1 https://doi.org/10.1371/journal.pbio.3000102	journal	January 2019
Bacterial variability in the mammalian gut captured by a single-cell synthetic oscillator. Riglar, David T.; Richmond, David L.; Potvin-Trottier, Laurent Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.46830	text	January 2019
Bacterial variability in the mammalian gut captured by a single-cell synthetic oscillator Riglar, David T.; Richmond, David L.; Potvin-Trottier, Laurent Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.68779	text	January 2019
Growth Rate of Escherichia coli During Human Urinary Tract Infection: Implications for Antibiotic Effect No authors listed Antibiotics, Vol. 8, Issue 3 https://doi.org/10.3390/antibiotics8030092	journal	July 2019