The human skin double-stranded DNA virome: Topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome

mBio

Volumn 6, Issue 5, 2015, Pages

  Hannigan, Geoffrey D ^a   Meisel, Jacquelyn S ^a   Tyldsley, Amanda S ^a   Zheng, Qi ^a   Hodkinson, Brendan P ^a   Sanmiguel, Adam J ^a   Minot, Samuel ^a   Bushman, Frederic D ^a   Grice, Elizabeth A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BACTERIOPHAGE; CONTROLLED STUDY; DNA SEQUENCE; DNA TRANSCRIPTION; DOUBLE-STRANDED DNA VIRUS; FEMALE; GENE LOCATION; HUMAN; MALE; MICROBIAL DIVERSITY; MYOVIRIDAE; NONHUMAN; PAPILLOMAVIRIDAE; POPULATION ABUNDANCE; POXVIRIDAE; PRIORITY JOURNAL; SIPHOVIRIDAE; VIRUS CELL INTERACTION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS VIRULENCE; WART VIRUS; BACTERIUM; BIOLOGY; CLASSIFICATION; GENETIC VARIATION; GENETICS; ISOLATION AND PURIFICATION; METAGENOMICS; MICROFLORA; SKIN; SPATIOTEMPORAL ANALYSIS; VIROLOGY;

DNA; DNA VIRUS; VIRUS DNA;

BACTERIA; BACTERIOPHAGES; COMPUTATIONAL BIOLOGY; DNA; DNA VIRUSES; DNA, VIRAL; GENETIC VARIATION; HUMANS; METAGENOMICS; MICROBIOTA; SEQUENCE ANALYSIS, DNA; SKIN; SPATIO-TEMPORAL ANALYSIS;

EID: 84946600312     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01578-15     Document Type: Article

References (71)

