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

eLife

Volumn 2015, Issue 4, 2015, Pages

  Raveh Sadka, Tali ^a   Thomas, Brian C ^a   Singh, Andrea ^a   Firek, Brian ^b   Brooks, Brandon ^a   Castelle, Cindy J ^a   Sharon, Itai ^a   Baker, Robyn ^c   Good, Misty ^b,c   Morowitz, Michael J ^b   Banfield, Jillian F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

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

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL STRAIN; CANDIDA PARAPSILOSIS; CLOSTRIDIUM PARAPUTRIFICUM; DNA SEQUENCE; ENTEROCOCCUS FAECALIS; FECES ANALYSIS; GENE DOSAGE; GENE LOCUS; GENE MAPPING; GENOTYPE; HUMAN; INCIDENCE; INFANT; INTESTINE FLORA; KLEBSIELLA; METAGENOMICS; MICROBIAL COMMUNITY; NECROTIZING ENTEROCOLITIS; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PREMATURITY; QUANTITATIVE TRAIT LOCUS MAPPING; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; BACTERIUM; HOSPITALIZATION; INTESTINE; ISOLATION AND PURIFICATION; MICROBIOLOGY; NEWBORN;

BACTERIA (MICROORGANISMS);

BACTERIA; ENTEROCOLITIS, NECROTIZING; HOSPITALIZATION; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INTESTINES;

EID: 85006276920     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05477     Document Type: Article

References (69)

