Applied Microbiology and Biotechnology

, Volume 98, Issue 23, pp 9595–9608 | Cite as

Mathematical tools to optimize the design of oligonucleotide probes and primers

  • Daniel R. Noguera
  • Erik S. Wright
  • Pamela Camejo
  • L. Safak Yilmaz
Mini-Review

Abstract

The identification and quantification of specific organisms in mixed microbial communities often relies on the ability to design oligonucleotide probes and primers with high specificity and sensitivity. The design of these oligonucleotides (or “oligos” for short) shares many of the same principles in spite of their widely divergent applications. Three common molecular biology technologies that require oligonucleotide design are polymerase chain reaction (PCR), fluorescence in situ hybridization (FISH), and DNA microarrays. This article reviews techniques and software available for the design and optimization of oligos with the goal of targeting a specific group of organisms within mixed microbial communities. Strategies for enhancing specificity without compromising sensitivity are described, as well as design tools well suited for this purpose.

Keywords

Oligonucleotides DNA probes FISH PCR Microarrays Mismatch stability Microbial diversity Primer design 

References

  1. Abell GCJ, Revill AT, Smith C, Bissett AP, Volkman JK, Robert SS (2010) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4(2):286–300. doi:10.1038/ismej.2009.105 PubMedCrossRefGoogle Scholar
  2. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56(6):1919–1925PubMedCentralPubMedGoogle Scholar
  3. Applied Biosystems (2004) Primer express software version 3.0. getting started guideGoogle Scholar
  4. Arvidsson S, Kwasniewski M, Riano-Pachon DM, Mueller-Roeber B (2008) QuantPrime—a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinforma 9. doi:10.1186/1471-2105-9-465Google Scholar
  5. Ayyadevara S, Thaden JJ, Reis RJS (2000) Discrimination of primer 3′-nucleotide mismatch by Taq DNA polymerase during polymerase chain reaction. Anal Biochem 284(1):11–18. doi:10.1006/abio.2000.4635 PubMedCrossRefGoogle Scholar
  6. Bakshi S, Siryaporn A, Goulian M, Weisshaar JC (2012) Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol Microbiol 85(1):21–38. doi:10.1111/j.1365-2958.2012.08081.x PubMedCentralPubMedCrossRefGoogle Scholar
  7. Baldwin BR, Nakatsu CH, Nies L (2003) Detection and enumeration of aromatic oxygenase genes by multiplex and real-time PCR. Appl Environ Microbiol 69(6):3350–3358. doi:10.1128/aem. 69.6.3350-3358.2003 PubMedCentralPubMedCrossRefGoogle Scholar
  8. Behrens S, Ruhland C, Inacio J, Huber H, Fonseca A, Spencer-Martins I, Fuchs BM, Amann R (2003) In situ accessibility of small-subunit rRNA of members of the domains bacteria, archaea, and eucarya to Cy3-labeled oligonucleotide probes. Appl Environ Microbiol 69(3):1748–1758. doi:10.1128/aem. 69.3.1748-1758.2003 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Bethge L, Jarikote DV, Seitz O (2008) New cyanine dyes as base surrogates in PNA: forced intercalation probes (FIT-probes) for homogeneous SNP detection. Bioorg Med Chem 16(1):114–125. doi:10.1016/j.bmc.2006.12.044 PubMedCrossRefGoogle Scholar
  10. Binder H, Preibisch S, Kirsten T (2005) Base pair interactions and hybridization isotherms of matched and mismatched oligonucleotide probes on microarrays. Langmuir 21(20):9287–302. doi:10.1021/la051231s PubMedCrossRefGoogle Scholar
  11. Burden CJ, Pittelkow YE, Wilson SR (2004) Statistical analysis of adsorption models for oligonucleotide microarrays. Stat Appl Genet Mol Biol 3:Article35 doi:10.2202/1544-6115.1095
  12. Cha RS, Zarbl H, Keohavong P, Thilly WG (1992) Mismatch amplification mutation assay (MAMA): application to the c-H-ras gene. PCR Methods Appl 2(1):14–20PubMedCrossRefGoogle Scholar
