Viruses in a 14th-century coprolite

Applied and Environmental Microbiology

Volumn 80, Issue 9, 2014, Pages 2648-2655

  Appelt, Sandra ^a   Fancello, Laura ^a   Le Bailly, Matthieu ^b   Raoult, Didier ^a   Drancourt, Michel ^a   Desnues, Christelle ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITÉ DE FRANCHE COMTÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA SEQUENCES; METABOLISM; POLYMERASE CHAIN REACTION;

ANTIBIOTIC RESISTANCE; ARCHAEA; FECAL MATERIALS; METABOLIC FUNCTION; METAGENOMES; METAGENOMICS; MICROBIOTAS; MIDDLE AGES;

VIRUSES;

BACTERIOPHAGE; BELGIUM; CLASSIFICATION; FECES; FOSSIL; GENETICS; HISTORY; HUMAN; ISOLATION AND PURIFICATION; METAGENOMICS; MICROFLORA; MOLECULAR GENETICS; PHYLOGENY; ULTRASTRUCTURE; VIROLOGY; VIRUS;

BACTERIOPHAGES; BELGIUM; FECES; FOSSILS; HISTORY, MEDIEVAL; HUMANS; METAGENOMICS; MICROBIOTA; MOLECULAR SEQUENCE DATA; PHYLOGENY; VIRUSES;

EID: 84898645213     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03242-13     Document Type: Article

References (46)

