Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development

Raveh-Sadka, Tali; Thomas, Brian C.; Singh, Andrea; Firek, Brian; Brooks, Brandon; Castelle, Cindy J.; Sharon, Itai; Baker, Robyn; Good, Misty; Morowitz, Michael J.; Banfield, Jillian F.

doi:10.7554/eLife.05477

Title: Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development

Journal Article · Tue Mar 03 00:00:00 EST 2015 · eLife

DOI:https://doi.org/10.7554/eLife.05477· OSTI ID:1171761

Raveh-Sadka, Tali ^[1]; Thomas, Brian C. ^[1]; Singh, Andrea ^[1]; Firek, Brian ^[2];

^[1]; Castelle, Cindy J. ^[1]; Sharon, Itai ^[1]; Baker, Robyn ^[3]; Good, Misty ^[4]; Morowitz, Michael J. ^[2]; Banfield, Jillian F. ^[1]

Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, United States
Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, United States
Division of Newborn Medicine, Children's Hospital of Pittsburgh and Magee-Womens Hospital of UPMC, Pittsburgh, United States
Division of Newborn Medicine, Children's Hospital of Pittsburgh and Magee-Womens Hospital of UPMC, Pittsburgh, United States, Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, United States

Premature infants are highly vulnerable to aberrant gastrointestinal tract colonization, a process that may lead to diseases like necrotizing enterocolitis. Thus, spread of potential pathogens among hospitalized infants is of great concern. Here, we reconstructed hundreds of high-quality genomes of microorganisms that colonized co-hospitalized premature infants, assessed their metabolic potential, and tracked them over time to evaluate bacterial strain dispersal among infants. We compared microbial communities in infants who did and did not develop necrotizing enterocolitis. Surprisingly, while potentially pathogenic bacteria of the same species colonized many infants, our genome-resolved analysis revealed that strains colonizing each baby were typically distinct. In particular, no strain was common to all infants who developed necrotizing enterocolitis. The paucity of shared gut colonizers suggests the existence of significant barriers to the spread of bacteria among infants. Importantly, we demonstrate that strain-resolved comprehensive community analysis can be accomplished on potentially medically relevant time scales.

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Research Organization:: Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0004918; ER65561

OSTI ID:: 1171761

Alternate ID(s):: OSTI ID: 1243127; OSTI ID: 1455039

Journal Information:: eLife, Journal Name: eLife Vol. 4; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 83 works

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References (57)