  13. Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35:D169–D172. doi:10.1093/nar/gkl889 PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66(4):1692–1697. doi:10.1128/aem. 66.4.1692-1697.2000 PubMedCentralPubMedCrossRefGoogle Scholar
  15. Courtenay ES, Capp MW, Saecker RM, Record MT (2000) Thermodynamic analysis of interactions between denaturants and protein surface exposed on unfolding: interpretation of urea and guanidinium chloride m-values and their correlation with changes in accessible surface area (ASA) using preferential interaction coefficients and the local-bulk domain model. Proteins Struct Funct Genet: 72–85Google Scholar
  16. Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22(3):434–444PubMedCrossRefGoogle Scholar
  17. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072. doi:10.1128/aem. 03006-05 PubMedCentralPubMedCrossRefGoogle Scholar
  18. DeSantis TZ, Brodie EL, Moberg JP, Zubieta IX, Piceno YM, Andersen GL (2007) High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microb Ecol 53(3):371–383. doi:10.1007/s00248-006-9134-9 PubMedCrossRefGoogle Scholar
  19. Dirks RM, Pierce NA (2004) Triggered amplification by hybridization chain reaction. Proc Natl Acad Sci U S A 101(43):15275–15278. doi:10.1073/pnas.0407024101 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Fazi S, Aulenta F, Majone M, Rossetti S (2008) Improved quantification of Dehalococcoides species by fluorescence in situ hybridization and catalyzed reporter deposition. Syst Appl Microbiol 31(1):62–67. doi:10.1016/j.syapm.2007.11.001 PubMedCrossRefGoogle Scholar
  21. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74(8):2461–2470. doi:10.1128/aem. 02272-07 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Fuchs BM, Wallner G, Beisker W, Schwippl I, Ludwig W, Amann R (1998) Flow cytometric analysis of the in situ accessibility of Escherichia coli 16S rRNA for fluorescently labeled oligonucleotide probes. Appl Environ Microbiol 64(12):4973–4982PubMedCentralPubMedGoogle Scholar
  23. Fuchs BM, Syutsubo K, Ludwig W, Amann R (2001) In situ accessibility of Escherichia coli 23S rRNA to fluorescently labeled oligonucleotide probes. Appl Environ Microbiol 67(2):961–968. doi:10.1128/AEM. 67.2.961-968.2001 PubMedCentralPubMedCrossRefGoogle Scholar
  24. Gudnason H, Dufva M, Bang DD, Wolff A (2007) Comparison of multiple DNA dyes for real-time PCR: effects of dye concentration and sequence composition on DNA amplification and melting temperature. Nucleic Acids Res 35(19):e127. doi:10.1093/nar/gkm671 PubMedCentralPubMedCrossRefGoogle Scholar
  25. Halperin A, Buhot A, Zhulina EB (2005) Brush effects on DNA chips: thermodynamics, kinetics, and design guidelines. Biophys J 89(2):796–811. doi:10.1529/biophysj.105.063479 PubMedCentralPubMedCrossRefGoogle Scholar
  26. Held GA, Grinstein G, Tu Y (2003) Modeling of DNA microarray data by using physical properties of hybridization. Proc Natl Acad Sci U S A 100(13):7575–80. doi:10.1073/pnas.0832500100 PubMedCentralPubMedCrossRefGoogle Scholar
  27. Hooyberghs J, Van Hummelen P, Carlon E (2009) The effects of mismatches on hybridization in DNA microarrays: determination of nearest neighbor parameters. Nucleic Acids Res 37(7):e53. doi:10.1093/nar/gkp109 PubMedCentralPubMedCrossRefGoogle Scholar
  28. Ilie L, Mohamadi H, Golding GB, Smyth WF (2013) BOND: basic oligonucleotide design. BMC Bioinforma 14(69):1–8. doi:10.1186/1471-2105-14-69 Google Scholar
  29. Jacobson H, Stockmayer WH (1950) Intramolecular reaction in polycondensations. I. The theory of linear systems. J Chem Phys 18:1600–1606CrossRefGoogle Scholar
  30. Jones CM, Stres B, Rosenquist M, Hallin S (2008) Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol Biol Evol 25(9):1955–1966. doi:10.1093/molbev/msn146 PubMedCrossRefGoogle Scholar
