Use of 16S rRNA gene for identification of a broad range of clinically relevant bacterial pathogens

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Srinivasan, Ramya ^a   Karaoz, Ulas ^b   Volegova, Marina ^d   MacKichan, Joanna ^f   Kato Maeda, Midori ^e   Miller, Steve ^c   Nadarajan, Rohan ^c   Brodie, Eoin L ^b   Lynch, Susan V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e SAN FRANCISCO GENERAL HOSPITAL   (United States)

^f VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

16S RRNA GENE; ACINETOBACTER BAUMANNII; ALPHA HEMOLYTIC STREPTOCOCCUS; ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BAYESIAN LEARNING; BORDETELLA PERTUSSIS; BURKHOLDERIA; BURKHOLDERIA AMBIFARIA; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; BURKHOLDERIA DOLOSA; BURKHOLDERIA MULTIVORANS; BURKHOLDERIA PYRROCINIA; BURKHOLDERIA STABILIS; BURKHOLDERIA VIETNAMIENSIS; CITROBACTER FREUNDII; CONTROLLED STUDY; ENTEROBACTER AEROGENES; ENTEROBACTER CLOACAE; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ESCHERICHIA COLI; GENE SEQUENCE; HAEMOPHILUS INFLUENZAE; KLEBSIELLA OXYTOCA; KLEBSIELLA PNEUMONIAE; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA LACTAMICA; NEISSERIA MENINGITIDIS; NONHUMAN; PROTEUS MIRABILIS; PSEUDOMONAS AERUGINOSA; SERRATIA MARCESCENS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STENOTROPHOMONAS MALTOPHILIA; STREPTOCOCCUS PNEUMONIAE; BACTERIAL INFECTION; BACTERIUM; BAYES THEOREM; BIOLOGY; CLASSIFICATION; DNA SEQUENCE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PROCEDURES; REPRODUCIBILITY;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

BACTERIA; BACTERIAL INFECTIONS; BACTERIOLOGICAL TECHNIQUES; BAYES THEOREM; CLASSIFICATION; COMPUTATIONAL BIOLOGY; HUMANS; REPRODUCIBILITY OF RESULTS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84922569156     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117617     Document Type: Article

References (70)

1. Martin GS, Mannino DM, Eaton S, Moss M (2003) The epidemiology of sepsis in the United States from 1979 through 2000. The New England journal of medicine 348: 1546-1554. PMID: 12700374
2. Iregui M, Ward S, Sherman G, Fraser VJ, Kollef MH (2002) Clinical importance of delays in the initiation of appropriate antibiotic treatment for ventilator-associated pneumonia. Chest 122: 262-268. PMID: 12114368
3. Shorr AF, Micek ST, Welch EC, Doherty JA, Reichley RM, et al. (2011) Inappropriate antibiotic therapy in Gram-negative sepsis increases hospital length of stay. Crit Care Med 39: 46-51. doi: 10.1097/CCM.0b013e3181fa41a7 PMID: 20890186
4. Hawkey PM (2008) The growing burden of antimicrobial resistance. J Antimicrob Chemother 62 Suppl 1: i1-9. doi: 10.1093/jac/dkn241 PMID: 18684701
5. Larson E (2007) Community factors in the development of antibiotic resistance. Annu Rev Public Health 28: 435-447. PMID: 17094768
6. Klevens RM, Edwards JR, Richards CL Jr, Horan TC, Gaynes RP, et al. (2007) Estimating health careassociated infections and deaths in U.S. hospitals, 2002. Public Health Rep 122: 160-166. PMID: 17357358
7. Plowman R, Graves N, Griffin MA, Roberts JA, Swan AV, et al. (2001) The rate and cost of hospital-acquired infections occurring in patients admitted to selected specialties of a district general hospital in England and the national burden imposed. J Hosp Infect 47: 198-209. PMID: 11247680
8. Clarridge JE 3rd (2004) Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 17: 840-862, table of contents. PMID: 15489351
9. Mignard S, Flandrois JP (2006) 16S rRNA sequencing in routine bacterial identification: a 30-month experiment. J Microbiol Methods 67: 574-581. PMID: 16859787
10. Barbut F, Monot M, Rousseau A, Cavelot S, Simon T, et al. (2011) Rapid diagnosis of Clostridium difficile infection by multiplex real-time PCR. Eur J Clin Microbiol Infect Dis 30: 1279-1285. doi: 10.1007/s10096-011-1224-z PMID: 21487764
