Early life dynamics of the human gut virome and bacterial microbiome in infants

Nature Medicine

Volumn 21, Issue 10, 2015, Pages 1228-1234

  Lim, Efrem S ^a   Zhou, Yanjiao ^a,b,c   Zhao, Guoyan ^a   Bauer, Irma K ^a   Droit, Lindsay ^a   Ndao, I Malick ^a   Warner, Barbara B ^a   Tarr, Phillip I ^a   Wang, David ^a   Holtz, Lori R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JACKSON LABORATORY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL FLORA; BACTERIAL STRAIN; BACTERIOPHAGE; BIRTH; CHILD DEVELOPMENT; COHORT ANALYSIS; CONTROLLED STUDY; DYNAMICS; FEMALE; HUMAN; HUMAN EXPERIMENT; INFANT; INTESTINE FLORA; KINETICS; LIFE CYCLE; MICROBIAL COMMUNITY; NORMAL HUMAN; PREDATOR PREY INTERACTION; PRIORITY JOURNAL; TWINS; VIRUS; VIRUS STRAIN; INTESTINE; MICROBIOLOGY; MICROFLORA; VIROLOGY;

COHORT STUDIES; HUMANS; INFANT; INTESTINES; MICROBIOTA;

EID: 84943657766     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3950     Document Type: Article

References (63)

