Impact of contaminating DNA in whole-genome amplification kits used for metagenomic shotgun sequencing for infection diagnosis

Journal of Clinical Microbiology

Volumn 55, Issue 6, 2017, Pages 1789-1801

  Thoendel, Matthew ^a   Jeraldo, Patricio ^a   Greenwood Quaintance, Kerryl E ^a   Yao, Janet ^a   Chia, Nicholas ^a   Hanssen, Arlen D ^a   Abdel, Matthew P ^a   Patela, Robin ^a  

^a MAYO CLINIC   (United States)

Author keywords

Metagenomics; Prosthetic joint infection; Whole genome amplification

Indexed keywords

BACTERIAL DNA;

ARTICLE; BACTERIUM CULTURE; BACTEROIDES FRAGILIS; BIOFILM; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; CORYNEBACTERIUM STRIATUM; DNA CONTAMINATION; GENE AMPLIFICATION; INTERMETHOD COMPARISON; JOINT PROSTHESIS; METAGENOMIC SHOTGUN SEQUENCING; METAGENOMICS; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS GROUP C; ULTRASOUND; WHOLE GENOME AMPLIFICATION; GENETICS; HUMAN; INFECTION; ISOLATION AND PURIFICATION; MICROBIOLOGY; NUCLEIC ACID AMPLIFICATION; PROCEDURES; PROSTHESES AND ORTHOSES; WHOLE GENOME SEQUENCING;

DNA, BACTERIAL; HUMANS; METAGENOMICS; NUCLEIC ACID AMPLIFICATION TECHNIQUES; PROSTHESES AND IMPLANTS; PROSTHESIS-RELATED INFECTIONS; WHOLE GENOME SEQUENCING;

EID: 85019556084     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.02402-16     Document Type: Article

References (37)