  31. Karkare S, Bhatnagar D (2006) Promising nucleic acid analogs and mimics: characteristic features and applications of PNA, LNA, and morpholino. Appl Microbiol Biotechnol 71(5):575–586. doi:10.1007/s00253-006-0434-2 PubMedCrossRefGoogle Scholar
  32. Kelly JJ, Siripong S, McCormack J, Janus LR, Urakawa H, El Fantroussi S, Noble PA, Sappelsa L, Rittmann BE, Stahl DA (2005) DNA microarray detection of nitrifying bacterial 16S rRNA in wastewater treatment plant samples. Water Res 39(14):3229–3238. doi:10.1016/j.watres.2005.05.044 PubMedCrossRefGoogle Scholar
  33. Klein M, Friedrich M, Roger AJ, Hugenholtz P, Fishbain S, Abicht H, Blackall LL, Stahl DA, Wagner M (2001) Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J Bacteriol 183(20):6028–6035. doi:10.1128/jb.183.20.6028-6035.2001 PubMedCentralPubMedCrossRefGoogle Scholar
  34. Korbie DJ, Mattick JS (2008) Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat Protoc 3(9):1452–1456. doi:10.1038/nprot.2008.133 PubMedCrossRefGoogle Scholar
  35. Kushwaha G, Srivastava GP, Dong X PRIMEGENSw3 (2011) A web-based tool for high-throughput primer and probe design. In 2011 I.E. International Conference on Bioinformatics and Biomedicine (BIBM), 12–15 Nov. 2011 2011. p 345–351 doi:10.1109/bibm.2011.43
  36. Kutyavin IV, Afonina IA, Mills A, Gorn VV, Lukhtanov EA, Belousov ES, Singer MJ, Walburger DK, Lokhov SG, Gall AA, Dempcy R, Reed MW, Meyer RB, Hedgpeth J (2000) 3′-minor groove binder-DNA probes increase sequence specificity at PCR extension temperatures. Nucleic Acids Res 28(2):655–661. doi:10.1093/nar/28.2.655 PubMedCentralPubMedCrossRefGoogle Scholar
  37. Lemoine S, Combes F, Le Crom S (2009) An evaluation of custom microarray applications: the oligonucleotide design challenge. Nucleic Acids Res 37(6):1726–1739. doi:10.1093/nar/gkp053 PubMedCentralPubMedCrossRefGoogle Scholar
  38. Lenk S, Arnds J, Zerjatke K, Musat N, Amann R, Mussmann M (2011) Novel groups of Gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment. Environ Microbiol 13(3):758–774. doi:10.1111/j.1462-2920.2010.02380.x PubMedCrossRefGoogle Scholar
  39. Li BH, Kadura I, Fu DJ, Watson DE (2004) Genotyping with TaqMAMA. Genomics 83(2):311–320. doi:10.1016/j.ygeno.2003.08.005 PubMedCrossRefGoogle Scholar
  40. Li X, He Z, Zhou J (2005) Selection of optimal oligonucleotide probes for microarrays using multiple criteria, global alignment and parameter estimation. Nucleic Acids Res 33(19):6114–23. doi:10.1093/nar/gki914 PubMedCentralPubMedCrossRefGoogle Scholar
  41. Liu WT, Mirzabekov AD, Stahl DA (2001) Optimization of an oligonucleotide microchip for microbial identification studies: a non-equilibrium dissociation approach. Environ Microbiol 3(10):619–629PubMedCrossRefGoogle Scholar
  42. Livak KJ (1999) Allelic discrimination using fluorogenic probes and the 5’ nuclease assay. Genet Anal-Biomol E 14(5–6):143–149. doi:10.1016/s1050-3862(98)00019-9 CrossRefGoogle Scholar
  43. Livak KJ, Flood SJA, Marmaro J, Giusti W, Deetz K (1995) Oligonucleotides with fluorescent dyes at opposite ends provide a quenched probe system useful for detecting PCR product and nucleic acid hybridization. PCR Meth Appl 4(6):357–362CrossRefGoogle Scholar
  44. Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J, Schleifer KH, Wagner M (2002) Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Microbiol 68(10):5064–5081. doi:10.1128/AEM. 68.10.5064-5081.2002 PubMedCentralPubMedCrossRefGoogle Scholar
  45. Loy A, Schulz C, Lucker S, Schopfer-Wendels A, Stoecker K, Baranyi C, Lehner A, Wagner M (2005) 16S rRNA gene-based oligonucleotide microarray for environmental monitoring of the betaproteobacterial order “Rhodocyclales”. Appl Environ Microbiol 71(3):1373–1386. doi:10.1128/AEM. 71.3.1373-1386.2005 PubMedCentralPubMedCrossRefGoogle Scholar