1. Hannigan GD, Grice EA. 2013. Microbial ecology of the skin in the era of metagenomics and molecular microbiology. Cold Spring Harb Perspect Med 3:a015362. http://dx.doi.org/10.1101/cshperspect.a015362.
2. Oh J, Byrd AL, Deming C, Conlan S, Program NCS, Kong HH, Segre JA. 2014. Biogeography and individuality shape function in the human skin metagenome. Nature 514:59-64. http://dx.doi.org/10.1038/nature13786.
3. Bohannan BJM, Lenski RE. 1997. Effect of resource enrichment on a chemostat community of bacteria and bacteriophage. Ecology 78:2303-2315. http://dx.doi.org/10.1890/0012-9658(1997)078[2303:EOREOA]2.0.CO;2.
4. Rodriguez-Brito B, Li L, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, Edwards R, Felts B, Haynes M, Liu H, Lipson D, Mahaffy J, Martin-Cuadrado AB, Mira A, Nulton J, Pašic´ L, Rayhawk S, Rodriguez-Mueller J, Rodriguez-Valera F, Salamon P, Srinagesh S, Thingstad TF, Tran T, Thurber RV, Willner D, Youle M, Rohwer F. 2010. Viral and microbial community dynamics in four aquatic environments. ISME J 4:739-751. http://dx.doi.org/10.1038/ismej.2010.1.
5. Tyson GW, Banfield JF. 2008. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10: 200-207.
6. Oliver KM, Degnan PH, Hunter MS, Moran NA. 2009. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992-994. http://dx.doi.org/10.1126/science.1174463.
7. Tyler JS, Beeri K, Reynolds JL, Alteri CJ, Skinner KG, Friedman JH, Eaton KA, Friedman DI. 2013. Prophage induction is enhanced and required for renal disease and lethality in an EHEC mouse model. PLoS Pathog 9:e1003236. http://dx.doi.org/10.1371/journal.ppat.1003236.
8. Brussow H, Canchaya C, Hardt W-. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560-602. http://dx.doi.org/10.1128/MMBR.68.3.560-602.2004.
9. Hurwitz BL, Brum JR, Sullivan MB. 2015. Depth-stratified functional and taxonomic niche specialization in the “core” and “flexible” Pacific Ocean virome. ISME J 9:472-484 http://dx.doi.org/10.1038/ismej.2014.143.
10. Modi SR, Lee HH, Spina CS, Collins JJ. 2013. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219-222. http://dx.doi.org/10.1038/nature12212.
11. Foulongne V, Sauvage V, Hebert C, Dereure O, Cheval J, Gouilh MA, Pariente K, Segondy M, Burguière A, Manuguerra J, Caro V, Eloit M. 2012. Human skin microbiota: high diversity ofDNAviruses identified on the human skin by high throughput sequencing. PLoS One 7:e38499. http://dx.doi.org/10.1371/journal.pone.0038499.
12. Wylie KM, Mihindukulasuriya KA, Zhou Y, Sodergren E, Storch GA, Weinstock GM. 2014. Metagenomic analysis of double-stranded DNA viruses in healthy adults. BMC Biol 12:71. http://dx.doi.org/10.1186/s12915-014-0071-7.
13. Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA, Jacobs-Sera D, Falbo J, Gross J, Pannunzio NR, Brucker W, Kumar V, Kandasamy J, Keenan L, Bardarov S, Kriakov J, Lawrence JG, Jacobs WR, Jr., Hendrix RW, Hatfull GF. 2003. Origins of highly mosaic mycobacteriophage genomes. Cell 113:171-182. http://dx.doi.org/10.1016/S0092-8674(03)00233-2.
14. Breitbart M. 2012. Marine viruses: truth or dare. Annu Rev Mar Sci 4:425-448. http://dx.doi.org/10.1146/annurev-marine-120709-142805.
15. Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F. 2009. Laboratory procedures to generate viral metagenomes. Nat Protoc 4:470-483. http://dx.doi.org/10.1038/nprot.2009.10.
16. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI. 2010. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334-338. http://dx.doi.org/10.1038/nature09199.
17. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD. 2011. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 21:1616-1625. http://dx.doi.org/10.1101/gr.122705.111.
18. Breitbart M, Haynes M, Kelley S, Angly F, Edwards RA, Felts B, Mahaffy JM, Mueller J, Nulton J, Rayhawk S, Rodriguez-Brito B, Salamon P, Rohwer F. 2008. Viral diversity and dynamics in an infant gut. Res Microbiol 159:367-373. http://dx.doi.org/10.1016/j.resmic.2008.04.006.
19. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P, Rohwer F. 2003. Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185:6220-6223. http://dx.doi.org/10.1128/JB.185.20.6220-6223.2003.
20. Wommack KE, Bhavsar J, Ravel J. 2008. Metagenomics: read length matters. Appl Environ Microbiol 74:1453-1463. http://dx.doi.org/10.1128/AEM.02181-07.
21. Roux S, Krupovic M, Debroas D, Forterre P, Enault F. 2013. Assessment of viral community functional potential from viral metagenomes may be hampered by contamination with cellular sequences. Open Biol 3:130160. http://dx.doi.org/10.1098/rsob.130160.
22. Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD. 2013. Rapid evolution of the human gut virome. Proc Natl Acad Sci U S A 110:12450-12455. http://dx.doi.org/10.1073/pnas.1300833110.
23. Oh J, Byrd AL, Deming C, Conlan S, Program NCS, Kong HH, Segre JA. 2014. Biogeography and individuality shape function in the human skin metagenome. Nature 514:59-64. http://dx.doi.org/10.1038/nature13786.