1. Arrieta MC, Stiemsma LT, Amenyogbe N, Brown EM, Finlay B. 2014. The intestinal microbiome in early life: health and disease. Frontiers in Immunology 5:427. doi: 10.3389/fimmu.2014.00427.
2. Boccia D, Stolfi I, Lana S, Moro ML. 2001. Nosocomial necrotising enterocolitis outbreaks: epidemiology and control measures. European Journal of Pediatrics 160:385-391. doi: 10.1007/s004310100749.
3. Brooks B, Firek BA, Miller CS, Sharon I, Thomas BC, Baker R, Morowitz MJ, Banfield JF. 2014. Microbes in the neonatal intensive care unit resemble those found in the gut of premature infants. Microbiome 2:1. doi: 10.1186/ 2049-2618-2-1.
4. Butel MJ, Suau A, Campeotto F, Magne F, Aires J, Ferraris L, Kalach N, Leroux B, Dupont C. 2007. Conditions of bifidobacterial colonization in preterm infants: a prospective analysis. Journal of Pediatric Gastroenterology and Nutrition 44:577-582. doi: 10.1097/MPG.0b013e3180406b20.
5. Carlisle EM, Morowitz MJ. 2013. The intestinal microbiome and necrotizing enterocolitis. Current Opinion in Pediatrics 25:382-387. doi: 10.1097/MOP.0b013e3283600e91.
6. Chang JY, Shin SM, Chun J, Lee JH, Seo JK. 2011. Pyrosequencing-based molecular monitoring of the intestinal bacterial colonization in preterm infants. Journal of Pediatric Gastroenterology and Nutrition 53:512-519. doi: 10. 1097/MPG.0b013e318227e518.
7. Chin CS, Sorenson J, Harris JB, Robins WP, Charles RC, Jean-Charles RR, Bullard J, Webster DR, Kasarskis A, Peluso P, Paxinos EE, Yamaichi Y, Calderwood SB, Mekalanos JJ, Schadt EE, Waldor MK. 2011. The origin of the Haitian cholera outbreak strain. New England Journal of Medicine 364:33-42. doi: 10.1056/NEJMoa1012928.
8. Claud EC, Keegan KP, Brulc JM, Lu L, Bartels D, Glass E, Chang EB, Meyer F, Antonopoulos DA. 2013. Bacterial community structure and functional contributions to emergence of health or necrotizing enterocolitis in preterm infants. Microbiome 1:20. doi: 10.1186/2049-2618-1-20.
9. Costello EK, Carlisle EM, Bik EM, Morowitz MJ, Relman DA. 2013. Microbiome assembly across multiple body sites in low-birthweight infants. mBio 4:e00782. doi: 10.1128/mBio.00782-13.
10. Darling AE, Mau B, Perna NT. 2010. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLOS ONE 5:e11147. doi: 10.1371/journal.pone.0011147.
11. De Leoz ML, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, Mills DA, Lebrilla CB. 2014. Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota: a proof-of-concept study. Journal of Proteome Research.
12. Delcher AL, Phillippy A, Carlton J, Salzberg SL. 2002. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Research 30:2478-2483. doi: 10.1093/nar/30.11.2478.
13. Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP, Banfield JF. 2009. Community-wide analysis of microbial genome sequence signatures. Genome Biology 10:R85. doi: 10.1186/gb-2009-10-8-r85.
14. Didelot X, Bowden R, Wilson DJ, Peto TE, Crook DW. 2012. Transforming clinical microbiology with bacterial genome sequencing. Nature Reviews Genetics 13:601-612. doi: 10.1038/nrg3226.
15. Dingle KE, Elliott B, Robinson E, Griffiths D, Eyre DW, Stoesser N, Vaughan A, Golubchik T, Fawley WN, Wilcox MH, Peto TE, Walker AS, Riley TV, Crook DW, Didelot X. 2014. Evolutionary history of the Clostridium difficile pathogenicity locus. Genome Biology and Evolution 6:36-52. doi: 10.1093/gbe/evt204.
16. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. doi: 10.1093/bioinformatics/btq461.
17. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312:1355-1359. doi: 10. 1126/science.1124234.
18. Gilmore MS, Lebreton F, van Schaik W. 2013. Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era. Current Opinion in Microbiology 16:10-16. doi: 10.1016/j.mib.2013.01.006.
19. Grave GD, Nelson SA, Walker WA, Moss RL, Dvorak B, Hamilton FA, Higgins R, Raju TN. 2007. New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatric Research 62:510-514. doi: 10.1203/PDR.0b013e318142580a.
20. Greenwood C, Morrow AL, Lagomarcino AJ, Altaye M, Taft DH, Yu Z, Newburg DS, Ward DV, Schibler KR. 2014. Early empiric antibiotic use in preterm infants is associated with lower bacterial diversity and higher relative abundance of enterobacter. The Journal of Pediatrics 165:23-29. doi: 10.1016/j.jpeds.2014.01.010.
21. Han VK, Sayed H, Chance GW, Brabyn DG, Shaheed WA. 1983. An outbreak of Clostridium difficile necrotizing enterocolitis: a case for oral vancomycin therapy? Pediatrics 71:935-941.
22. Härtel C, Faust K, Avenarius S, Bohnhorst B, Emeis M, Gebauer C, Groneck P, Heitmann F, Hoehn T, Hubert M, Kribs A, Küster H, Laux R, Mögel M, Müller D, Olbertz D, Roll C, Siegel J, Stein A, Vochem M, Weller U, von der Wense A, Wieg C, Wintgens J, Hemmelmann C, Simon A, Herting E, Göpel W, German Neonatal Network (GNN). 2012. Epidemic microclusters of blood-culture proven sepsis in very-low-birth weight infants: experience of the German Neonatal Network. PLOS ONE 7:e38304. doi: 10.1371/journal.pone.0038304.