  46. Loy A, Maixner F, Wagner M, Horn M (2007) probeBase—an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res 35:D800–D804. doi:10.1093/nar/gkl856 PubMedCentralPubMedCrossRefGoogle Scholar
  47. Loy A, Arnold R, Tischler P, Rattei T, Wagner M, Horn M (2008) probeCheck—a central resource for evaluating oligonucleotide probe coverage and specificity. Environ Microbiol 10(10):2894–2898. doi:10.1111/j.1462-2920.2008.01706.x PubMedCentralPubMedCrossRefGoogle Scholar
  48. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32(4):1363–71. doi:10.1093/nar/gkh293 PubMedCentralPubMedCrossRefGoogle Scholar
  49. Manz W, Amann R, Ludwig W, Wagner M, Schleifer KH (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria—problems and solutions. Syst Appl Microbiol 15(4):593–600CrossRefGoogle Scholar
  50. Markham NR, Zuker M (2008) UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 453:3–31. doi:10.1007/978-1-60327-429-6_1 PubMedCrossRefGoogle Scholar
  51. Mathews D, Burkard M, Freier S, Wyatt J, Turner D (1999a) Predicting oligonucleotide affinity to nucleic acid targets. RNA 5:1458–1469. doi:10.1017/S1355838299991148 PubMedCentralPubMedCrossRefGoogle Scholar
  52. Mathews D, Sabina J, Zuker M, Turner D (1999b) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940. doi:10.1006/jmbi.1999.2700 PubMedCrossRefGoogle Scholar
  53. McIlroy SJ, Tillett D, Petrovski S, Seviour RJ (2011) Non-target sites with single nucleotide insertions or deletions are frequently found in 16S rRNA sequences and can lead to false positives in fluorescence in situ hybridization (FISH). Environ Microbiol 13(1):33–47. doi:10.1111/j.1462-2920.2010.02306.x PubMedCrossRefGoogle Scholar
  54. Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schaffer AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24(16):1757–1764. doi:10.1093/bioinformatics/btn322 PubMedCentralPubMedCrossRefGoogle Scholar
  55. Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10(11):3002–3016. doi:10.1111/j.1462-2920.2008.01764.x PubMedCrossRefGoogle Scholar
  56. Nielsen HB (2003) Design of oligonucleotides for microarrays and perspectives for design of multi-transcriptome arrays. Nucleic Acids Res 31(13):3491–3496. doi:10.1093/nar/gkg622 PubMedCentralPubMedCrossRefGoogle Scholar
  57. Nordberg EK (2005) YODA: selecting signature oligonucleotides. Bioinformatics 21(8):1365–70. doi:10.1093/bioinformatics/bti182 PubMedCrossRefGoogle Scholar
  58. Okten HE, Yilmaz LS, Noguera DR (2012) Exploring the in situ accessibility of small subunit ribosomal RNA of members of the domains Bacteria and Eukarya to oligonucleotide probes. Syst Appl Microbiol 35(8):485–495. doi:10.1016/j.syapm.2011.11.001 PubMedCrossRefGoogle Scholar
  59. Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68(6):3094–3101. doi:10.1128/AEM. 68.6.3094-3101.2002 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Perry-O’Keefe H, Rigby S, Oliveira K, Sorensen D, Slender H, Coull J, Hyldig-Nielsen JJ (2001) Identification of indicator microorganisms using a standardized PNA FISH method. J Microbiol Methods 47(3):281–292. doi:10.1016/s0167-7012(01)00303-7 PubMedCrossRefGoogle Scholar
  61. Pester M, Rattei T, Flechl S, Grongroft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14(2):525–539. doi:10.1111/j.1462-2920.2011.02666.x PubMedCentralPubMedCrossRefGoogle Scholar
  62. Peterson AW, Heaton RJ, Georgiadis RM (2001) The effect of surface probe density on DNA hybridization. Nucleic Acids Res 29(24):5163–5168. doi:10.1093/nar/29.24.5163 PubMedCentralPubMedCrossRefGoogle Scholar
