VirSorter: Mining viral signal from microbial genomic data

PeerJ

Volumn 2015, Issue 5, 2015, Pages

  Roux, Simon ^a,d   Enault, Francois ^b,c   Hurwitz, Bonnie L ^a   Sullivan, Matthew B ^a,d  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

^c UNIVERSITÉ BLAISE PASCAL   (France)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

Bacteriophage; Metagenomics; Prophage; Single cell amplified genome; Viral metagenomics; Virus

Indexed keywords

VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CAUDOVIRALES; ECOSYSTEM; EVOLUTIONARY ALGORITHM; GENE AMPLIFICATION; GENE SEQUENCE; GENOMIC FRAGMENT; INFORMATION PROCESSING; INOVIRIDAE; MEASUREMENT PRECISION; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIAL GENETICS; NONHUMAN; PREDICTION; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS; SIGNAL DETECTION; SIGNAL TRANSDUCTION; SIMULATION; VIRSORTER; VIRUS DETECTION; VIRUS GENE;

EID: 84930658013     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.985     Document Type: Article

References (59)

1. Akhter S, Aziz RK, Edwards RA. 2012. PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Research 40:1-13 DOI 10.1093/nar/gks406.
2. Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH. 2013. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nature Biotechnology 31:533-538 DOI 10.1038/nbt.2579.
3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25:3389-3402 DOI 10.1093/nar/25.17.3389.
4. Anantharaman K, Duhaime MB, Breier JA, Wendt K, Toner BM, Dick GJ. 2014. Sulfur oxidation genes in diverse deep-sea viruses. Science 344:757-760 DOI 10.3354/meps145269.
5. Boyd EF. 2012. Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions. In: Łobocka M, Szybalski WT, eds. Advances in virus research, vol. 82. Amsterdam: Elsevier, 91-118.
6. Breitbart M, Thompson LR, Suttle CA, Sullivan MB. 2007. Exploring the vast diversity of marine viruses. Oceanography 20:135-139 DOI 10.5670/oceanog.2007.58.
7. Breitbart M, Rohwer F. 2005. Here a virus, there a virus, everywhere the same virus? Trends in Microbiology 13:278-284 DOI 10.1016/j.tim.2005.04.003.
8. Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A, Chaffron S, Coppola L, Cruaud C, de Vargas C, Gasol JM, Gorsky G, Gregory AC, Guidi L, Hingamp P, Iudicone D, Not F, Ogata H, Pesant S, Poulos BT, Schwenck SM, Speich S, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Coordinators TO, Bork P, Bowler C, Karsenti E, Sunagawa S, Wincker P, Sullivan MB. 2015. Patterns and ecological drivers of ocean viral communities. Science 22(348):6237 DOI 10.1126/science.1261498.
9. Brum JR, Sullivan MB. 2015. Rising to the challenge: accelerated pace of discovery transforms marine virology. Nature Reviews Microbiology 13:147-159 DOI 10.1038/nrmicro3404.
10. Busby B, Kristensen DM, Koonin EV. 2013. Contribution of phage-derived genomic islands to the virulence of facultative bacterial pathogens. Environmental Microbiology 15:307-312 DOI 10.1111/j.1462-2920.2012.02886.x.
11. Bush K, Courvalin P, Dantas G, Davies J, Eisenstein B, Huovinen P, Jacoby GA, Kishony R, Kreiswirth BN, Kutter E, Lerner SA, Levy S, Lewis K, Lomovskaya O, Miller JH, Mobashery S, Piddock LJV, Projan S, Thomas CM, Tomasz A, Tulkens PM, Walsh TR, Watson JD, Witkowski J, Witte W, Wright G, Yeh P, Zgurskaya HI. 2011. Tackling antibiotic resistance. Nature Reviews Microbiology 9:894-896 DOI 10.1038/nrmicro2693.
12. Canchaya C, Fournous G, Brüssow H. 2004. The impact of prophages on bacterial chromosomes. Molecular Microbiology 53:9-18 DOI 10.1111/j.1365-2958.2004.04113.x.
13. Casjens S. 2003. Prophages and bacterial genomics: what have we learned so far? Molecular Microbiology 49:277-300 DOI 10.1046/j.1365-2958.2003.03580.x.
14. Delcher AL, Salzberg SL, Phillippy AM. 2003. Using MUMmer to identify similar regions in large sequence sets. Current Protocols in Bioinformatics (online) DOI 10.1002/0471250953.bi1003s00.
15. Eddy SR. 2011. Accelerated Profile HMM Searches. PLoS Computational Biology 7:e1002195 DOI 10.1371/journal.pcbi.1002195.
16. Edwards RA, Rohwer F. 2005. Viral metagenomics. Nature Reviews Microbiology 3:504-510 DOI 10.1038/nrmicro1163.
