Evidence for persistent and shared bacterial strains against a background of largely unique gut colonization in hospitalized premature infants

ISME Journal

Volumn 10, Issue 12, 2016, Pages 2817-2830

  Raveh Sadka, Tali ^a   Firek, Brian ^b   Sharon, Itai ^a   Baker, Robyn ^b   Brown, Christopher T ^a   Thomas, Brian C ^a   Morowitz, Michael J ^b   Banfield, Jillian F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC DIGESTION; ANTIBIOTICS; BACTERIUM; COHORT ANALYSIS; COLONIZATION; DISPERSAL; GENOME; ISOLATED POPULATION; MICROBIAL COMMUNITY; PERSISTENCE;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS; STAPHYLOCOCCUS EPIDERMIDIS;

BACTERIUM; CLASSIFICATION; COHORT ANALYSIS; FECES; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; INFANT; INTESTINE FLORA; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY; NEWBORN; PREMATURITY;

BACTERIA; COHORT STUDIES; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT; INFANT, NEWBORN; INFANT, PREMATURE; MALE;

EID: 84976329731     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2016.83     Document Type: Article

References (52)

1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. (2014). The placenta harbors a unique microbiome. Sci Transl Med 6: 237ra65-237ra65.
2. Arboleya S, Binetti A, Salazar N, Fernández N, Solís G, Hernández-Barranco A et al. (2012). Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol 79: 763-772.
3. Arrieta M-C, Stiemsma LT, Amenyogbe N, Brown EM, Finlay B. (2014). The intestinal microbiome in early life: health and disease. Front Immunol 5: e-pub ahead of print, doi: 10.3389/fimmu.2014.00427.
4. Aujoulat F, Roudière L, Picaud J-C, Jacquot A, Filleron A, Neveu D et al. (2014). Temporal dynamics of the very premature infant gut dominant microbiota. BMC Microbiol 14: 2320.
5. Barrett E, Kerr C, Murphy K, O'Sullivan O, Ryan CA, Dempsey EM et al. (2013). The individual-specific and diverse nature of the preterm infant microbiota. Arch Dis Child Fetal Neonatal Ed 98: F334-F340.
6. Brooks B, Firek BA, Miller CS, Sharon I, Thomas BC, Baker R et al. (2014). Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants. Microbiome 2: 1.
7. Brown CT, Sharon I, Thomas BC, Castelle CJ, Morowitz MJ, Banfield JF. (2013). Genome resolved analysis of a premature infant gut microbial community reveals a Varibaculum cambriense genome and a shift towards fermentation-based metabolism during the third week of life. Microbiome 1: 30.
8. Carlisle EM, Morowitz MJ. (2013). The intestinal microbiome and necrotizing enterocolitis. Curr Opin Pediatr 25: 382-387.
9. Chin C-S, Sorenson J, Harris JB, Robins WP, Charles RC, Jean-Charles RR et al. (2010). The origin of the haitian cholera outbreak strain. N Engl J Med 364: 33-42.
10. Costello EK, Carlisle EM, Bik EM, Morowitz MJ, Relman DA. (2013). Microbiome assembly across multiple body sites in low-birthweight infants. MBio 4: e00782-13.
11. De la Cochetiere M-F, Piloquet H, des Robert C, Darmaun D, Galmiche J-P, Roze J-C. (2004). Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of Clostridium. Pediatr Res 56: 366-370.
12. Deatherage DE, Barrick JE. (2014). Identification of mutations in laboratory-evolved microbes from nextgeneration sequencing data using breseq. Methods Mol Biol 1151: 165-188.
13. Delcher AL, Phillippy A, Carlton J, Salzberg SL. (2002). Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30: 2478-2483.
14. Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP et al. (2009). Community-wide analysis of microbial genome sequence signatures. Genome Biol 10: R85.
15. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
16. Fossum S, Crooke E, Skarstad K. (2007). Organization of sister origins and replisomes during multifork DNA replication in Escherichia coli. EMBO J 26: 4514-4522.
17. Funkhouser LJ, Bordenstein SR. (2013). Mom knows best: the universality of maternal microbial transmission. PLoS Biol 11: e1001631.
18. Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA. (2014). Development of the preterm infant gut microbiome: a research priority. Microbiome 2: 38.
19. Guttman D, Dykhuizen D. (1994). Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266: 1380-1383.
20. He M, Miyajima F, Roberts P, Ellison L, Pickard DJ, Martin MJ et al. (2013). Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nat Genet 45: 109-113.
21. Hendricks CW. (1972). Enteric bacterial growth rates in river water. Appl Microbiol 24: 168-174.
22. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