  63. Pfeiffer S, Pastar M, Mitter B, Lippert K, Hackl E, Lojan P, Oswald A, Sessitsch A (2014) Improved group-specific primers based on the full SILVA 16S rRNA gene reference database. Environ Microbiol. doi:10.1111/1462-2920.12350 Google Scholar
  64. Pilhofer M, Pavlekovic M, Lee NM, Ludwig W, Schleifer KH (2009) Fluorescence in situ hybridization for intracellular localization of nifH mRNA. Syst Appl Microbiol 32(3):186–192. doi:10.1016/j.syapm.2008.12.007 PubMedCrossRefGoogle Scholar
  65. Pozhitkov A, Noble PA, Domazet-Loso T, Nolte AW, Sonnenberg R, Staehler P, Beier M, Tautz D (2006) Tests of rRNA hybridization to microarrays suggest that hybridization characteristics of oligonucleotide probes for species discrimination cannot be predicted. Nucleic Acids Res 34(9): doi:10.1093/nar/gkl133
  66. Pozhitkov AE, Tautz D, Noble PA (2007) Oligonucleotide microarrays: widely applied—poorly understood. Brief Funct Genomic Proteomic 6(2):141–8. doi:10.1093/bfgp/elm014 PubMedCrossRefGoogle Scholar
  67. Pratscher J, Stichternoth C, Fichtl K, Schleifer KH, Braker G (2009) Application of recognition of individual genes-fluorescence in situ hybridization (RING-FISH) to detect nitrite reductase genes (nirK) of denitrifiers in pure cultures and environmental samples. Appl Environ Microbiol 75(3):802–810. doi:10.1128/aem. 01992-08 PubMedCentralPubMedCrossRefGoogle Scholar
  68. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596. doi:10.1093/nar/gks1219 PubMedCentralPubMedCrossRefGoogle Scholar
  69. Rasmussen JP, Saint CP, Monis PT (2007) Use of DNA melting simulation software for in silico diagnostic assay design: targeting regions with complex melting curves and confirmation by real-time PCR using intercalating dyes. BMC Bioinforma 8. doi:10.1186/1471-2105-8-107Google Scholar
  70. Rosenthal AZ, Zhang XN, Lucey KS, Ottesen EA, Trivedi V, Choi HMT, Pierce NA, Leadbetter JR (2013) Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy. Proc Natl Acad Sci U S A 110(40):16163–16168. doi:10.1073/pnas.1307876110 PubMedCentralPubMedCrossRefGoogle Scholar
  71. Rouillard JM (2003) OligoArray 2.0: design of oligonucleotide probes for DNA microarrays using a thermodynamic approach. Nucleic Acids Res 31(12):3057–3062. doi:10.1093/nar/gkg426 PubMedCentralPubMedCrossRefGoogle Scholar
  72. SantaLucia J Jr (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc Natl Acad Sci U S A 95:1460–1465. doi:10.1073/pnas.95.4.1460 PubMedCentralPubMedCrossRefGoogle Scholar
  73. SantaLucia J Jr, Hicks D (2004) The thermodynamics of DNA structural motifs. Annu Rev Biophys Biomol Struct 33:415–40. doi:10.1146/annurev.biophys.32.110601.141800 PubMedCrossRefGoogle Scholar
  74. Schellman JA (1978) Solvent denaturation. Biopolymers 17:1305–1322CrossRefGoogle Scholar
  75. Schwartz SB, Thurman KA, Mitchell SL, Wolff BJ, Winchell JM (2009) Genotyping of Mycoplasma pneumoniae isolates using real-time PCR and high-resolution melt analysis. Clin Microbiol Infect 15(8):756–762. doi:10.1111/j.1469-0691.2009.02814.x PubMedCrossRefGoogle Scholar
  76. Silahtaroglu A, Pfundheller H, Koshkin A, Tommerup N, Kauppinen S (2004) LNA-modified oligonucleotides are highly efficient as FISH probes. Cytogenet Genome Res 107(1–2):32–37. doi:10.1159/000079569 PubMedCrossRefGoogle Scholar
  77. Stadhouders R, Pas SD, Anber J, Voermans J, Mes THM, Schutten M (2010) The effect of primer-template mismatches on the detection and quantification of nucleic acids using the 5′ nuclease assay. J Mol Diagn 12(1):109–117. doi:10.2353/jmoldx.2010.090035 PubMedCentralPubMedCrossRefGoogle Scholar
  78. Stahl DA, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 205–248Google Scholar
  79. Strunk O (2001) ARB: entwicklung eines programmsystems zur erfassung, Verwaltung und auswertung von nuklein- und aminosäuresequenzen. PhD Thesis, Technische Universität MünchenGoogle Scholar