1. Goldberg B, Sichtig H, Geyer C, Ledeboer N, Weinstock GM. 2015. Making the leap from research laboratory to clinic: challenges and opportunities for next-generation sequencing in infectious disease diagnostics. mBio 6:e01888-15. https://doi.org/10.1128/mBio.01888-15.
2. Quan PL, Wagner TA, Briese T, Torgerson TR, Hornig M, Tashmukhamedova A, Firth C, Palacios G, Baisre-De-Leon A, Paddock CD, Hutchison SK, Egholm M, Zaki SR, Goldman JE, Ochs HD, Lipkin WI. 2010. Astrovirus encephalitis in boy with X-linked agammaglobulinemia. Emerg Infect Dis 16:918-925. https://doi.org/10.3201/eid1606.091536.
3. Wilson MR, Naccache SN, Samayoa E, Biagtan M, Bashir H, Yu G, Salamat SM, Somasekar S, Federman S, Miller S, Sokolic R, Garabedian E, Candotti F, Buckley RH, Reed KD, Meyer TL, Seroogy CM, Galloway R, Henderson SL, Gern JE, DeRisi JL, Chiu CY. 2014. Actionable diagnosis of neuroleptospirosis by next-generation sequencing. N Engl J Med 370:2408-2417. https://doi.org/10.1056/NEJMoa1401268.
4. Hoffmann B, Tappe D, Hoper D, Herden C, Boldt A, Mawrin C, Niederstrasser O, Muller T, Jenckel M, van der Grinten E, Lutter C, Abendroth B, Teifke JP, Cadar D, Schmidt-Chanasit J, Ulrich RG, Beer M. 2015. A variegated squirrel bornavirus associated with fatal human encephalitis. N Engl J Med 373:154-162. https://doi.org/10.1056/NEJMoa1415627.
5. Naccache SN, Peggs KS, Mattes FM, Phadke R, Garson JA, Grant P, Samayoa E, Federman S, Miller S, Lunn MP, Gant V, Chiu CY. 2015. Diagnosis of neuroinvasive astrovirus infection in an immunocompromised adult with encephalitis by unbiased next-generation sequencing. Clin Infect Dis 60:919-923. https://doi.org/10.1093/cid/ciu912.
6. Greninger AL, Messacar K, Dunnebacke T, Naccache SN, Federman S, Bouquet J, Mirsky D, Nomura Y, Yagi S, Glaser C, Vollmer M, Press CA, Kleinschmidt-DeMasters BK, Dominguez SR, Chiu CY. 2015. Clinical metagenomic identification of Balamuthia mandrillaris encephalitis and assembly of the draft genome: the continuing case for reference genome sequencing. Genome Med 7:113. https://doi.org/10.1186/s13073-015-0235-2.
7. Thoendel M, Jeraldo P, Greenwood-Quaintance KE, Chia N, Abdel MP, Steckelberg JM, Osmon DR, Patel R. A possible novel prosthetic joint infection pathogen, Mycoplasma salivarium, identified by metagenomic shotgun sequencing. Clin Infect Dis, in press.
8. Gibson MK, Forsberg KJ, Dantas G. 2015. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J 9:207-216. https://doi.org/10.1038/ismej.2014.106.
9. Yang Y, Jiang X, Chai B, Ma L, Li B, Zhang A, Cole JR, Tiedje JM, Zhang T. 2016. ARGs-OAP: online analysis pipeline for antibiotic resistance genes detection from metagenomic data using an integrated structured ARG-database. Bioinformatics 32:2346-2351. https://doi.org/10.1093/bioinformatics/btw136.
10. Scholz M, Ward DV, Pasolli E, Tolio T, Zolfo M, Asnicar F, Truong DT, Tett A, Morrow AL, Segata N. 2016. Strain-level microbial epidemiology and population genomics from shotgun metagenomics. Nat Methods 13:435-438. https://doi.org/10.1038/nmeth.3802.
11. Jeraldo P, Hernandez A, Nielsen HB, Chen X, White BA, Goldenfeld N, Nelson H, Alhquist D, Boardman L, Chia N. 2016. Capturing one of the human gut microbiome's most wanted: reconstructing the genome of a novel butyrate-producing, clostridial scavenger from metagenomic sequence data. Front Microbiol 7:783. https://doi.org/10.3389/fmicb.2016.00783.
12. Yergeau E, Masson L, Elias M, Xiang S, Madey E, Huang H, Brooks B, Beaudette LA. 2016. Comparison of methods to identify pathogens and associated virulence functional genes in biosolids from two different wastewater treatment facilities in Canada. PLoS One 11:e0153554. https://doi.org/10.1371/journal.pone.0153554.
13. Utturkar SM, Cude WN, Robeson MS, II, Yang ZK, Klingeman DM, Land ML, Allman SL, Lu TS, Brown SD, Schadt CW, Podar M, Doktycz MJ, Pelletier DA. 2016. Enrichment of root endophytic bacteria from Populus deltoides and single-cell genomics analysis. Appl Environ Microbiol 82:5698-5708. https://doi.org/10.1128/AEM.01285-16.
14. Court CM, Ankeny JS, Sho S, Hou S, Li Q, Hsieh C, Song M, Liao X, Rochefort MM, Wainberg Z, Graeber TG, Tseng HR, Tomlinson JS. 2016. Reality of single circulating tumor cell sequencing for molecular diagnostics in pancreatic cancer. J Mol Diagn 18:688-696. https://doi.org/10.1016/j.jmoldx.2016.03.006.
15. Capal P, Blavet N, Vrana J, Kubalakova M, Dolezel J. 2015. Multiple displacement amplification of the DNA from single flow-sorted plant chromosome. Plant J 84:838-844. https://doi.org/10.1111/tpj.13035.
16. Prado-Alvarez M, Couraleau Y, Chollet B, Tourbiez D, Arzul I. 2015. Whole-genome amplification: a useful approach to characterize new genes in unculturable protozoan parasites such as Bonamia exitiosa. Parasitology 142:1523-1534. https://doi.org/10.1017/S0031182015000967.