11. Hallin M, Maes N, Byl B, Jacobs F, De Gheldre Y, et al. (2003) Clinical impact of a PCR assay for identification of Staphylococcus aureus and determination of methicillin resistance directly from blood cultures. J Clin Microbiol 41: 3942-3944. PMID: 12904425
12. Lehmann LE, Hunfeld KP, Emrich T, Haberhausen G, Wissing H, et al. (2008) A multiplex real-time PCR assay for rapid detection and differentiation of 25 bacterial and fungal pathogens from whole blood samples. Med Microbiol Immunol 197: 313-324. PMID: 18008085
13. Brown J, Paladino JA (2010) Impact of rapid methicillin-resistant Staphylococcus aureus polymerase chain reaction testing on mortality and cost effectiveness in hospitalized patients with bacteraemia: a decision model. Pharmacoeconomics 28: 567-575. doi: 10.2165/11533020-000000000-00000 PMID: 20550222
14. Adekambi T, Drancourt M, Raoult D (2009) The rpoB gene as a tool for clinical microbiologists. Trends Microbiol 17: 37-45. doi: 10.1016/j.tim.2008.09.008 PMID: 19081723
15. Bartual SG, Seifert H, Hippler C, Luzon MA, Wisplinghoff H, et al. (2005) Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol 43: 4382-4390. PMID: 16145081
16. Enright MC, Knox K, Griffiths D, Crook DW, Spratt BG (2000) Molecular typing of bacteria directly from cerebrospinal fluid. Eur J Clin Microbiol Infect Dis 19: 627-630. PMID: 11014627
17. Mathema B, Kurepina NE, Bifani PJ, Kreiswirth BN (2006) Molecular epidemiology of tuberculosis: current insights. Clin Microbiol Rev 19: 658-685. PMID: 17041139
18. Slack AT, Symonds ML, Dohnt MF, Smythe LD (2006) Identification of pathogenic Leptospira species by conventional or real-time PCR and sequencing of the DNA gyrase subunit B encoding gene. BMC Microbiol 6: 95. PMID: 17067399
19. Conlan S, Kong HH, Segre JA (2012) Species-level analysis of DNA sequence data from the NIH Human Microbiome Project. PLoS One 7: e47075. doi: 10.1371/journal.pone.0047075 PMID: 23071716
20. Fettweis JM, Serrano MG, Sheth NU, Mayer CM, Glascock AL, et al. (2012) Species-level classification of the vaginal microbiome. BMC Genomics 13 Suppl 8: S17.
21. Newton IL, Roeselers G (2012) The effect of training set on the classification of honey bee gut microbiota using the Naive Bayesian Classifier. BMC Microbiol 12: 221. doi: 10.1186/1471-2180-12-221 PMID: 23013113
22. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-145. doi: 10.1093/nar/gkn879 PMID: 19004872
23. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, et al. (2006) Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072. PMID: 16820507
24. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196. PMID: 17947321
25. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6: 1621-1624. doi: 10.1038/ismej.2012.8 PMID: 22402401
26. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, et al. (2009) Bacterial community variation in human body habitats across space and time. Science 326: 1694-1697. doi: 10.1126/science.1177486 PMID: 19892944
27. Huse SM, Dethlefsen L, Huber JA, Mark Welch D, Relman DA, et al. (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4: e1000255. doi: 10.1371/journal.pgen.1000255 PMID: 19023400
28. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, et al. (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41: e1. doi: 10.1093/nar/gks808 PMID: 22933715
29. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214. doi: 10.1038/nature11234 PMID: 22699609
30. Hall L, Doerr KA, Wohlfiel SL, Roberts GD (2003) Evaluation of the MicroSeq system for identification of mycobacteria by 16S ribosomal DNA sequencing and its integration into a routine clinical mycobacteriology laboratory. J Clin Microbiol 41: 1447-1453. PMID: 12682128