1. Virgin, H. W. The virome in mammalian physiology and disease. Cell 157, 142-150 (2014).
2. Norman, J. M. , Handley, S. A. & Virgin, H. W. Kingdom-agnostic metagenomics and the importance of complete characterization of enteric microbial communities. Gastroenterology 146, 1459-1469 (2014).
3. Qin, N. et al. Alterations of the human gut microbiome in liver cirrhosis. Nature 513, 59-64 (2014).
4. Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260-270 (2012)
5. Littman, D. R. & Pamer, E. G. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe 10, 311-323 (2011).
6. Borody, T. J. & Khoruts, A. Fecal microbiota transplantation and emerging applications. Nat. Rev. Gastroenterol. Hepatol. 9, 88-96 (2012).
7. Gritz, E. C. & Bhandari, V. The human neonatal gut microbiome: a brief review. Front. Pediatr 3, 17 (2015).
8. Koenig, J. E. et al. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA 108 (suppl. 1), 4578-4585 (2011).
9. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222-227 (2012).
10. Subramanian, S. et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510, 417-421 (2014).
11. Bckhed, F. et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690-703 (2015).
12. Dominguez-Bello, M. G. et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA 107, 11971-11975 (2010).
13. La Rosa, P. S. et al. Patterned progression of bacterial populations in the premature infant gut. Proc. Natl. Acad. Sci. USA 111, 12522-12527 (2014).
14. Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480-484 (2009).
15. Walter, J. & Ley, R. The human gut microbiome: ecology and recent evolutionary changes. Annu. Rev. Microbiol. 65, 411-429 (2011).
16. Palmer, C. , Bik, E. M. , DiGiulio, D. B. , Relman, D. A. & Brown, P. O. Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 (2007).
17. Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334-338 (2010).
18. Goodrich, J. K. et al. Human genetics shape the gut microbiome. Cell 159, 789-799 (2014).
19. Oh, J. et al. Biogeography and individuality shape function in the human skin metagenome. Nature 514, 59-64 (2014).
20. De Vlaminck, I. et al. Temporal response of the human virome to immunosuppression and antiviral therapy. Cell 155, 1178-1187 (2013).
21. Bé land, K. et al. Torque Teno virus in children who underwent orthotopic liver transplantation: new insights about a common pathogen. J. Infect. Dis. 209, 247-254 (2014).
22. McElvania TeKippe, E. et al. Increased prevalence of anellovirus in pediatric patients with fever. PLoS ONE 7, e50937 (2012).
23. Li, L. et al. AIDS alters the commensal plasma virome. J. Virol. 87, 10912-10915 (2013).
24. Handley, S. A. et al. Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151, 253-266 (2012).
25. Barton, E. S. et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447, 326-329 (2007).
26. Minot, S. et al. Rapid evolution of the human gut virome. Proc. Natl. Acad. Sci. USA 110, 12450-12455 (2013).
27. Breitbart, M. et al. Metagenomic analyses of an uncultured viral community from human feces. J. Bacteriol. 185, 6220-6223 (2003).
28. Minot, S. et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21, 1616-1625 (2011).
29. Norman, J. M. et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160, 447-460 (2015).
30. Parsons, R. J. , Breitbart, M. , Lomas, M. W. & Carlson, C. A. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6, 273-284 (2012).
31. Hennes, K. P. & Simon, M. Significance of bacteriophages for controlling bacterioplankton growth in a mesotrophic lake. Appl. Environ. Microbiol. 61, 333-340 (1995).
32. Cortez, M. H. & Weitz, J. S. Coevolution can reverse predator-prey cycles. Proc. Natl. Acad. Sci. USA 111, 7486-7491 (2014).
33. Breitbart, M. et al. Viral diversity and dynamics in an infant gut. Res. Microbiol. 159, 367-373 (2008).
34. Kapusinszky, B. , Minor, P. & Delwart, E. Nearly constant shedding of diverse enteric viruses by two healthy infants. J. Clin. Microbiol. 50, 3427-3434 (2012).
35. Finkbeiner, S. R. et al. Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS Pathog. 4, e1000011 (2008).
36. Holtz, L. R. et al. Geographic variation in the eukaryotic virome of human diarrhea. Virology 468-470, 556-564 (2014).
37. Kapoor, A. et al. A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc. Natl. Acad. Sci. USA 105, 20482-20487 (2008).
38. Olszak, T. et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336, 489-493 (2012).
39. Gurnee, E. A. et al. Gut colonization of healthy children and their mothers with pathogenic ciprofloxacin-resistant Escherichia coli. J. Infect. Dis. doi:10. 1093/infdis/jiv279 (2015).
40. Edwards, R. A. & Rohwer, F. Viral metagenomics. Nat. Rev. Microbiol. 3, 504-510 (2005).
41. Dutilh, B. E. et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5, 4498 (2014).
42. Ninomiya, M. , Takahashi, M. , Nishizawa, T. , Shimosegawa, T. & Okamoto, H. Development of PCR assays with nested primers specific for differential detection of three human anelloviruses and early acquisition of dual or triple infection during infancy. J. Clin. Microbiol. 46, 507-514 (2008).
43. Rodriguez-Valera, F. et al. Explaining microbial population genomics through phage predation. Nat. Rev. Microbiol. 7, 828-836 (2009).
44. Thingstad, T. F. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45, 1320-1328 (2000).
45. Kircher, M. , Heyn, P. & Kelso, J. Addressing challenges in the production and analysis of illumina sequencing data. BMC Genomics 12, 382 (2011).
46. Fé lix, M. A. et al. Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol. 9, e1000586 (2011).
47. Aronesty, E. ea-utils: command-line tools for processing biological sequencing data http://code. google. com/p/ea-utils (2011).
48. Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658-1659 (2006).
49. Zhao, G. et al. Identification of novel viruses using VirusHunter-an automated data analysis pipeline. PLoS ONE 8, e78470 (2013).
50. Huson, D. H. , Mitra, S. , Ruscheweyh, H. J. , Weber, N. & Schuster, S. C. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552-1560 (2011).
51. Oksanen, J. F et al. vegan: Community Ecology Package. R package version 2. 0-10 https://cran. r-project. org/web/packages/vegan/index. html (2013).
52. Vázquez-Baeza, Y. , Pirrung, M. , Gonzalez, A. & Knight, R. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2, 16 (2013).
53. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
54. Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649 (2012).
55. Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (2003).
56. Abascal, F. , Zardoya, R. & Posada, D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105 (2005).
57. Darriba, D. , Taboada, G. L. , Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772 (2012).
58. Nix, W. A. et al. Detection of all known parechoviruses by real-time PCR. J. Clin. Microbiol. 46, 2519-2524 (2008).
59. Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380 (2005).
60. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
61. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
62. McDonald, D. et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618 (2012).
63. Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 108 (suppl. 1), 4516-4522 (2011).