1. 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.
2. Lopez-Bueno A, Tamames J, Velazquez D, Moya A, Quesada A, Alcami A. 2009. High diversity of the viral community from an Antarctic lake. Science 326:858-861. http://dx.doi.org/10.1126/science.1179287.
3. Desnues C, Rodriguez-Brito B, Rayhawk S, Kelley S, Tran T, Haynes M, Liu H, Furlan M, Wegley L, Chau B, Ruan Y, Hall D, Angly FE, Edwards RA, Li L, Thurber RV, Reid RP, Siefert J, Souza V, Valentine DL, Swan BK, Breitbart M, Rohwer F. 2008. Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452: 340-343. http://dx.doi.org/10.1038/nature06735.
4. Kim KH, Chang HW, Nam YD, Roh SW, Kim MS, Sung Y, Jeon CO, Oh HM, Bae JW. 2008. Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl. Environ. Microbiol. 74:5975-5985. http://dx.doi.org/10.1128/AEM.01275-08.
5. Briese T, Paweska JT, McMullan LK, Hutchison SK, Street C, Palacios G, Khristova ML, Weyer J, Swanepoel R, Egholm M, Nichol ST, Lipkin WI. 2009. Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog. 5:e1000455. http://dx.doi.org/10.1371/journal.ppat.1000455.
6. Anderson NG, Gerin JL, Anderson NL. 2003. Global screening for human viral pathogens. Emerg. Infect. Dis. 9:768-774. http://dx.doi.org/10.3201/eid0907.030004.
7. Nakamura S, Yang CS, Sakon N, Ueda M, Tougan T, Yamashita A, Goto N, Takahashi K, Yasunaga T, Ikuta K, Mizutani T, Okamoto Y, Tagami M, Morita R, Maeda N, Kawai J, Hayashizaki Y, Nagai Y, Horii T, Iida T, Nakaya T. 2009. Direct metagenomic detection of viral pathogens in nasal and fecal specimens using an unbiased high-throughput sequencing approach. PLoS One 4:e4219. http://dx.doi.org/10.1371/journal.pone.0004219.
8. 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.
9. Breitbart M, Rohwer F. 2005. Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing. Biotechniques 39:729-736. http://dx.doi.org/10.2144/000112019.
10. 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.
11. 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.
12. Kim MS, Park EJ, Roh SW, Bae JW. 2011. Diversity and abundance of single-stranded DNA viruses in human feces. Appl. Environ. Microbiol. 77:8062-8070. http://dx.doi.org/10.1128/AEM.06331-11.
13. Pääbo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M. 2004. Genetic analyses from ancient DNA. Annu. Rev. Genet. 38:645-679. http://dx.doi.org/10.1146/annurev.genet.37.110801.143214.
14. Willerslev E, Cooper A. 2005. Ancient DNA. Proc. Biol. Sci. 272:3-16. http://dx.doi.org/10.1098/rspb.2004.2813.
15. Drancourt M, Raoult D. 2005. Palaeomicrobiology: current issues and perspectives. Nat. Rev. Microbiol. 3:23-35. http://dx.doi.org/10.1038/nrmicro1063.
16. th century Italian mummy. J. Hyg. Epidemiol. Microbiol. Immunol. 34:227-231.
17. Bedarida S, Dutour O, Buzhilova AP, de Micco P, Biagini P. 2011. Identification of viral DNA (Anelloviridae) in a 200-year-old dental pulp sample (Napoleon's Great Army, Kaliningrad, 1812). Infect. Genet. Evol. 11:358-362. http://dx.doi.org/10.1016/j.meegid.2010.11.007.
18. Biagini P, Theves C, Balaresque P, Geraut A, Cannet C, Keyser C, Nikolaeva D, Gerard P, Duchesne S, Orlando L, Willerslev E, Alekseev AN, de Micco P, Ludes B, Crubezy E. 2012. Variola virus in a 300-yearold Siberian mummy. N. Engl. J. Med. 367:2057-2059. http://dx.doi.org/10.1056/NEJMc1208124.
19. Li HC, Fujiyoshi T, Lou H, Yashiki S, Sonoda S, Cartier L, Nunez L, Munoz I, Horai S, Tajima K. 1999. The presence of ancient human T-cell lymphotropic virus type I provirus DNA in an Andean mummy. Nat. Med. 5:1428-1432. http://dx.doi.org/10.1038/71006.
20. Sonoda S, Li HC, Cartier L, Nunez L, Tajima K. 2000. Ancient HTLV type 1 provirus DNA of Andean mummy. AIDS Res. Hum. Retroviruses 16:1753-1756. http://dx.doi.org/10.1089/08892220050193263.
21. 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.
22. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
23. Angly FE, Willner D, Prieto-Davo 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.
24. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA. 2008. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. http://dx.doi.org/10.1186/1471-2105-9-386.
25. 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.
26. Liu B, Pop M. 2009. ARDB-Antibiotic Resistance Genes Database. Nucleic Acids Res. 37:D443-D447. http://dx.doi.org/10.1093/nar/gkn656.
27. 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. http://dx.doi.org/10.1186/1471-2105-11-119.
28. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. http://dx.doi.org/10.1093/nar/gkh340.
29. Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56:564-577. http://dx.doi.org/10.1080/10635150701472164.
30. Guindon S, Delsuc F, Dufayard JF, Gascuel O. 2009. Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol. 537:113-137. http://dx.doi.org/10.1007/978-1-59745-251-9_6.
31. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-W469. http://dx.doi.org/10.1093/nar/gkn180.
32. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599. http://dx.doi.org/10.1093/molbev/msm092.
33. 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.
34. Kristiansson E, Hugenholtz P, Dalevi D. 2009. ShotgunFunctionalizeR: an R-package for functional comparison of metagenomes. Bioinformatics 25:2737-2738. http://dx.doi.org/10.1093/bioinformatics/btp508.
35. Raoult D, Aboudharam G, Crubezy E, Larrouy G, Ludes B, Drancourt M. 2000. Molecular identification by "suicide PCR" of Yersinia pestis as the agent of medieval black death. Proc. Natl. Acad. Sci. U. S. A. 97:12800-12803. http://dx.doi.org/10.1073/pnas.220225197.
36. Rocha GCd. 2003. Praça das Armas, Namur, Bélgica. Contribuição de um estudo paleoparasitológico. Escola Nacional de Saúde Pública-Fiocruz, Rio de Janeiro, Rio de Janeiro, Brazil.
37. Cooper A, Poinar HN. 2000. Ancient DNA: do it right or not at all. Science 289:1139. http://dx.doi.org/10.1126/science.289.5482.1139b.
38. Hofreiter M, Serre D, Poinar HN, Kuch M, Paabo S. 2001. Ancient DNA. Nat. Rev. Genet. 2:353-359. http://dx.doi.org/10.1038/35072071.
39. Willner D, Furlan M, Haynes M, Schmieder R, Angly FE, Silva J, Tammadoni S, Nosrat B, Conrad D, Rohwer F. 2009. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS One 4:e7370. http://dx.doi.org/10.1371/journal.pone.0007370.
40. Muniesa M, Garcia A, Miro E, Mirelis B, Prats G, Jofre J, Navarro F. 2004. Bacteriophages and diffusion of β-lactamase genes. Emerg. Infect. Dis. 10:1134-1137. http://dx.doi.org/10.3201/eid1006.030472.
41. Colomer-Lluch M, Jofre J, Muniesa M. 2011. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 6:e17549. http://dx.doi.org/10.1371/journal.pone.0017549.
42. Mazaheri Nezhad Fard R, Barton MD, Heuzenroeder MW. 2011. Bacteriophage-mediated transduction of antibiotic resistance in enterococci. Lett. Appl. Microbiol. 52:559-564. http://dx.doi.org/10.1111/j.1472-765X.2011.03043.x.
43. Hall BG, Barlow M. 2004. Evolution of the serine β-lactamases: past, present and future. Drug Resist. Updates 7:111-123. http://dx.doi.org/10.1016/j.drup.2004.02.003.
44. Garau G, Di Guilmi AM, Hall BG. 2005. Structure-based phylogeny of the metallo-β-lactamases. Antimicrob. Agents Chemother. 49:2778-2784. http://dx.doi.org/10.1128/AAC.49.7.2778-2784.2005.
45. Aminov RI, Mackie RI. 2007. Evolution and ecology of antibiotic resistance genes. FEMS Microbiol. Lett. 271:147-161. http://dx.doi.org/10.1111/j.1574-6968.2007.00757.x.
46. D'Costa VM, King CE, Kalan L, Morar M, Sung WW, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD. 2011. Antibiotic resistance is ancient. Nature 477:457-461. http://dx.doi.org/10.1038/nature10388.