New Therapies and Preventive Approaches for Necrotizing Enterocolitis: Report of a Research Planning Workshop Grave, Gilman D.; Nelson, Stefanie A.; Walker, W. Allan Pediatric Research, Vol. 62, Issue 4 https://doi.org/10.1203/PDR.0b013e318142580a	journal	October 2007
Human intestinal bacteria as reservoirs for antibiotic resistance genes Salyers, A.; Gupta, A.; Wang, Y. Trends in Microbiology, Vol. 12, Issue 9 https://doi.org/10.1016/j.tim.2004.07.004	journal	September 2004
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
Evidence for Clostridial Implication in Necrotizing Enterocolitis through Bacterial Fermentation in a Gnotobiotic Quail Model Waligora-Dupriet, Anne-Judith; Dugay, Annabelle; Auzeil, Nicolas Pediatric Research, Vol. 58, Issue 4 https://doi.org/10.1203/01.PDR.0000180538.13142.84	journal	October 2005
The Impact of Different DNA Extraction Kits and Laboratories upon the Assessment of Human Gut Microbiota Composition by 16S rRNA Gene Sequencing Kennedy, Nicholas A.; Walker, Alan W.; Berry, Susan H. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0088982	journal	February 2014
Microbial Genomics and Infectious Diseases Relman, David A. New England Journal of Medicine, Vol. 365, Issue 4 https://doi.org/10.1056/NEJMra1003071	journal	July 2011
The human gut virome: Inter-individual variation and dynamic response to diet Minot, S.; Sinha, R.; Chen, J. Genome Research, Vol. 21, Issue 10 https://doi.org/10.1101/gr.122705.111	journal	August 2011
Necrotizing enterocolitis: A multifactorial disease with no cure Schnabl, Kareena L.; Aerde, John E. Van; Thomson, Alan BR World Journal of Gastroenterology, Vol. 14, Issue 14 https://doi.org/10.3748/wjg.14.2142	journal	January 2008
Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants Brooks, Brandon; Firek, Brian A.; Miller, Christopher S. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-1	journal	January 2014
Emergence and global spread of epidemic healthcare-associated Clostridium difficile He, Miao; Miyajima, Fabio; Roberts, Paul Nature Genetics, Vol. 45, Issue 1 https://doi.org/10.1038/ng.2478	journal	December 2012
Metagenomic Analysis of the Human Distal Gut Microbiome Gill, S. R.; Pop, M.; DeBoy, R. T. Science, Vol. 312, Issue 5778 https://doi.org/10.1126/science.1124234	journal	June 2006
Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization Sharon, I.; Morowitz, M. J.; Thomas, B. C. Genome Research, Vol. 23, Issue 1 https://doi.org/10.1101/gr.142315.112	journal	August 2012
The Intestinal Microbiome in Early Life: Health and Disease Arrieta, Marie-Claire; Stiemsma, Leah T.; Amenyogbe, Nelly Frontiers in Immunology, Vol. 5 https://doi.org/10.3389/fimmu.2014.00427	journal	September 2014
Necrotizing Enterocolitis Neu, Josef; Walker, W. Allan New England Journal of Medicine, Vol. 364, Issue 3 https://doi.org/10.1056/NEJMra1005408	journal	January 2011
Data, information, knowledge and principle: back to metabolism in KEGG Kanehisa, Minoru; Goto, Susumu; Sato, Yoko Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1076	journal	November 2013
Nosocomial necrotising enterocolitis outbreaks: epidemiology and control measures Boccia, Delia; Stolfi, Ilaria; Lana, Susanna European Journal of Pediatrics, Vol. 160, Issue 6 https://doi.org/10.1007/s004310100749	journal	May 2001
Community-wide analysis of microbial genome sequence signatures Dick, Gregory J.; Andersson, Anders F.; Baker, Brett J. Genome Biology, Vol. 10, Issue 8 https://doi.org/10.1186/gb-2009-10-8-r85	journal	January 2009
Outbreak of Necrotizing Enterocolitis Caused by Norovirus in a Neonatal Intensive Care Unit Turcios-Ruiz, Reina M.; Axelrod, Peter; St. John, Keith The Journal of Pediatrics, Vol. 153, Issue 3 https://doi.org/10.1016/j.jpeds.2008.04.015	journal	September 2008
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.0955	journal	March 1997
