Identical bacterial populations colonize premature infant gut, skin, & oral microbiomes & exhibit different in situ growth rates

Genome Research

Volumn 27, Issue 4, 2017, Pages 601-612

  Olm, Matthew R ^a   Brown, Christopher T ^a   Brooks, Brandon ^a   Firek, Brian ^b   Baker, Robyn ^c   Burstein, David ^d   Soenjoyo, Karina ^a   Thomas, Brian C ^d   Morowitz, Michael ^b   Banfield, Jillian F ^d,e,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

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

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIOPHAGE; CITROBACTER KOSERI; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA BASE COMPOSITION; DNA SEQUENCE; GENE LOCUS; GENE REPLICATION; GENETIC POLYMORPHISM; HUMAN; INFANT; INTESTINE FLORA; METAGENOMICS; MICROBIOME; MOUTH FLORA; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; PREMATURITY; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SERRATIA MARCESCENS; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN FLORA; STAPHYLOCOCCUS EPIDERMIDIS; EXTREMELY LOW BIRTH WEIGHT; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOUTH; NEWBORN; PATHOGENICITY; SKIN;

CITROBACTER KOSERI; GASTROINTESTINAL MICROBIOME; GENOME, BACTERIAL; HUMANS; INFANT, EXTREMELY LOW BIRTH WEIGHT; INFANT, NEWBORN; INFANT, PREMATURE; MOUTH; POLYMORPHISM, GENETIC; SKIN;

EID: 85017559090     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.213256.116     Document Type: Article

References (73)