31. Rogall T, Wolters J, Flohr T, Bottger EC (1990) Towards a phylogeny and definition of species at the molecular level within the genus Mycobacterium. Int J Syst Bacteriol 40: 323-330. PMID: 2275850
32. Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, et al. (2000) 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38: 3623-3630. PMID: 11015374
33. Bosshard PP, Abels S, Zbinden R, Bottger EC, Altwegg M (2003) Ribosomal DNA sequencing for identification of aerobic gram-positive rods in the clinical laboratory (an 18-month evaluation). J Clin Microbiol 41: 4134-4140. PMID: 12958237
34. Spilker T, Coenye T, Vandamme P, LiPuma JJ (2004) PCR-based assay for differentiation of Pseudomonas aeruginosa from other Pseudomonas species recovered from cystic fibrosis patients. J Clin Microbiol 42: 2074-2079. PMID: 15131172
35. Fontana C, Favaro M, Pelliccioni M, Pistoia ES, Favalli C (2005) Use of the MicroSeq 500 16S rRNA gene-based sequencing for identification of bacterial isolates that commercial automated systems failed to identify correctly. J Clin Microbiol 43: 615-619. PMID: 15695654
36. Woo PC, Ng KH, Lau SK, Yip KT, Fung AM, et al. (2003) Usefulness of the MicroSeq 500 16S ribosomal DNA-based bacterial identification system for identification of clinically significant bacterial isolates with ambiguous biochemical profiles. J Clin Microbiol 41: 1996-2001. PMID: 12734240
37. Simmon KE, Croft AC, Petti CA (2006) Application of Smart Gene IDNS software to partial 16S rRNA gene sequences for a diverse group of bacteria in a clinical laboratory. J Clin Microbiol 44: 4400-4406. PMID: 17050811
38. Harmsen D, Rothganger J, Frosch M, Albert J (2002) RIDOM: Ribosomal Differentiation of Medical Micro-organisms Database. Nucleic Acids Res 30: 416-417. PMID: 11752353
39. Woo PC, Teng JL, Yeung JM, Tse H, Lau SK, et al. (2011) Automated identification of medically important bacteria by 16S rRNA gene sequencing using a novel comprehensive database, 16 Spath DB. J Clin Microbiol 49: 1799-1809. doi: 10.1128/JCM.02350-10 PMID: 21389154
40. Teng JL, Ho TC, Yeung RS, Wong AY, Wang H, et al. (2014) Evaluation of 16SpathDB 2.0, an automated 16S rRNA gene sequence database, using 689 complete bacterial genomes. Diagn Microbiol Infect Dis 78: 105-115. doi: 10.1016/j.diagmicrobio.2013.10.019 PMID: 24295571
41. Winn WC, Koneman EW (2006) Koneman's color atlas and textbook of diagnostic microbiology. Philadelphia: Lippincott Williams & Wilkins. PMID: 25590126
42. de Filippis I, de Andrade CF, de Almeida AE, Clementino MM, Fernandes CA, et al. (2007) Neisseria meningitidis PorA variable regions: rapid detection of P1.7 and P1.19 variants by PCR. Lett Appl Microbiol 45: 426-431. PMID: 17897387
43. Hulbert RR, Cotter PA (2009) Laboratory Maintenance of Bordetella pertussis. Curr Protoc Microbiol Chapter 4: Unit 4B 1.
44. Schloss PD (2010) The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput Biol 6: e1000844. doi: 10.1371/journal.pcbi.1000844 PMID: 20628621
45. Jumpstart Consortium Human Microbiome Project Data Generation Working Group (2012) Evaluation of 16S rDNA-based community profiling for human microbiome research. PLoS One 7: e39315. doi: 10.1371/journal.pone.0039315 PMID: 22720093
46. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267. PMID: 17586664
47. Versalovic J, American Society for Microbiology (2011) Manual of clinical microbiology. Washington, DC: ASM Press. doi: 10.1111/j.1758-8111.2010.00005.x PMID: 22362179
48. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541. doi: 10.1128/AEM.01541-09 PMID: 19801464
49. R Development Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing,. doi: 10.1016/j.fsigen.2014.12.009 PMID: 25596557
50. Liu D (2011) Molecular detection of human bacterial pathogens. Boca Raton, FL: Taylor & Francis/CRC Press. xxvii, 1251 p. p.