17. Emerson JB, Thomas BC, Andrade K, Allen EE, Heidelberg KB, Banfield JF. 2012. Metagenomic assembly reveals dynamic viral populations in hypersaline systems. Applied and Environmental Microbiology 78:6309-6320 DOI 10.1128/AEM.01212-12.
18. Enright AJ, Van Dongen S, Ouzounis CA. 2002. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Research 30:1575-1584 DOI 10.1093/nar/30.7.1575.
19. Fouts DE. 2006. Phage Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Research 34:5839-5851 DOI 10.1093/nar/gkl732.
20. Fuhrman JA. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548 DOI 10.1038/21119.
21. Goff SA, Vaughn M, McKay S, Lyons E, Stapleton AE, Gessler D, Matasci N, Wang L, Hanlon M, Lenards A, Muir A, Merchant N, Lowry S, Mock S, Helmke M, Kubach A, Narro M, Hopkins N, Micklos D, Hilgert U, Gonzales M, Jordan C, Skidmore E, Dooley R, Cazes J, McLay R, Lu Z, Pasternak S, Koesterke L, Piel WH, Grene R, Noutsos C, Gendler K, Feng X, Tang C, Lent M, Kim S-J, Kvilekval K, Manjunath BS, Tannen V, Stamatakis A, Sanderson M, Welch SM, Cranston KA, Soltis P, Soltis D, O'Meara B, Ane C, Brutnell T, Kleibenstein DJ, White JW, Leebens-Mack J, Donoghue MJ, Spalding EP, Vision TJ, Myers CR, Lowenthal D, Enquist BJ, Boyle B, Akoglu A, Andrews G, Ram S, Ware D, Stein L, Stanzione D. 2011. The iplant collaborative: cyberinfrastructure for plant biology. Frontiers in Plant Science 2:34 DOI 10.3389/fpls.2011.00034.
22. Hurwitz BL, Brum JR, Sullivan MB. 2015. Depth-stratified functional and taxonomic niche specialization in the core and "flexible" Pacific Ocean Virome. The ISME Journal 9:472-484 DOI 10.1038/ismej.2014.143.
23. Hurwitz BL, Hallam SJ, Sullivan MB. 2013. Metabolic reprogramming by viruses in the sunlit and dark ocean. Genome Biology 14:R123 DOI 10.1186/gb-2013-14-11-r123.
24. Jia B, Xuan L, Cai K, Hu Z, Ma L, Wei C. 2013. NeSSM: a next-generation sequencing simulator for metagenomics. PLoS ONE 8:e75448 DOI 10.1371/journal.pone.0075448.
25. Kamke J, Sczyrba A, Ivanova N. 2013. Single-cell genomics reveals complex carbohydrate degradation patterns in poribacterial symbionts of marine sponges. The ISME Journal 7:2287-2300 DOI 10.1038/ismej.2013.111.
26. Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ, Coe A, Ding H, Marttinen P, Malmstrom RR, Stocker R, Follows MJ, Stepanauskas R, Chisholm SW, Biller J. 2014. Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416-420 DOI 10.1126/science.1248575.
27. Koonin EV, Senkevich TG, Dolja VV. 2006. The ancient Virus World and evolution of cells. Biology Direct 1:29 DOI 10.1186/1745-6150-1-29.
28. Labonté JM, Swan BK, Poulos BT, Luo H, Koren S, Hallam SJ, Sullivan MB, Woyke T, Wommack EK, Stepanauskas R. 2015. Single cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. The ISME Journal Epub ahead of print 7 April 2015 DOI 10.1038/ismej.2015.48.
29. Letarov A, Kulikov E. 2009. The bacteriophages in human- and animal body-associated microbial communities. Journal of Applied Microbiology 107:1-13 DOI 10.1111/j.1365-2672.2009.04143.x.
30. Lima-Mendez G, Van Helden J, Toussaint A, Leplae R. 2008. Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 24:863-865 DOI 10.1093/bioinformatics/btn043.
31. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW. 2005. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86-89 DOI 10.1038/nature04111.
32. Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD. 2013. Rapid evolution of the human gut virome. Proceedings of the National Academy of Sciences of the United States of America 110:12450-12455 DOI 10.1073/pnas.1300833110.
33. Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfield JF, Allen EE. 2012. De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. The ISME Journal 6:81-93 DOI 10.1038/ismej.2011.78.
34. Nobrega FL, Costa AR, Kluskens LD, Azeredo J. 2015. Revisiting phage therapy: new applications for old resources. Trends in Microbiology 23:185-191 DOI 10.1016/j.tim.2015.01.006.
35. Noguchi H, Taniguchi T, Itoh T. 2008. MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Research 15:387-396 DOI 10.1093/dnares/dsn027.
36. 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 DOI 10.1093/bioinformatics/bts174.
37. Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C, White RA, Loomer P, Armitage GC, Relman DA. 2011. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. The ISME Journal 6:915-926 DOI 10.1038/ismej.2011.169.