1. Achtman M, Wagner M. 2008. Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6: 431-440.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Arrieta M-C, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S, Kuzeljevic B, Gold MJ, Britton HM, Lefebvre DL, et al. 2015. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med 7: 307ra152.
4. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, et al. 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17: 690-703.
5. 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.
6. Brown CT, Olm MR, Thomas BC, Banfield JF. 2016. Measurement of bacterial replication rates in microbial communities. Nat Biotechnol 34: 1256-1263.
7. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA, Stares MD, Goulding D, Lawley TD. 2016. Culturing of 'unculturable'humanmicrobiota reveals novel taxa and extensive sporulation. Nature 533: 543-546.
8. Bushnell B. 2014. BBMap: A fast, accurate, splice-Aware aligner. Report Number: LBNL-7065E, Lawrence Berkeley National Laboratory, Berkeley, CA.
9. Cahenzli J, Köller Y, Wyss M, Geuking MB, McCoy KD. 2013. Intestinal microbial diversity during early-life colonization shapes long-Term IgE levels. Cell Host Microbe 14: 559-570.
10. Cilieborg MS, Boye M, Sangild PT. 2012. Bacterial colonization and gut development in preterm neonates. Early Hum Dev 88: S41-S49.
11. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA. 2012. The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255-1262.
12. 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.
13. Deatherage DE, Barrick JE. 2014. Identification of mutations in laboratoryevolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 1151: 165-188.
14. Ding T, Schloss PD. 2014. Dynamics and associations of microbial community types across the human body. Nature 509: 357-360.
15. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. 2010. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci 107: 11971-11975.
16. Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, Bokulich NA, Song SJ, Hoashi M, Rivera-Vinas JI, et al. 2016. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med 22: 250-253.
17. Donaldson GP, Lee SM, Mazmanian SK. 2015. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 14: 20-32.
18. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
19. El Tahir Y, Skurnik M. 2001. YadA, the multifaceted Yersinia adhesin. Int J Med Microbiol 291: 209-218.
20. Erkus O, de Jager VC, Spus M, van Alen-Boerrigter IJ, van Rijswijck IM, Hazelwood L, Janssen PW, van Hijum SA, Kleerebezem M, Smid EJ. 2013. Multifactorial diversity sustains microbial community stability. ISME J 7: 2126-2136.
21. Faith JJ, Colombel J-F, Gordon JI. 2015. Identifying strains that contribute to complex diseases through the study of microbial inheritance. Proc Natl Acad Sci 112: 633-640.
22. Gibson MK, Wang B, Ahmadi S, Burnham C-AD, Tarr PI, Warner BB, Dantas G. 2016. Developmental dynamics of the preterm infant gut microbiota and antibiotic resistome. Nat Microbiol 1: 16024.
23. Grigoriev A. 1998. Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res 26: 2286-2290.
24. Grissa I, Vergnaud G, Pourcel C. 2007. CRISPRFinder: A web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35: W52-W57.
25. Horvath P, Barrangou R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167-170.
26. 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.
27. Jaspers E, Overmann J. 2004. Ecological significance of microdiversity: Identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70: 4831-4839.
28. Jovel J, Patterson J, WangW, Hotte N, O'Keefe S, Mitchel T, Perry T, Kao D, Mason AL, Madsen KL, et al. 2016. Characterization of the gut microbiome using 16S or shotgun metagenomics. Front Microbiol 7: 459.
29. 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.
30. Karl DM. 1979. Measurement of microbial activity and growth in the ocean by rates of stable ribonucleic acid synthesis. Appl Environ Microbiol 38: 850-860.
31. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, et al. 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649.
32. King KC, Brockhurst MA, Vasieva O, Paterson S, Betts A, Ford SA, Frost CL, Horsburgh MJ, Haldenby S, Hurst GD. 2016. Rapid evolution of microbe- mediated protection against pathogens in a worm host. ISME J 10: 1915-1924.
33. Koboldt DC, Chen K, Wylie T, Larson DE, McLellan MD, Mardis ER, Weinstock GM, Wilson RK, Ding L. 2009. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 25: 2283-2285.
34. Korem T, Zeevi D, Suez J, Weinberger A, Avnit-Sagi T, Pompan-Lotan M, Matot E, Jona G, Harmelin A, Cohen N, et al. 2015. Growth dynamics of gut microbiota in health and disease inferred from single metagenomic samples. Science 349: 1101-1106.
35. Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, Botstein D, Desai MM. 2013. Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571-574.
36. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
37. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
38. Liu B, Faller LL, Klitgord N, Mazumdar V, Ghodsi M, Sommer DD, Gibbons TR, Treangen TJ, Chang Y-C, Li S, et al. 2012. Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One 7: E37919.
39. Lowe TM, Eddy SR. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
40. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM, Konstantinidis KT. 2011. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci 108: 7200-7205.