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Transfer of antimicrobial resistance plasmids from Klebsiella pneumoniae to Escherichia coli in the mouse intestine Schjorring, S.; Struve, C.; Krogfelt, K. A. Journal of Antimicrobial Chemotherapy, Vol. 62, Issue 5 https://doi.org/10.1093/jac/dkn323	journal	July 2008
Conditions of Bifidobacterial Colonization in Preterm Infants: A Prospective Analysis Butel, Marie-José; Suau, Antonia; Campeotto, Florence Journal of Pediatric Gastroenterology and Nutrition, Vol. 44, Issue 5 https://doi.org/10.1097/MPG.0b013e3180406b20	journal	January 2007
Association of Necrotizing Enterocolitis with Elective Packed Red Blood Cell Transfusions in Stable, Growing, Premature Neonates Mally, Pradeep; Golombek, Sergio; Mishra, Ravi American Journal of Perinatology, Vol. 23, Issue 8 https://doi.org/10.1055/s-2006-951300	journal	November 2006
Pyrosequencing-Based Molecular Monitoring of the Intestinal Bacterial Colonization in Preterm Infants Chang, Ju Young; Shin, Son Moon; Chun, Jongsik Journal of Pediatric Gastroenterology and Nutrition https://doi.org/10.1097/MPG.0b013e318227e518	journal	January 2011
Early Empiric Antibiotic Use in Preterm Infants Is Associated with Lower Bacterial Diversity and Higher Relative Abundance of Enterobacter Greenwood, Corryn; Morrow, Ardythe L.; Lagomarcino, Anne J. The Journal of Pediatrics, Vol. 165, Issue 1 https://doi.org/10.1016/j.jpeds.2014.01.010	journal	July 2014
Experimental and analytical tools for studying the human microbiome Kuczynski, Justin; Lauber, Christian L.; Walters, William A. Nature Reviews Genetics, Vol. 13, Issue 1 https://doi.org/10.1038/nrg3129	journal	December 2011
The intestinal microbiome and necrotizing enterocolitis Carlisle, Erica M.; Morowitz, Michael J. Current Opinion in Pediatrics, Vol. 25, Issue 3 https://doi.org/10.1097/MOP.0b013e3283600e91	journal	January 2013
Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants Morrow, Ardythe L.; Lagomarcino, Anne J.; Schibler, Kurt R. Microbiome, Vol. 1, Issue 1 https://doi.org/10.1186/2049-2618-1-13	journal	April 2013
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Intestinal Microbial Ecology and Environmental Factors Affecting Necrotizing Enterocolitis Torrazza, Roberto Murgas; Ukhanova, Maria; Wang, Xiaoyu PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0083304	journal	December 2013
A Culture-Independent Sequence-Based Metagenomics Approach to the Investigation of an Outbreak of Shiga-Toxigenic Escherichia coli O104:H4 Loman, Nicholas J.; Constantinidou, Chrystala; Christner, Martin JAMA, Vol. 309, Issue 14 https://doi.org/10.1001/jama.2013.3231	journal	April 2013
Epidemic Microclusters of Blood-Culture Proven Sepsis in Very-Low-Birth Weight Infants: Experience of the German Neonatal Network Härtel, Christoph; Faust, Kirstin; Avenarius, Stefan PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0038304	journal	June 2012
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement Darling, Aaron E.; Mau, Bob; Perna, Nicole T. PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011147	journal	June 2010
Intestinal microbial profiles in extremely preterm infants with and without necrotizing enterocolitis Normann, Erik; Fahlén, Annika; Engstrand, Lars Acta Paediatrica, Vol. 102, Issue 2 https://doi.org/10.1111/apa.12059	journal	November 2012
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Katoh, K. Nucleic Acids Research, Vol. 30, Issue 14 https://doi.org/10.1093/nar/gkf436	journal	July 2002
Human Occupancy as a Source of Indoor Airborne Bacteria Hospodsky, Denina; Qian, Jing; Nazaroff, William W. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0034867	journal	April 2012
Bacterial community structure and functional contributions to emergence of health or necrotizing enterocolitis in preterm infants Claud, Erika C.; Keegan, Kevin P.; Brulc, Jennifer M. Microbiome, Vol. 1, Issue 1 https://doi.org/10.1186/2049-2618-1-20	journal	July 2013
