Strain-resolved analysis of hospital rooms and infants reveals overlap between the human and room microbiome

Abstract

Preterm infants exhibit different microbiome colonization patterns relative to full-term infants, and it is speculated that the hospital room environment may contribute to infant microbiome development. Here, we present a genome-resolved metagenomic study of microbial genotypes from the gastrointestinal tracts of infants and from the neonatal intensive care unit (NICU) room environment. Some strains detected in hospitalized infants also occur in sinks and on surfaces, and belong to species such as Staphylococcus epidermidis, Enterococcus faecalis, Pseudomonas aeruginosa, and Klebsiella pneumoniae, which are frequently implicated in nosocomial infection and preterm infant gut colonization. Of the 15 K. pneumoniae strains detected in the study, four were detected in both infant gut and room samples. Time series experiments showed that nearly all strains associated with infant gut colonization can be detected in the room after, and often before, detection in the gut. Thus, we conclude that a component of premature infant gut colonization is the cycle of microbial exchange between the room and the occupant.

Fig. 1

Subspecies found in the infant gut across several cohorts and years are also present in rooms. Fecal (columns 1, 2, 3, and 5) and room (column 4) samples from defined sampling time periods (the 2011, 2012, 2013, and 2014 cohorts) are arrayed on the x axis. Dots indicate the percent of infants, or rooms for column 4, in each cohort that contain a given subspecies (the top three highest percentages are labeled for clarity). The y axis labels indicate a representative genotype from clusters of genotypes that share > 99% gANI. The first digit in the name indicates the species and the second indicates the specific subspecies. See Supplementary Data 3–11 for further genome-clustering results. Only genomes that were found across different cohorts or in both an infant and a room are displayed. Triangles indicate organisms classified as persistent taxa (“persisters”) because they appear in the room and in infant cohorts more than 1 year apart

Fig. 2

Gut strains are consistently detected in the room. Room reads from all room samples were mapped to each infant’s dereplicated fecal genome set. Symbols indicate fecal genomes present in the room with at least 99.999% ANI. Circles represent cases where a fecal genome was detected in a separate room from which the infant was housed, and stars represent matched infant/room pairs. Wipe, swab, and sink metagenomes are filled in red, green, and blue, respectively

Fig. 3

Strains associated with infant 5 also occurred in this infant’s room and in rooms of previously and subsequently hospitalized infants. Detection in swabs from frequently touched surfaces (yellow), sinks (blue), and wipes from other surfaces (green). The results are shown in chronological order from left to right. Genomes recovered from specific days of life from infant 5’s samples are indicated by black dots. Room detection of strains is indicated by a colored bar because room samples from one environment type were pooled, either by infant or for three time periods for infant 5