51. Facklam R (2002) What happened to the streptococci: overview of taxonomic and nomenclature changes. Clin Microbiol Rev 15: 613-630. PMID: 12364372
52. Boone DR, Castenholz RW, Garrity GM, Bergey DH (2001) Bergey's manual of systematic bacteriology. New York: Springer. v. p. PMID: 25506954
53. Pei AY, Oberdorf WE, Nossa CW, Agarwal A, Chokshi P, et al. (2010) Diversity of 16S rRNA genes within individual prokaryotic genomes. Appl Environ Microbiol 76: 3886-3897. doi: 10.1128/AEM. 02953-09 PMID: 20418441
54. Coenye T, Spilker T, Martin A, LiPuma JJ (2002) Comparative assessment of genotyping methods for epidemiologic study of Burkholderia cepacia genomovar III. J Clin Microbiol 40: 3300-3307. PMID: 12202570
55. Lipuma JJ (2005) Update on the Burkholderia cepacia complex. Curr Opin Pulm Med 11: 528-533. PMID: 16217180
56. Bernards AT, van der Toorn J, van Boven CP, Dijkshoorn L (1996) Evaluation of the ability of a commercial system to identify Acinetobacter genomic species. Eur J Clin Microbiol Infect Dis 15: 303-308. PMID: 8781881
57. Joyanes P, del Carmen Conejo M, Martinez-Martinez L, Perea EJ (2001) Evaluation of the VITEK 2 system for the identification and susceptibility testing of three species of nonfermenting gram-negative rods frequently isolated from clinical samples. J Clin Microbiol 39: 3247-3253. PMID: 11526158
58. Day AM, Sandoe JA, Cove JH, Phillips-Jones MK (2001) Evaluation of a biochemical test scheme for identifying clinical isolates of Enterococcus faecalis and Enterococcus faecium. Lett Appl Microbiol 33: 392-396. PMID: 11696103
59. Deasy BM, Rea MC, Fitzgerald GF, Cogan TM, Beresford TP (2000) A rapid PCR based method to distinguish between Lactococcus and Enterococcus. Syst Appl Microbiol 23: 510-522. PMID: 11249021
60. Carvalho MG, Steigerwalt AG, Thompson T, Jackson D, Facklam RR (2003) Confirmation of nontypeable Streptococcus pneumoniae-like organisms isolated from outbreaks of epidemic conjunctivitis as Streptococcus pneumoniae. J Clin Microbiol 41: 4415-4417. PMID: 12958280
61. Hanage WP, Kaijalainen T, Herva E, Saukkoriipi A, Syrjanen R, et al. (2005) Using multilocus sequence data to define the pneumococcus. J Bacteriol 187: 6223-6230. PMID: 16109964
62. Whatmore AM, Efstratiou A, Pickerill AP, Broughton K, Woodard G, et al. (2000) Genetic relationships between clinical isolates of Streptococcus pneumoniae, Streptococcus oralis, and Streptococcus mitis: characterization of "Atypical" pneumococci and organisms allied to S. mitis harboring S. pneumoniae virulence factor-encoding genes. Infect Immun 68: 1374-1382. PMID: 10678950
63. Havarstein LS, Hakenbeck R, Gaustad P (1997) Natural competence in the genus Streptococcus: evidence that streptococci can change pherotype by interspecies recombinational exchanges. J Bacteriol 179: 6589-6594. PMID: 9352904
64. Park JS, Hong KH, Lee HJ, Choi SH, Song SH, et al. (2011) Evaluation of three phenotypic identification systems for clinical isolates of Raoultella ornithinolytica. J Med Microbiol 60: 492-499. doi: 10.1099/jmm.0.020768-0 PMID: 21212145
65. Hejazi A, Falkiner FR (1997) Serratia marcescens. J Med Microbiol 46: 903-912. PMID: 9368530
66. Brouqui P, Raoult D (2001) Endocarditis due to rare and fastidious bacteria. Clin Microbiol Rev 14: 177-207. PMID: 11148009
67. LaClaire LL, Facklam RR (2000) Comparison of three commercial rapid identification systems for the unusual gram-positive cocci Dolosigranulum pigrum, Ignavigranum ruoffiae, and Facklamia species. J Clin Microbiol 38: 2037-2042. PMID: 10834950
68. Woo PC, Lau SK, Fung AM, Chiu SK, Yung RW, et al. (2003) Gemella bacteraemia characterised by 16S ribosomal RNA gene sequencing. J Clin Pathol 56: 690-693. PMID: 12944554
69. Werner JJ, Koren O, Hugenholtz P, DeSantis TZ, Walters WA, et al. (2012) Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys. ISME J 6: 94-103. doi: 10.1038/ismej.2011.82 PMID: 21716311
70. Fournier PE, Raoult D (2011) Prospects for the future using genomics and proteomics in clinical microbiology. Annu Rev Microbiol 65: 169-188. doi: 10.1146/annurev-micro-090110-102922 PMID: 21639792