23. He M, Miyajima F, Roberts P, Ellison L, Pickard DJ, Martin MJ, Connor TR, Harris SR, Fairley D, Bamford KB, D'Arc S, Brazier J, Brown D, Coia JE, Douce G, Gerding D, Kim HJ, Koh TH, Kato H, Senoh M, Louie T, Michell S, Butt E, Peacock SJ, Brown NM, Riley T, Songer G, Wilcox M, Pirmohamed M, Kuijper E, Hawkey P, Wren BW, Dougan G, Parkhill J, Lawley TD. 2013. Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nature Genetics 45:109-113. doi: 10.1038/ng.2478.
24. Hospodsky D, Qian J, Nazaroff WW, Yamamoto N, Bibby K, Rismani-Yazdi H, Peccia J. 2012. Human occupancy as a source of indoor airborne bacteria. PLOS ONE 7:e34867. doi: 10.1371/journal.pone.0034867.
25. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. doi: 10.1186/1471-2105-11-119.
26. Joshi N, Fass J. 2011. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.29) [Software].
27. 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 Research 42:D199-D205. doi: 10.1093/nar/gkt1076.
28. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30:3059-3066. doi: 10.1093/nar/gkf436.
29. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649. doi: 10. 1093/bioinformatics/bts199.
30. Kennedy NA, Walker AW, Berry SH, Duncan SH, Farquarson FM, Louis P, Thomson JM, UK IBD Genetics Consortium, Satsangi J, Flint HJ, Parkhill J, Lees CW, Hold GL. 2014. The impact of different DNA extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. PLOS ONE 9:e88982. doi: 10.1371/journal.pone.0088982.
31. Köser CU, Holden MT, Ellington MJ, Cartwright EJ, Brown NM, Ogilvy-Stuart AL, Hsu LY, Chewapreecha C, Croucher NJ, Harris SR, Sanders M, Enright MC, Dougan G, Bentley SD, Parkhill J, Fraser LJ, Betley JR, Schulz- Trieglaff OB, Smith GP, Peacock SJ. 2012. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. New England Journal of Medicine 366:2267-2275. doi: 10.1056/NEJMoa1109910.
32. Kuczynski J, Lauber CL, Walters WA, Parfrey LW, Clemente JC, Gevers D, Knight R. 2012. Experimental and analytical tools for studying the human microbiome. Nature Reviews Genetics 13:47-58. doi: 10.1038/ nrg3129.
33. Leinonen R, Diez FG, Binns D, Fleischmann W, Lopez R, Apweiler R. 2004. UniProt archive. Bioinformatics 20: 3236-3237. doi: 10.1093/bioinformatics/bth191.
34. Loman NJ, Constantinidou C, Christner M, Rohde H, Chan JZ, Quick J, Weir JC, Quince C, Smith GP, Betley JR, Aepfelbacher M, Pallen MJ. 2013. A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of Shiga-toxigenic Escherichia coli O104:H4. JAMA 309:1502-1510. doi: 10.1001/ jama.2013.3231.
35. Lowe TM, Eddy SR. 1997. Trnascan-se: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25:0955-0964. doi: 10.1093/nar/25.5.0955.
36. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, Theriaque D, Li N, Sharma R, Hudak M, Neu J. 2011. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLOS ONE 6:e20647. doi: 10.1371/ journal.pone.0020647.
37. Mally P, Golombek SG, Mishra R, Nigam S, Mohandas K, Depalhma H, LaGamma EF. 2006. Association of necrotizing enterocolitis with elective packed red blood cell transfusions in stable, growing, premature neonates. American Journal of Perinatology 23:451-458. doi: 10.1055/s-2006-951300.
38. Meinzen-Derr J, Morrow AL, Hornung RW, Donovan EF, Dietrich KN, Succop PA. 2009. Epidemiology of necrotizing enterocolitis temporal clustering in two neonatology practices. The Journal of Pediatrics 154: 656-661. doi: 10.1016/j.jpeds.2008.11.002.
39. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD. 2011. The human gut virome: interindividual variation and dynamic response to diet. Genome Research 21:1616-1625. doi: 10.1101/gr.122705.111.
40. Morowitz MJ, Poroyko V, Caplan M, Alverdy J, Liu DC. 2010. Redefining the role of intestinal microbes in the pathogenesis of necrotizing enterocolitis. Pediatrics 125:777-785. doi: 10.1542/peds.2009-3149.
41. Morrow AL, Lagomarcino AJ, Schibler KR, Taft DH, Yu Z, Wang B, Altaye M, Wagner M, Gevers D, Ward DV, Kennedy MA, Huttenhower C, Newburg DS. 2013. Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome 1:13. doi: 10.1186/2049-2618-1-13.
42. Mshvildadze M, Neu J, Shuster J, Theriaque D, Li N, Mai V. 2010. Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. The Journal of Pediatrics 156:20-25. doi: 10.1016/j.jpeds.2009.06.063.
43. Nawrocki EP, Eddy SR. 2013. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933-2935. doi: 10.1093/bioinformatics/btt509.
44. Neu J, Walker WA. 2011. Necrotizing enterocolitis. The New England Journal of Medicine 364:255-264. doi: 10. 1056/NEJMra1005408.
45. Normann E, Fahlén A, Engstrand L, Lilja HE. 2013. Intestinal microbial profiles in extremely preterm infants with and without necrotizing enterocolitis. Acta Paediatrica 102:129-136. doi: 10.1111/apa.12059.
46. Nueno-Palop C, Narbad A. 2011. Probiotic assessment of Enterococcus faecalis CP58 isolated from human gut. International Journal of Food Microbiology 145:390-394. doi: 10.1016/j.ijfoodmicro.2010.12.029.