Epidemiology of Necrotizing Enterocolitis Temporal Clustering in Two Neonatology Practices Meinzen-Derr, Jareen; Morrow, Ardythe L.; Hornung, Richard W. The Journal of Pediatrics, Vol. 154, Issue 5 https://doi.org/10.1016/j.jpeds.2008.11.002	journal	May 2009
Packed red blood cell transfusion is an independent risk factor for necrotizing enterocolitis in premature infants Wan-Huen, P.; Bateman, D.; Shapiro, D. M. Journal of Perinatology, Vol. 33, Issue 10 https://doi.org/10.1038/jp.2013.60	journal	May 2013
Microbial Succession in the Gut: Directional Trends of Taxonomic and Functional Change in a Birth Cohort of Spanish Infants Vallès, Yvonne; Artacho, Alejandro; Pascual-García, Alberto PLoS Genetics, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pgen.1004406	journal	June 2014
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
Intestinal microbiota of preterm infants differ over time and between hospitals Taft, Diana H.; Ambalavanan, Namasivayam; Schibler, Kurt R. Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-36	journal	January 2014
Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era Gilmore, Michael S.; Lebreton, Francois; van Schaik, Willem Current Opinion in Microbiology, Vol. 16, Issue 1 https://doi.org/10.1016/j.mib.2013.01.006	journal	February 2013
Intestinal Microbial Ecology in Premature Infants Assessed with Non–Culture-Based Techniques Mshvildadze, Maka; Neu, Josef; Shuster, Jonathan The Journal of Pediatrics, Vol. 156, Issue 1 https://doi.org/10.1016/j.jpeds.2009.06.063	journal	January 2010
Redefining the Role of Intestinal Microbes in the Pathogenesis of Necrotizing Enterocolitis Morowitz, M. J.; Poroyko, V.; Caplan, M. PEDIATRICS, Vol. 125, Issue 4 https://doi.org/10.1542/peds.2009-3149	journal	March 2010
Probiotic assessment of Enterococcus faecalis CP58 isolated from human gut Nueno-Palop, Carmen; Narbad, Arjan International Journal of Food Microbiology, Vol. 145, Issue 2-3 https://doi.org/10.1016/j.ijfoodmicro.2010.12.029	journal	February 2011
Fecal Microbiota in Premature Infants Prior to Necrotizing Enterocolitis Mai, Volker; Young, Christopher Michael; Ukhanova, Maria PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0020647	journal	June 2011
Tracking a Hospital Outbreak of Carbapenem-Resistant Klebsiella pneumoniae with Whole-Genome Sequencing Snitkin, E. S.; Zelazny, A. M.; Thomas, P. J. Science Translational Medicine, Vol. 4, Issue 148 https://doi.org/10.1126/scitranslmed.3004129	journal	August 2012
Late-Onset Sepsis in Very Low Birth Weight Neonates: The Experience of the NICHD Neonatal Research Network Stoll, B. J.; Hansen, N.; Fanaroff, A. A. PEDIATRICS, Vol. 110, Issue 2 https://doi.org/10.1542/peds.110.2.285	journal	August 2002
UniProt archive Leinonen, R.; Diez, F. G.; Binns, D. Bioinformatics, Vol. 20, Issue 17 https://doi.org/10.1093/bioinformatics/bth191	journal	March 2004
Enterococcus faecalis from Healthy Infants Modulates Inflammation through MAPK Signaling Pathways Wang, Shugui; Hibberd, Martin Lloyd; Pettersson, Sven PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0097523	journal	May 2014
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
Fast algorithms for large-scale genome alignment and comparison Delcher, A. L. Nucleic Acids Research, Vol. 30, Issue 11 https://doi.org/10.1093/nar/30.11.2478	journal	June 2002
Evolutionary History of the Clostridium difficile Pathogenicity Locus Dingle, Kate E.; Elliott, Briony; Robinson, Esther Genome Biology and Evolution, Vol. 6, Issue 1 https://doi.org/10.1093/gbe/evt204	journal	December 2013
Transforming clinical microbiology with bacterial genome sequencing Didelot, Xavier; Bowden, Rory; Wilson, Daniel J. Nature Reviews Genetics, Vol. 13, Issue 9 https://doi.org/10.1038/nrg3226	journal	August 2012
Microbiome Assembly across Multiple Body Sites in Low-Birthweight Infants Costello, Elizabeth K.; Carlisle, Erica M.; Bik, Elisabeth M. mBio, Vol. 4, Issue 6 https://doi.org/10.1128/mBio.00782-13	journal	October 2013

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