title: 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-associatedCitrobacter koserigenomes 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.
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA.
authors.forename: Matthew R
authors.initials: MR
authors.lastname: Olm
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA.
authors.forename: Christopher T
authors.initials: CT
authors.lastname: Brown
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA.
authors.forename: Brandon
authors.initials: B
authors.lastname: Brooks
authors.affiliation: Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213, USA.
authors.forename: Brian
authors.initials: B
authors.lastname: Firek
authors.affiliation: Division of Newborn Medicine, Children's Hospital of Pittsburgh and Magee-Womens Hospital of UPMC, Pittsburgh, Pennsylvania 15213, USA.
authors.forename: Robyn
authors.initials: R
authors.lastname: Baker
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley, California 94709, USA.
authors.forename: David
authors.initials: D
authors.lastname: Burstein
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA.
authors.forename: Karina
authors.initials: K
authors.lastname: Soenjoyo
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley, California 94709, USA.
authors.forename: Brian C
authors.initials: BC
authors.lastname: Thomas
authors.affiliation: Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213, USA.
authors.forename: Michael
authors.initials: M
authors.lastname: Morowitz
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley, California 94709, USA.|Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720, USA.|Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Jillian F
authors.initials: JF
authors.lastname: Banfield
mesh_terms: D041041:Citrobacter koseri / Q000235:genetics* / Q000254:growth & development / Q000302:isolation & purification / Q000472:pathogenicity; D000069196:Gastrointestinal Microbiome; D016680:Genome, Bacterial; D006801:Humans; D052577:Infant, Extremely Low Birth Weight; D007231:Infant, Newborn; D007234:Infant, Premature; D009055:Mouth / Q000382:microbiology*; D011110:Polymorphism, Genetic; D012867:Skin / Q000382:microbiology*