38. Rappé MS, Giovannoni SJ. 2003. The uncultured microbial majority. Annual Review of Microbiology 57:369-394 DOI 10.1146/annurev.micro.57.030502.090759.
39. 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 DOI 10.1038/nature09199.
40. Reyes A, Semenkovich NP, Whiteson K, Rohwer F, Gordon JI. 2012. Going viral: next-generation sequencing applied to phage populations in the human gut. Nature Reviews Microbiology 10:607-617 DOI 10.1038/nrmicro2853.
41. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, LiuW-T, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T. 2013. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431-437 DOI 10.1038/nature12352.
42. Rodriguez-Valera F, Martin-Cuadrado A-B, Rodriguez-Brito B, Pasić L, Thingstad TF, Rohwer F, Mira A. 2009. Explaining microbial population genomics through phage predation. Nature Reviews Microbiology 7:828-836 DOI 10.1038/nrmicro2235.
43. Rohwer F, Thurber RV. 2009. Viruses manipulate the marine environment. Nature 459:207-212 DOI 10.1038/nature08060.
44. 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 Biology 3:130160 DOI 10.1098/rsob.130160.
45. Roux S, Tournayre J, Mahul A, Debroas D, Enault F. 2014a. Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinformatics 15:1-12 DOI 10.1186/1471-2105-15-76.
46. Roux S, Hawley AK, Torres Beltran M, Scofield M, Schwientek P, Stepanauskas R, Woyke T, Hallam SJ, Sullivan MB. 2014b. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta- genomics. eLife 3:1-20 DOI 10.7554/eLife.03125.
47. Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F, Atamna-Ismaeel N, Pinter RY, Partensky F, Koonin EV, Wolf YI, Nelson N, Béjà O. 2009. Photosystem I gene cassettes are present in marine virus genomes. Nature 461:258-262 DOI 10.1038/nature08284.
48. Sharon I, Battchikova N, Aro E-M, Giglione C, Meinnel T, Glaser F, Pinter RY, Breitbart M, Rohwer F, Béjà O. 2011. Comparative metagenomics of microbial traits within oceanic viral communities. The ISME journal 5:1178-1190 DOI 10.1038/ismej.2011.2.
49. Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW. 2006. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biology 4:e234 DOI 10.1371/journal.pbio.0040234.
50. Suttle C. 2002. Cyanophages and their role in the ecology of cyanobacteria. In: Whitton BA, Potts M, eds. The ecology of cyanobacteria. Dordrecht: Springer, 564-584.
51. Suttle CA. 2007. Marine viruses-major players in the global ecosystem. Nature Reviews Microbiology 5:801-812 DOI 10.1038/nrmicro1750.
52. Swan BK, Martinez-Garcia M, Preston CM, Sczyrba A, Woyke T, Lamy D, Reinthaler T, Poulton NJ, Masland EDP, Gomez ML, Sieracki ME, DeLong EF, Herndl GJ, Stepanauskas R. 2011. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333:1296-1300 DOI 10.1126/science.1203690.
53. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J, Chisholm SW. 2011. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proceedings of the National Academy of Sciences of the United States of America 108:E757-E764 DOI 10.1073/pnas.1102164108.
54. Waldor MK, Mekalanos JJ. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910-1914 DOI 10.1126/science.272.5270.1910.
55. Weinbauer MG. 2004. Ecology of prokaryotic viruses. FEMS Microbiology Reviews 28:127-181 DOI 10.1016/j.femsre.2003.08.001.
56. Winstanley C, Langille MGI, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C, Sanschagrin F, Thomson NR, Winsor GL, Quail MA, Lennard N, Bignell A, Clarke L, Seeger K, Saunders D, Harris D, Parkhill J, Hancock REW, Brinkman FSL, Levesque RC. 2009. Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa. Genome Research 19:12-23 DOI 10.1101/gr.086082.108.
57. Wommack KE, Colwell RR. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiology and Molecular Biology Reviews 64:69-114 DOI 10.1128/MMBR.64.1.69-114.2000.
58. Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki ME, Wilson WH, Yang EC, Duffy S, Bhattacharya D. 2011. Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332:714-717 DOI 10.1126/science.1203163.
59. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. 2011. PHAST: a fast phage search tool. Nucleic Acids Research 39:W347-W352 DOI 10.1093/nar/gkr485.