17. Rinke C, Lee J, Nath N, Goudeau D, Thompson B, Poulton N, Dmitrieff E, Malmstrom R, Stepanauskas R, Woyke T. 2014. Obtaining genomes from uncultivated environmental microorganisms using FACS-based single-cell genomics. Nat Protoc 9:1038-1048. https://doi.org/10.1038/nprot.2014.067.
18. Dean FB, Hosono S, Fang L, Wu X, Faruqi AF, Bray-Ward P, Sun Z, Zong Q, Du Y, Du J, Driscoll M, Song W, Kingsmore SF, Egholm M, Lasken RS. 2002. Comprehensive human genome amplification using multiple displacement amplification. Proc Natl Acad Sci U S A 99:5261-5266. https://doi.org/10.1073/pnas.082089499.
19. de Bourcy CF, De Vlaminck I, Kanbar JN, Wang J, Gawad C, Quake SR. 2014. A quantitative comparison of single-cell whole genome amplification methods. PLoS One 9:e105585. https://doi.org/10.1371/journal.pone.0105585.
20. Probst AJ, Weinmaier T, DeSantis TZ, Santo Domingo JW, Ashbolt N. 2015. New perspectives on microbial community distortion after whole-genome amplification. PLoS One 10:e0124158. https://doi.org/10.1371/journal.pone.0124158.
21. Direito SO, Zaura E, Little M, Ehrenfreund P, Roling WF. 2014. Systematic evaluation of bias in microbial community profiles induced by whole genome amplification. Environ Microbiol 16:643-657. https://doi.org/10.1111/1462-2920.12365.
22. Yilmaz S, Allgaier M, Hugenholtz P. 2010. Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat Methods 7:943-944. https://doi.org/10.1038/nmeth1210-943.
23. Raghunathan A, Ferguson HR, Jr, Bornarth CJ, Song W, Driscoll M, Lasken RS. 2005. Genomic DNA amplification from a single bacterium. Appl Environ Microbiol 71:3342-3347. https://doi.org/10.1128/AEM.71.6.3342-3347.2005.
24. Blainey PC, Quake SR. 2011. Digital MDA for enumeration of total nucleic acid contamination. Nucleic Acids Res 39:e19. https://doi.org/10.1093/nar/gkq1074.
25. Tande AJ, Patel R. 2014. Prosthetic joint infection. Clin Microbiol Rev 27:302-345. https://doi.org/10.1128/CMR.00111-13.
26. Thoendel M, Jeraldo PR, Greenwood-Quaintance KE, Yao JZ, Chia N, Hanssen AD, Abdel MP, Patel R. 2016. Comparison of microbial DNA enrichment tools for metagenomic whole genome sequencing. J Microbiol Methods 127:141-145. https://doi.org/10.1016/j.mimet.2016.05.022.
27. 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. https://doi.org/10.1186/s12915-014-0087-z.
28. Bukowska-Osko I, Perlejewski K, Nakamura S, Motooka D, Stokowy T, Kosinska J, Popiel M, Ploski R, Horban A, Lipowski D, Caraballo Cortes K, Pawelczyk A, Demkow U, Stepien A, Radkowski M, Laskus T. 2017. Sensitivity of next-generation sequencing metagenomic analysis for detection of RNA and DNA viruses in cerebrospinal fluid: the confounding effect of background contamination. Adv Exp Med Biol 944:53-62. https://doi.org/10.1007/5584-2016-138.
29. Perlejewski K, Bukowska-Osko I, Nakamura S, Motooka D, Stokowy T, Ploski R, Rydzanicz M, Zakrzewska-Pniewska B, Podlecka-Pietowska A, Nojszewska M, Gogol A, Caraballo Cortes K, Demkow U, Stepien A, Laskus T, Radkowski M. 2016. Metagenomic analysis of cerebrospinal fluid from patients with multiple sclerosis. Adv Exp Med Biol 935:89-98. https://doi.org/10.1007/5584-2016-25.
30. Ames SK, Hysom DA, Gardner SN, Lloyd GS, Gokhale MB, Allen JE. 2013. Scalable metagenomic taxonomy classification using a reference genome database. Bioinformatics 29:2253-2260. https://doi.org/10.1093/bioinformatics/btt389.
31. Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G, Pasolli E, Tett A, Huttenhower C, Segata N. 2015. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 12:902-903. https://doi.org/10.1038/nmeth.3589.
32. Ames SK, Gardner SN, Marti JM, Slezak TR, Gokhale MB, Allen JE. 2015. Using populations of human and microbial genomes for organism detection in metagenomes. Genome Res 25:1056-1067. https://doi.org/10.1101/gr.184879.114.
33. Marcy Y, Ishoey T, Lasken RS, Stockwell TB, Walenz BP, Halpern AL, Beeson KY, Goldberg SM, Quake SR. 2007. Nanoliter reactors improve multiple displacement amplification of genomes from single cells. PLoS Genet 3:1702-1708.
34. Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK, Osmon DR, Mandrekar JN, Cockerill FR, Steckelberg JM, Greenleaf JF, Patel R. 2007. Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 357:654-663. https://doi.org/10.1056/NEJMoa061588.
35. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. https://doi.org/10.1093/bioinformatics/btu170.
36. Chu J, Sadeghi S, Raymond A, Jackman SD, Nip KM, Mar R, Mohamadi H, Butterfield YS, Robertson AG, Birol I. 2014. BioBloom tools: fast, accurate and memory-efficient host species sequence screening using bloom filters. Bioinformatics 30:3402-3404. https://doi.org/10.1093/bioinformatics/btu558.
37. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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. https://doi.org/10.1038/nmeth.f.303.