24. Gutiérrez D, Adriaenssens EM, Martínez B, Rodríguez A, Lavigne R, Kropinski AM, García P. 2014. Three proposed new bacteriophage genera of staphylococcal phages: “3alikevirus,” “77likevirus” and “Phietalikevirus.” Arch Virol 159:389-398. http://dx.doi.org/10.1007/s00705-013-1833-1.
25. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C. 2012. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 9:811-814. http://dx.doi.org/10.1038/nmeth.2066.
26. Segata N, Boernigen D, Tickle TL, Morgan XC, Garrett WS, Huttenhower C. 2013. Computational meta’omics for microbial community studies. Mol Syst Biol 9:666. http://dx.doi.org/10.1038/msb.2013.22.
27. Huson DH, Mitra S, Ruscheweyh H-, Weber N, Schuster SC. 2011. Integrative analysis of environmental sequences using MEGAN4. Genome Res 21:1552-1560. http://dx.doi.org/10.1101/gr.120618.111.
28. Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207-214. http://dx.doi.org/10.1038/nature11234.
29. Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, Schoenfeld D, Nomicos E, Park M, Becker J, Benjamin B, Blakesley R, Bouffard G, Brooks S, Coleman H, Dekhtyar M, Gregory M, Guan X, Gupta J, Han J, Hargrove A, Ho SL, Johnson T, Legaspi R, Lovett S, Maduro Q, Masiello C, Maskeri B, McDowell J, Montemayor C, Mullikin J, Park M, Riebow N, Schandler K, Schmidt B, Sison C, Stantripop M, Thomas J, Thomas P, Vemulapalli M, Young A, Kong HH, Segre JA. 2013. Topographic diversity of fungal and bacterial communities in human skin. Nature 498:367-370 http://dx.doi.org/10.1038/nature12171.
30. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, NISC Comparative Sequencing Program, Bouffard GG, Blakesley RW, Murray PR, Green ED, Turner ML, Segre JA. 2009. Topographical and temporal diversity of the human skin microbiome. Science 324: 1190-1192. http://dx.doi.org/10.1126/science.1171700.
31. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, Chan AM, Haynes M, Kelley S, Liu H, Mahaffy JM, Mueller JE, Nulton J, Olson R, Parsons R, Rayhawk S, Suttle CA, Rohwer F. 2006. The marine viromes of four oceanic regions. PLoS Biol 4:e368. http://dx.doi.org/10.1371/journal.pbio.0040368.
32. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. 2009. Bacterial community variation in human body habitats across space and time. Science 326:1694-1697. http://dx.doi.org/10.1126/science.1177486.
33. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, Bouffard GG, Blakesley RW, Murray PR, Green ED, Turner ML, Segre JA. 2009. Topographical and temporal diversity of the human skin microbiome. Science 324:1190-1192. http://dx.doi.org/10.1126/science.1171700.
34. Leplae R, Hebrant A, Wodak SJ, Toussaint A. 2004. ACLAME: a CLAssification of mobile genetic elements. Nucleic Acids Res 32:D45-D49. http://dx.doi.org/10.1093/nar/gkh084.
35. Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27-30. http://dx.doi.org/10.1093/nar/28.1.27.
36. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O, Kelley ST, Methé B, Schloss PD, Gevers D, Mitreva M, Huttenhower C. 2012. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 8:e1002358. http://dx.doi.org/10.1371/journal.pcbi.1002358.
37. Schloss PD, Handelsman J. 2008. A statistical toolbox for metagenomics: assessing functional diversity in microbial communities. BMC Bioinformatics 9:34. http://dx.doi.org/10.1186/1471-2105-9-34.
38. Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C, White RA III, Loomer P, Armitage GC, Relman DA. 2012. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J 6:915-926. http://dx.doi.org/10.1038/ismej.2011.169.
39. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Bhullar K, Canova MJ, De Pascale G, Ejim L, Kalan L, King AM, Koteva K, Morar M, Mulvey MR, O’Brien JS, Pawlowski AC, Piddock LJV, Spanogiannopoulos P, Sutherland AD, Tang I, Taylor PL, Thaker M, Wang W, Yan M, Yu T, Wright GD. 2013. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57:3348-3357. http://dx.doi.org/10.1128/AAC.00419-13.
40. Brötz E, Kulik A, Vikineswary S, Lim CT, Tan GY, Zinecker H, Imhoff JF, Paululat T, Fiedler HP. 2011. Phenelfamycins G and H, new elfamycin-type antibiotics produced by Streptomyces albospinus Acta 3619. J Antibiot 64:257-266. http://dx.doi.org/10.1038/ja.2010.170.
41. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q. 2005. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33: D325-D328. http://dx.doi.org/10.1093/nar/gki008.
42. Soffer N, Zaneveld J, Vega Thurber R. 2015. Phage-bacteria network analysis and its implication for the understanding of coral disease. Environ Microbiol 17:1203-1218. http://dx.doi.org/10.1111/1462-2920.12553.
43. Barabasi A, Albert R. 1999. Emergence of scaling in random networks. Science 286:509-512. http://dx.doi.org/10.1126/science.286.5439.509.
44. Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X. 2010. Functional molecular ecological networks. mBio 1:e00169. http://dx.doi.org/10.1128/mBio.00169-10.
45. Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, Chow CT, Sachdeva R, Jones AC, Schwalbach MS, Rose JM, Hewson I, Patel A, Sun F, Caron DA, Fuhrman JA. 2011. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J 5:1414-1425. http://dx.doi.org/10.1038/ismej.2011.24.
46. Marinelli LJ, Fitz-Gibbon S, Hayes C, Bowman C, Inkeles M, Loncaric A, Russell DA, Jacobs-Sera D, Cokus S, Pellegrini M, Kim J, Miller JF, Hatfull GF, Modlin RL. 2012. Propionibacterium acnes bacteriophages display limited genetic diversity and broad killing activity against bacterial skin isolates. mBio 3:e00279-12. http://dx.doi.org/10.1128/mBio.00279-12.
47. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW. 2014. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87. http://dx.doi.org/10.1186/s12915-014-0087-z.
48. Hannigan GD, Hodkinson BP, McGinnis K, Tyldsley AS, Anari JB, Horan AD, Grice EA, Mehta S. 2014. Culture-independent pilot study of microbiota colonizing open fractures and association with severity, mechanism, location, and complication from presentation to early outpatient follow-up. J Orthop Res 32:597-605. http://dx.doi.org/10.1002/jor.22578.
49. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST_: architecture and applications. BMC Bioinformatics 10:421. http://dx.doi.org/10.1186/1471-2105-10-421.
50. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with bowtie 2. Nat Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
51. Schmieder R, Edwards R. 2011. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS One 6:e17288. http://dx.doi.org/10.1371/journal.pone.0017288.
52. Boisvert S, Raymond F, Godzaridis É, Laviolette F, Corbeil J. 2012. Ray Meta: scalable de novo metagenome assembly and profiling. Genome Biol 13:R122. http://dx.doi.org/10.1186/gb-2012-13-12-r122.
53. UniProt C. 2014. Activities at the universal protein resource (UniProt). Nucleic Acids Res 42:D191-D198. http://dx.doi.org/10.1093/nar/gkt1140.
54. Angly F, Rodriguez-Brito B, Bangor D, McNairnie P, Breitbart M, Salamon P, Felts B, Nulton J, Mahaffy J, Rohwer F. 2005. PHACCS, an online tool for estimating the structure and diversity of uncultured viral communities using metagenomic information. BMCBioinformatics 6:41. http://dx.doi.org/10.1186/1471-2105-6-41.
55. Angly FE, Willner D, Prieto-Davó A, Edwards RA, Schmieder R, Vega-Thurber R, Antonopoulos DA, Barott K, Cottrell MT, Desnues C, Dinsdale EA, Furlan M, Haynes M, Henn MR, Hu Y, Kirchman DL, McDole T, McPherson JD, Meyer F, Miller RM, Mundt E, Naviaux RK, Rodriguez-Mueller B, Stevens R, Wegley L, Zhang L, Zhu B, Rohwer F. 2009. The GAAS metagenomic tool and its estimations of viral and microbial average genome size in four major biomes. PLOS Comput Biol 5:e1000593. http://dx.doi.org/10.1371/journal.pcbi.1000593.
56. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H. 2014. Vegan: community ecology package. R package version 2.2-0. http://CRAN.Rproject. org/package_vegan.
57. Wickham H. 2009. ggplot2: elegant graphics for data analysis. Springer, New York, NY.
58. McGill R, Tukey JW, Larsen WA. 1978. Variations of box plots. Am Stat 32:12-16. http://dx.doi.org/10.1080/00031305.1978.10479236.
59. Zheng Q, Wang X-. 2008. GOEAST: a web-based software toolkit for gene ontology enrichment analysis. Nucleic Acids Res 36:W358-W363. http://dx.doi.org/10.1093/nar/gkn276.
60. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with glimmer. Bioinformatics 23:673-679. http://dx.doi.org/10.1093/bioinformatics/btm009.
61. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. http://dx.doi.org/10.1093/bioinformatics/btq461.
62. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. http://dx.doi.org/10.1038/nmeth.f.303.
63. Chen L, Xiong Z, Sun L, Yang J, Jin Q. 2012. VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40:D641-D645. http://dx.doi.org/10.1093/nar/gkr989.
64. 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. http://dx.doi.org/10.1093/bioinformatics/bts199.
65. Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C. 2012. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8:e1002606. http://dx.doi.org/10.1371/journal.pcbi.1002606.
66. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504. http://dx.doi.org/10.1101/gr.1239303.
67. Sarkar SK, Chang C. 1997. The Simes method for multiple hypothesis testing with positively dependent test statistics. J Am Stat Assoc 92: 1601-1608. http://dx.doi.org/10.1080/01621459.1997.10473682.
68. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodological 57:289-300.
69. Assenov Y, Ramirez F, Schelhorn S-, Lengauer T, Albrecht M. 2008. Computing topological parameters of biological networks. Bioinformatics 24:282-284. http://dx.doi.org/10.1093/bioinformatics/btm554.
70. Edgar RC. 2007. PILER-CR: fast and accurate identification of CRISPR repeats. BMC Bioinformatics 8:18. http://dx.doi.org/10.1186/1471-2105-8-18.
71. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res 19:1639-1645. http://dx.doi.org/10.1101/gr.092759.109.