Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates
- Matthew R. Olm1,
- Christopher T. Brown1,
- Brandon Brooks1,
- Brian Firek2,
- Robyn Baker3,
- David Burstein4,
- Karina Soenjoyo1,
- Brian C. Thomas4,
- Michael Morowitz2 and
- Jillian F. Banfield4,5,6
- 1Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA;
- 2Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213, USA;
- 3Division of Newborn Medicine, Children's Hospital of Pittsburgh and Magee-Womens Hospital of UPMC, Pittsburgh, Pennsylvania 15213, USA;
- 4Department of Earth and Planetary Science, University of California, Berkeley, California 94709, USA;
- 5Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720, USA;
- 6Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA
- Corresponding author: Jbanfield{at}berkeley.edu
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 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.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.213256.116.
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Freely available online through the Genome Research Open Access option.
- Received July 22, 2016.
- Accepted January 9, 2017.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