23. Joshi N, Fass J. (2011), Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.29) [Software].
24. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. (2014). Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42: D199-D205.
25. Köser CU, Holden MTG, Ellington MJ, Cartwright EJP, Brown NM, Ogilvy-Stuart AL et al. (2012). Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366: 2267-2275.
26. La Rosa PS, Warner BB, Zhou Y, Weinstock GM, Sodergren E, Hall-Moore CM et al. (2014). Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci 111: 12522-12527.
27. Langmead B, Salzberg SL. (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
28. Lee H, Popodi E, Tang H, Foster PL. (2012). Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by wholegenome sequencing. Proc Natl Acad Sci USA 109: E2774-E2783.
29. Leinonen R, Diez FG, Binns D, Fleischmann W, Lopez R, Apweiler R. (2004). UniProt archive. Bioinformatics 20: 3236-3237.
30. Loman N, Constantinidou C, Christner M, Rohde H, Chan JZ, Quick J et al. (2013). A culture-independent sequencebased metagenomics approach to the investigation of an outbreak of shiga-toxigenic escherichia coli o104: h4. JAMA 309: 1502-1510.
31. Lowe TM, Eddy SR. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 0955-0964.
32. Macdorman MF, Declercq E, Mathews TJ. (2013). Recent trends in out-of-hospital births in the United States. J Midwifery Women's Heal 58: 494-501.
33. Magne F, Abély M, Boyer F, Morville P, Pochart P, Suau A. (2006). Low species diversity and high interindividual variability in faeces of preterm infants as revealed by sequences of 16S rRNA genes and PCR-temporal temperature gradient gel electrophoresis profiles. FEMS Microbiol Ecol 57: 128-138.
34. Markowitz VM, Chen I-MA, Palaniappan K, Chu K, Szeto E, Pillay M et al. (2014). IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res 42: D560-D567.
35. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ et al. (2013). The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57: 3348-3357.
36. Moles L, Gómez M, Heilig H, Bustos G, Fuentes S, de Vos W et al. (2013). Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One 8: e66986.
37. Moran NA, McLaughlin HJ, Sorek R. (2009). The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323: 379-382.
38. Morowitz MJ, Denef VJ, Costello EK, Thomas BC, Poroyko V, Relman DA et al. (2011). Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proc Natl Acad Sci USA 108: 1128-1133.
39. Morrow AL, Lagomarcino AJ, Schibler KR, Taft DH, Yu Z, Wang B et al. (2013). Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome 1: 13.
40. Nawrocki EP, Eddy SR. (2013). Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29: 2933-2935.
41. Neu J, Walker WA. (2011). Necrotizing enterocolitis. N Engl J Med 364: 255-264.
42. Peng Y, Leung HCM, Yiu SM, Chin FYL. (2012). IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28: 1420-1428.
43. Raveh-Sadka T, Thomas BC, Singh A, Firek B, Brooks B, Castelle CJ et al. (2015). Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development. Elife; e-pub ahead of print 3 March 2015; doi:10.7554/eLife.05477.
44. Schnabl K-L, Van Aerde J-E, Thomson A-B, Clandinin M-T. (2008). Necrotizing enterocolitis: a multifactorial disease with no cure. World J Gastroenterol 14: q2142-2161.
45. Sha1ron I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF. (2013). Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res 23: 111-120.
46. Sim K, Shaw AG, Randell P, Cox MJ, McClure ZE, Li M-S et al. (2015). Dysbiosis anticipating necrotizing enterocolitis in very premature infants. Clin Infect Dis 60: 389-397.
47. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, Henderson DK, Palmore TN et al. (2012). Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4: 148ra116.
48. Sommer DD, Delcher AL, Salzberg SL, Pop M. (2007). Minimus: a fast, lightweight genome assembler. BMC Bioinformatics 8: 64.
49. Ultsch A, Moerchen F. (2005). ESOM-Maps: tools for clustering, visualization, and classification with Emergent SOM. Tech Rep Dep Math Comput Sci Univ Marburg, Ger 46.
50. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J et al. (2009). 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 3: 944-954.
51. Zerbino DR, Birney E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
52. Zhou Y, Shan G, Sodergren E, Weinstock G, Walker WA, Gregory KE. (2015). Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study. PLoS One 10: e0118632.