Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms

Olm, Matthew R.; West, Patrick T.; Brooks, Brandon; Firek, Brian A.; Baker, Robyn; Morowitz, Michael J.; Banfield, Jillian F.

doi:10.1186/s40168-019-0638-1

Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms

Journal Article · Fri Feb 15 00:00:00 EST 2019 · Microbiome

DOI:https://doi.org/10.1186/s40168-019-0638-1· OSTI ID:1627050

Olm, Matthew R. ^[1]; West, Patrick T. ^[2]; Brooks, Brandon ^[2]; Firek, Brian A. ^[3]; Baker, Robyn ^[4]; Morowitz, Michael J. ^[3]; Banfield, Jillian F. ^[5]

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, PA (United States). School of Medicine. Dept. of Surgery
Univ. of Pittsburgh, PA (United States). School of Medicine. Magee-Womens Hospital. 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 Environmental Science, Policy, and Management; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division; Chan Zuckerberg Biohub, San Francisco, CA (United States)

Background: Fungal infections are a significant cause of mortality and morbidity in hospitalized preterm infants, yet little is known about eukaryotic colonization of infants and of the neonatal intensive care unit as a possible source of colonizing strains. This is partly because microbiome studies often utilize bacterial 16S rRNA marker gene sequencing, a technique that is blind to eukaryotic organisms. Knowledge gaps exist regarding the phylogeny and microdiversity of eukaryotes that colonize hospitalized infants, as well as potential reservoirs of eukaryotes in the hospital room built environment. Results: Genome-resolved analysis of 1174 time-series fecal metagenomes from 161 premature infants revealed fungal colonization of 10 infants. Relative abundance levels reached as high as 97% and were significantly higher in the first weeks of life (p = 0.004). When fungal colonization occurred, multiple species were present more often than expected by random chance (p = 0.008). Twenty-four metagenomic samples were analyzed from hospital rooms of six different infants. Compared to floor and surface samples, hospital sinks hosted diverse and highly variable communities containing genomically novel species, including from Diptera (fly) and Rhabditida (worm) for which genomes were assembled. With the exception of Diptera and two other organisms, zygosity of the newly assembled diploid eukaryote genomes was low. Interestingly, Malassezia and Candida species were present in both room and infant gut samples. Conclusions: Increased levels of fungal co-colonization may reflect synergistic interactions or differences in infant susceptibility to fungal colonization. Discovery of eukaryotic organisms that have not been sequenced previously highlights the benefit of genome-resolved analyses, and low zygosity of assembled genomes could reflect inbreeding or strong selection imposed by room conditions.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627050

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 7; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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The first microbial environment of infants born by C-section: the operating room microbes Shin, Hakdong; Pei, Zhiheng; Martinez, Keith A. Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-015-0126-1	journal	December 2015
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Bacterial Diversity in Two Neonatal Intensive Care Units (NICUs) Hewitt, Krissi M.; Mannino, Frank L.; Gonzalez, Antonio PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054703	journal	January 2013
Fungal Colonization in the Very Low Birth Weight Infant Baley, Jill E.; Kliegman, Robert M.; Boxerbaum, Bernard Pediatrics, Vol. 78, Issue 2 https://doi.org/10.1542/peds.78.2.225	journal	August 1986
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Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. Salter, Susannah; Cox, Michael J.; Turek, Elena M. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.41109	text	January 2014
An inter-laboratory study to investigate the impact of the bioinformatics component on microbiome analysis using mock communities. O'Sullivan, Denise M.; Doyle, Ronan M.; Temisak, Sasithon Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.71609	text	January 2021
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Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development Raveh-Sadka, Tali; Thomas, Brian C.; Singh, Andrea eLife, Vol. 4 https://doi.org/10.7554/eLife.05477	journal	March 2015

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The use of taxon-specific reference databases compromises metagenomic classification R. Marcelino, Vanessa; Holmes, Edward C.; Sorrell, Tania C. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-6592-2	journal	February 2020
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Additional file 3 of Using strain-resolved analysis to identify contamination in metagenomics data Lou, Yue Clare; Hoff, Jordan; Olm, Matthew R. figshare https://doi.org/10.6084/m9.figshare.22613114.v1	dataset	January 2023
Early exposure to antibiotics in the neonatal intensive care unit alters the taxonomic and functional infant gut microbiome Bender, Jeffrey M.; Li, Fan; Purswani, Heena The Journal of Maternal-Fetal & Neonatal Medicine https://doi.org/10.1080/14767058.2019.1684466	journal	November 2019
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Hospitalized Premature Infants Are Colonized by Related Bacterial Strains with Distinct Proteomic Profiles

Journal Article · Mon Apr 09 20:00:00 EDT 2018 · mBio (Online) · OSTI ID:1474619

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Eukaryotes
Genome-resolved metagenomics
Hospital microbiome
Metagenomics
Microbiology
Neonatal intensive care unit
Premature infants

Additional file 10: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729763 The current record is supplemented by this image	image	January 2019
Additional file 10: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729763.v1 The current record is supplemented by this image	image	January 2019
Additional file 11: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729769 The current record is supplemented by this image	image	January 2019
Additional file 11: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729769.v1 The current record is supplemented by this image	image	January 2019
Additional file 12: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729778 The current record is supplemented by this text	text	January 2019
Additional file 12: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729778.v1 The current record is supplemented by this text	text	January 2019
Additional file 13: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729784 The current record is supplemented by this image	image	January 2019
Additional file 13: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729784.v1 The current record is supplemented by this image	image	January 2019
Additional file 14: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729790 The current record is supplemented by this image	image	January 2019
Additional file 14: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729790.v1 The current record is supplemented by this image	image	January 2019
Additional file 15: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729799 The current record is supplemented by this image	image	January 2019
Additional file 15: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729799.v1 The current record is supplemented by this image	image	January 2019
Additional file 1: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729805 The current record is supplemented by this dataset	dataset	January 2019
Additional file 1: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729805.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 2: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729811 The current record is supplemented by this dataset	dataset	January 2019
Additional file 2: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729811.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 3: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729817 The current record is supplemented by this image	image	January 2019
Additional file 3: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729817.v1 The current record is supplemented by this image	image	January 2019
Additional file 4: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729820 The current record is supplemented by this image	image	January 2019
Additional file 4: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729820.v1 The current record is supplemented by this image	image	January 2019
Additional file 5: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729829 The current record is supplemented by this dataset	dataset	January 2019
Additional file 5: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729829.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 6: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729835 The current record is supplemented by this text	text	January 2019
Additional file 6: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729835.v1 The current record is supplemented by this text	text	January 2019
Additional file 7: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729844 The current record is supplemented by this dataset	dataset	January 2019
Additional file 7: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729844.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 8: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729847 The current record is supplemented by this dataset	dataset	January 2019
Additional file 8: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729847.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 9: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729853 The current record is supplemented by this image	image	January 2019
Additional file 9: of Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.7729853.v1 The current record is supplemented by this image	image	January 2019
Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.c.4404395 The current record is supplemented by this collection	collection	January 2019
Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms Olm, Matthew; West, Patrick; Brooks, Brandon https://doi.org/10.6084/m9.figshare.c.4404395.v1 The current record is supplemented by this collection	collection	January 2019

Genome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms

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