  80. Sugimoto N, Nakano S, Katoh M, Matsumura A, Nakamuta H, Ohmichi T, Yoneyama M, Sasaki M (1995) Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes. Biochemistry 34(35):11211–6. doi:10.1021/bi00035a029 PubMedCrossRefGoogle Scholar
  81. Sugimoto N, Nakano M, Nakano S (2000) Thermodynamics-structure relationship of single mismatches in RNA/DNA duplexes. Biochemistry 39(37):11270–11281. doi:10.1021/bi000819p PubMedCrossRefGoogle Scholar
  82. Turner D (2000) Chapter 8: conformational changes. In: Bloomfield VA, Crothers DM, Tinoco IJ (eds) Nucleic acids: structures, properties, and functions. University Science, SausalitoGoogle Scholar
  83. Turner DH, Mathews DH (2010) NNDB: the nearest neighbor parameter database for predicting stability of nucleic acid secondary structure. Nucleic Acids Res 38:D280–D282. doi:10.1093/nar/gkp892 PubMedCentralPubMedCrossRefGoogle Scholar
  84. Tyagi S, Kramer FR (1996) Molecular beacons: probes that fluoresce upon hybridization. Nat Biotechnol 14(3):303–308. doi:10.1038/nbt0396-303 PubMedCrossRefGoogle Scholar
  85. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. doi:10.1093/nar/gkm306 PubMedCentralPubMedCrossRefGoogle Scholar
  86. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40(15):e115. doi:10.1093/nar/gks596 PubMedCentralPubMedCrossRefGoogle Scholar
  87. Urakawa H, Noble PA, El Fantroussi S, Kelly JJ, Stahl DA (2002) Single-base-pair discrimination of terminal mismatches by using oligonucleotide microarrays and neural network analyses. Appl Environ Microbiol 68(1):235–244. doi:10.1128/AEM. 68.1.235-244.2002 PubMedCentralPubMedCrossRefGoogle Scholar
  88. Wagner M, Haider S (2012) New trends in fluorescence in situ hybridization for identification and functional analyses of microbes. Curr Opin Biotechnol 23(1):96–102. doi:10.1016/j.copbio.2011.10.010 PubMedCrossRefGoogle Scholar
  89. Watkins NE, Kennelly WJ, Tsay MJ, Tuin A, Swenson L, Lee HR, Morosyuk S, Hicks DA, SantaLucia J (2011) Thermodynamic contributions of single internal rA circle dot dA, rC circle dot dC, rG circle dot dG and rU circle dot dT mismatches in RNA/DNA duplexes. Nucleic Acids Res 39(5):1894–1902. doi:10.1093/nar/gkq905 PubMedCentralPubMedCrossRefGoogle Scholar
  90. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S Ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703PubMedCentralPubMedGoogle Scholar
  91. Weller SA, Elphinstone JG, Smith NC, Boonham N, Stead DE (2000) Detection of Ralstonia solanacearum strains with a quantitative, multiplex, real-time, fluorogenic PCR (TaqMan) assay. Appl Environ Microbiol 66(7):2853–2858. doi:10.1128/aem. 66.7.2853-2858.2000 PubMedCentralPubMedCrossRefGoogle Scholar
  92. Wilcox TM, Schwartz MK, McKelvey KS, Young MK, Lowe WH (2014) A blocking primer increases specificity in environmental DNA detection of bull trout (Salvelinus confluentus). Conserv Genet Resour 6(2):283–284. doi:10.1007/s12686-013-0113-4 CrossRefGoogle Scholar
  93. Wittwer CT, Herrmann MG, Moss AA, Rasmussen RP (1997) Continuous fluorescence monitoring of rapid cycle DNA amplification. Biotechniques 22(1):130PubMedGoogle Scholar
  94. Wright ES (2012) DECIPHER: database enabled code for ideal probe hybridization Employing R. R Package version 1.12.0. http://www.bioconductor.org/packages/2.12/bioc/html/DECIPHER.html
  95. Wright ES, Strait JM, Yilmaz LS, Harrington GW, Noguera DR (2013) Identification of bacterial and archaeal communities from source to tap. Water Research Foundation, DenverGoogle Scholar
  96. Wright ES, Yilmaz LS, Corcoran AM, Okten HE, Noguera DR (2014a) Automated design of probes for rRNA-targeted fluorescence in situ hybridization (FISH) reveals the advantages of dual probes for accurate identification. Appl Environ Microbiol 80(16):5124–5133. doi:10.1128/AEM. 01685-14 PubMedCrossRefGoogle Scholar