41. Luo C, Knight R, Siljander H, Knip M, Xavier RJ, Gevers D. 2015. ConStrains identifies microbial strains in metagenomic datasets. Nat Biotechnol 33: 1045-1052.
42. Morowitz MJ, Denef VJ, Costello EK, Thomas BC, Poroyko V, Relman DA, Banfield JF. 2011. Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proc Natl Acad Sci 108: 1128-1133.
43. Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. 2015. The infant microbiome development: mom matters. Trends Mol Med 21: 109-117.
44. Nawrocki E. 2009. "Structural RNA homology search and alignment using covariance models." PhD dissertation, Washington University, St. Louis, MO. http://openscholarship.wustl.edu/etd/256/.
45. Nawrocki EP, Eddy SR. 2013. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29: 2933-2935.
46. Nocker A, Cheung C-Y, Camper AK. 2006. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J Microbiol Methods 67: 310-320.
47. Palmer KL, Gilmore MS. 2010. Multidrug-resistant Enterococci lack CRISPRcas. MBio 1: E0022710-e0022719.
48. 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.
49. Pride DT, Sun CL, Salzman J, Rao N, Loomer P, Armitage GC, Banfield JF, Relman DA. 2011. Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 21: 126-136.
50. Prosser JI, Bohannan BJ, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, Green JL, Green LE, Killham K, Lennon JJ. 2007. The role of ecological theory in microbial ecology. Nat Rev Microbiol 5: 384-392.
51. Raes J, Korbel JO, Lercher MJ, Von Mering C, Bork P. 2007. Prediction of effective genome size in metagenomic samples. Genome Biol 8: 1.
52. Raveh-Sadka T, Thomas BC, Singh A, Firek B, Brooks B, Castelle CJ, Sharon I, Baker R, Good M, Morowitz MJ, et al. 2015. Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development. eLife 4: E05477.
53. Raveh-Sadka T, Firek B, Sharon I, Baker R, Brown CT, Thomas BC, Morowitz MJ, Banfield JF. 2016. Evidence for persistent and shared bacterial strains against a background of largely unique gut colonization in hospitalized premature infants. ISME J 10: 2817-2830.
54. Richter M, Rosselló-Móra R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106: 19126-19131.
55. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT. 2009. Reordering contigs of draft genomes using the Mauve Aligner. Bioinformatics 25: 2071-2073.
56. Rodriguez GG, Phipps D, Ishiguro K, Ridgway HF. 1992. Use of a fluorescent redox probe for direct visualization of actively respiring bacteria. Appl Environ Microbiol 58: 1801-1808.
57. Rodriguez-Brito B, Li L, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, Edwards R, et al. 2010. Viral and microbial community dynamics in four aquatic environments. ISME J 4: 739-751.
58. Rosen MJ, Davison M, Bhaya D, Fisher DS. 2015. Fine-scale diversity and extensive recombination in a quasisexual bacterial population occupying a broad niche. Science 348: 1019-1023.
59. Salzberg SL, Yorke JA. 2005. Beware of mis-Assembled genomes. Bioinformatics 21: 4320-4321.
60. 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 Res 23: 111-120.
61. Shin H, Pei Z, Martinez KA, Rivera-Vinas JI, Mendez K, Cavallin H, Dominguez-Bello MG. 2015. The first microbial environment of infants born by C-section: The operating room microbes. Microbiome 3: 59.
62. Sim K, Powell E, Shaw AG, McClure Z, Bangham M, Kroll JS. 2013. The neonatal gastrointestinal microbiota: The foundation of future health? Arch Dis Child Fetal Neonatal Ed 98: F362-F364.
63. Snitkin ES, Zelazny AM, Thomas PJ, Stock F; NISC Comparative Sequencing Program Group, Henderson DK, Palmore TN, Segre JA. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4: 148ra116.
64. Sun CL, Thomas BC, Barrangou R, Banfield JF. 2016. Metagenomic reconstructions of bacterial CRISPR loci constrain population histories. ISME J 10: 858-870.
65. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH. 2007. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23: 1282-1288.
66. Tenaillon O, Skurnik D, Picard B, Denamur E. 2010. The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8: 207-217.
67. Touchon M, Rocha EPC. 2010. The small, slow and specialized CRISPR and anti-CRISPR of Escherichia and Salmonella. PLoS One 5: E11126.
68. Touchon M, Charpentier S, Clermont O, Rocha EPC, Denamur E, Branger C. 2011. CRISPR distribution within the Escherichia coli species is not suggestive of immunity-Associated diversifying selection. J Bacteriol 193: 2460-2467.
69. Tsai Y-C, Conlan S, Deming C; NISC Comparative Sequencing Program, Segre JA, Kong HH, Korlach J, Oh J. 2016. Resolving the complexity of human skin metagenomes using single-molecule sequencing. MBio 7: E01948-15.
70. Tu Q, He Z, Zhou J. 2014. Strain/species identification in metagenomes using genome-specific markers. Nucleic Acids Res 42: E67.
71. Tyson GW, Banfield JF. 2007. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10: 200-207.
72. Ward DV, Scholz M, Zolfo M, Taft DH, Schibler KR, Tett A, Segata N, Morrow AL. 2016. Metagenomic sequencing with strain-level resolution implicates uropathogenic E. coli in necrotizing enterocolitis and mortality in preterm infants. Cell Rep 14: 2912-2924.
73. Wilm A, Aw PPK, Bertrand D, Yeo GHT, Ong SH, Wong CH, Khor CC, Petric R, Hibberd ML, Nagarajan N. 2012. LoFreq: A sequence-quality aware, ultra- sensitive variant caller for uncovering cell-population heterogeneity from high-Throughput sequencing datasets. Nucleic Acids Res 40: 11189-11201.