47. Palmer KL, Gilmore MS. 2010. Multidrug-resistant enterococci lack CRISPR-cas. mBio 1:. doi: 10.1128/mBio. 00227-10.
48. Peng Y, Leung HC, Yiu SM, Chin FY. 2012. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28:1420-1428. doi: 10.1093/bioinformatics/bts174.
49. Pérez-González J, Ventura Faci MP, Samper Villagrasa MP, Gallego Beamonte JA, Ruiz Lázaro PJ, Castillo Garćıa FJ. 1996. An epidemic outbreak of necrotizing enterocolitis due to Clostridium difficile in term newborn infants. Anales Españoles De Pediatría 44:173-175.
50. Ramirez-Farias C, Slezak K, Fuller Z, Duncan A, Holtrop G, Louis P. 2009. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. The British Journal of Nutrition 101:541-550. doi: 10.1017/S0007114508019880.
51. Relman DA. 2011. Microbial genomics and infectious diseases. The New England Journal of Medicine 365: 347-357. doi: 10.1056/NEJMra1003071.
52. Salyers AA, Gupta A, Wang Y. 2004. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends in Microbiology 12:412-416. doi: 10.1016/j.tim.2004.07.004.
53. Schjørring S, Struve C, Krogfelt KA. 2008. Transfer of antimicrobial resistance plasmids from Klebsiella pneumoniae to Escherichia coli in the mouse intestine. The Journal of Antimicrobial Chemotherapy 62: 1086-1093. doi: 10.1093/jac/dkn323.
54. Schnabl KL, Van Aerde JE, Thomson AB, Clandinin MT. 2008. Necrotizing enterocolitis: a multifactorial disease with no cure. World Journal of Gastroenterology 14:2142-2161. doi: 10.3748/wjg.14.2142.
55. Sharon 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 Research 23:111-120. doi: 10.1101/gr.142315.112.
56. Snitkin ES, Zelazny AM, Thomas PJ, Stock FNISC Comparative Sequencing Program GroupHenderson DK, Palmore TN, Segre JA. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Science Translational Medicine 4:148ra116. doi: 10.1126/scitranslmed.3004129.
57. Stoll BJ, Hansen N, Fanaroff AA, Wright LL, Carlo WA, Ehrenkranz RA, Lemons JA, Donovan EF, Stark AR, Tyson JE, Oh W, Bauer CR, Korones SB, Shankaran S, Laptook AR, Stevenson DK, Papile LA, Poole WK. 2002. Lateonset sepsis in very low birth weight neonates: the experience of the NICHD Neonatal Research Network. Pediatrics 110:285-291. doi: 10.1542/peds.110.2.285.
58. Taft DH, Ambalavanan N, Schibler KR, Yu Z, Newburg DS, Ward DV, Morrow AL. 2014. Intestinal microbiota of preterm infants differ over time and between hospitals. Microbiome 2:36. doi: 10.1186/2049-2618-2-36.
59. Torrazza RM, Ukhanova M, Wang X, Sharma R, Hudak ML, Neu J, Mai V. 2013. Intestinal microbial ecology and environmental factors affecting necrotizing enterocolitis. PLOS ONE 8:e83304. doi: 10.1371/journal.pone. 0083304.
60. Turcios-Ruiz RM, Axelrod P, St John K, Bullitt E, Donahue J, Robinson N, Friss HE. 2008. Outbreak of necrotizing enterocolitis caused by norovirus in a neonatal intensive care unit. The Journal of Pediatrics 153:339-344. doi: 10. 1016/j.jpeds.2008.04.015.
61. Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37-43. doi: 10.1038/nature02340.
62. Tyson GW, Banfield JF. 2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environmental Microbiology 10:200-207.
63. Ultsch A, Moerchen F. 2005. ESOM-Maps: tools for clustering, visualization, and classification with Emergent SOM. Technical Report Department of Mathematics and Computer Science, University of Marburg, Germany (46).
64. Vallès Y, Artacho A, Pascual-Garćıa A, Ferruś ML, Gosalbes MJ, Abellán JJ, Francino MP. 2014. Microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of Spanish infants. PLOS Genetics 10:e1004406. doi: 10.1371/journal.pgen.1004406.
65. Waligora-Dupriet AJ, Dugay A, Auzeil N, Huerre M, Butel MJ. 2005. Evidence for clostridial implication in necrotizing enterocolitis through bacterial fermentation in a gnotobiotic quail model. Pediatric Research 58: 629-635. doi: 10.1203/01.PDR.0000180538.13142.84.
66. Wan-Huen P, Bateman D, Shapiro DM, Parravicini E. 2013. Packed red blood cell transfusion is an independent risk factor for necrotizing enterocolitis in premature infants. Journal of Perinatology 33:786-790. doi: 10.1038/jp. 2013.60.
67. Wang S, Hibberd ML, Pettersson S, Lee YK. 2014. Enterococcus faecalis from healthy infants modulates inflammation through MAPK signaling pathways. PLOS ONE 9:e97523. doi: 10.1371/journal.pone.0097523.
68. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J, Antonopoulos DA, Chang EB, Claud EC. 2009. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. The ISME journal 3:944-954. doi: 10.1371/journal.pone.0097523.
69. Wilson MR, Naccache SN, Samayoa E, Biagtan M, Bashir H, Yu G, Salamat SM, Somasekar S, Federman S, Miller S, Sokolic R, Garabedian E, Candotti F, Buckley RH, Reed KD, Meyer TL, Seroogy CM, Galloway R, Henderson SL, Gern JE, DeRisi JL, Chiu CY. 2014. Actionable diagnosis of Neuroleptospirosis by next-generation sequencing. New England Journal of Medicine 370:2408-2417. doi: 10.1056/NEJMoa1401268.