  97. Wright ES, Yilmaz LS, Ram S, Gasser JM, Harrington GW, Noguera DR (2014b) Exploiting extension bias in polymerase chain reaction to improve primer specificity in ensembles of nearly identical DNA templates. Environ Microbiol 16(5):1354–1365. doi:10.1111/1462-2920.12259 PubMedCrossRefGoogle Scholar
  98. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinforma 13. doi:10.1186/1471-2105-13-134Google Scholar
  99. Yilmaz LS, Noguera DR (2004) Mechanistic approach to the problem of hybridization efficiency in fluorescent in situ hybridization. Appl Environ Microbiol 70(12):7126–7139. doi:10.1128/AEM. 70.12.7126-7139.2004 PubMedCentralPubMedCrossRefGoogle Scholar
  100. Yilmaz LS, Noguera DR (2007) Development of thermodynamic models for simulating probe dissociation profiles in fluorescence in situ hybridization. Biotechnol Bioeng 96(2):349–363. doi:10.1002/bit.21114 PubMedCrossRefGoogle Scholar
  101. Yilmaz LS, Okten HE, Noguera DR (2006) Making all parts of the 16S rRNA of Escherichia coli accessible in situ to single DNA oligonucleotides. Appl Environ Microbiol 72(1):733–744. doi:10.1128/AEM. 72.1.733-744.2006 PubMedCentralPubMedCrossRefGoogle Scholar
  102. Yilmaz LS, Bergsven LI, Noguera DR (2008) Systematic evaluation of single mismatch stability predictors for fluorescence in situ hybridization. Environ Microbiol 10(10):2872–2885. doi:10.1111/j.1462-2920.2008.01719.x PubMedCrossRefGoogle Scholar
  103. Yilmaz LS, Parnerkar S, Noguera DR (2011) mathFISH, a web tool that uses thermodynamics-based mathematical models for in silico evaluation of oligonucleotide probes for fluorescence in situ hybridization. Appl Environ Microbiol 77(3):1118–1122. doi:10.1128/aem. 01733-10 PubMedCentralPubMedCrossRefGoogle Scholar
  104. Yilmaz LS, Loy A, Wright ES, Wagner M, Noguera DR (2012) Modeling formamide denaturation of probe-target hybrids for improved microarray probe design in microbial diagnostics. PLoS ONE 7(8):e43862. doi:10.1371/journal.pone.0043862 PubMedCentralPubMedCrossRefGoogle Scholar
  105. Zhang T, Fang HHP (2006) Applications of real-time polymerase chain reaction for quantification of microorganisms in environmental samples. Appl Microbiol Biotechnol 70(3):281–289. doi:10.1007/s00253-006-0333-6 PubMedCrossRefGoogle Scholar
  106. Znosko BM, Silvestri SB, Volkman H, Boswell B, Serra MJ (2002) Thermodynamic parameters for an expanded nearest-neighbor model for the formation of RNA duplexes with single nucleotide bulges. Biochemistry 41(33):10406–10417. doi:10.1021/bi025781q PubMedCrossRefGoogle Scholar
  107. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31(13):3406–15. doi:10.1093/nar/gkg595 PubMedCentralPubMedCrossRefGoogle Scholar
  108. Zwirglmaler K, Ludwig W, Schleifer KH (2003) Improved fluorescence in situ hybridization of individual microbial cells using polynucleotide probes: the network hypothesis. Syst Appl Microbiol 26(3):327–337. doi:10.1078/072320203322497356 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Daniel R. Noguera
    • 1
    • 2
    • 6
  • Erik S. Wright
    • 3
    • 4
  • Pamela Camejo
    • 1
  • L. Safak Yilmaz
    • 5
  1. 1.Department of Civil and Environmental EngineeringUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Great Lakes Bioenergy Research CenterUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Systems Biology Theme, Wisconsin Institute for DiscoveryUniversity of Wisconsin-MadisonMadisonUSA
  4. 4.Department of BacteriologyUniversity of Wisconsin-MadisonMadisonUSA
  5. 5.Program in Systems BiologyUniversity of Massachusetts Medical SchoolWorcesterUSA
  6. 6.MadisonUSA

Personalised recommendations