Next-generation approaches to the microbial ecology of food fermentations

  • Bokulich, Nicholas A. ;
  • Mills, David A.
  • Received : 2012.05.21
  • Published : 2012.07.31


Food fermentations have enhanced human health since the dawn of time and remain a prevalent means of food processing and preservation. Due to their cultural and nutritional importance, many of these foods have been studied in detail using molecular tools, leading to enhancements in quality and safety. Furthermore, recent advances in high-throughput sequencing technology are revolutionizing the study of food microbial ecology, deepening insight into complex fermentation systems. This review provides insight into novel applications of select molecular techniques, particularly next-generation sequencing technology, for analysis of microbial communities in fermented foods. We present a guideline for integrated molecular analysis of food microbial ecology and a starting point for implementing next-generation analysis of food systems.


Food fermentation;Microbial community profiling;Molecular profiling tools;Next-generation sequencing;TRFLP


  1. Hayes, M., Ross, R. P., Fitzgerald, G. F. and Stanton, C. (2007) Putting microbes to work: dairy fermentation, cell factories and bioactive peptides. Part I: overview. Biotechnol. J. 2, 426-434.
  2. Nout, M. J. (2009) Rich nutrition from the poorest - cereal fermentations in Africa and Asia. Food Microbiol. 26, 685-692.
  3. Ross, R. P., Morgan, S. and Hill, C. (2002) Preservation and fermentation: past, present and future. Int. J. Food Microbiol. 79, 3-16.
  4. Rouse, S. and van Sinderen, D. (2008) Bioprotective potential of lactic acid bacteria in malting and brewing. J. Food Prot. 71, 1724-1733.
  5. Ray, R. C. and Sivakumar, P. S. (2009) Traditional and novel fermented foods and beverages from tropical root and tuber crops: review. Int. J. Food Sci. Technol. 44, 1073-1087.
  6. Tannock, G. W. (2002) Probiotics and prebiotics: Where are we going? (eds.), Caister Academic Press, Norfork, England.
  7. Heard, G. M. and Fleet, G. H. (1986) Evaluation of selective media for enumeration of yeast during wine fermentation. J. Appl. Bacteriol. 60, 477-481.
  8. Ampe, F., Omar, N. B., Moizan, C., Wacher, C. and Guyot, J. P. (1999) Polyphasic study of the spatial distribution of microorganisms in mexican pozol, a fermented maize dough, demonstrates the need for cultivation- independent methods to investigate traditional fermentations. Appl. Environ. Microbiol. 65, 5464-5473.
  9. Divol, B. and Lonvaud-Funel, A. (2005) Evidence for viable but nonculturable yeasts in botrytis-affected wine. J. Appl. Microbiol. 99, 85-93.
  10. Millet, V. and Lonvaud-Funel, A. (2000) The viable but non-culturable state of wine micro-organisms during storage. Lett. Appl. Microbiol. 30, 136-141.
  11. Bottari, B., Ercolini, D., Gatti, M. and Neviani, E. (2006) Application of FISH technology for microbiological analysis: current state and prospects. Appl. Microbiol. Biotechnol. 73, 485-494.
  12. Andorra, I., Monteiro, M., Esteve-Zarzoso, B., Albergaria, H. and Mas, A. (2011) Analysis and direct quantification of Saccharomyces cerevisiae and Hanseniaspora guilliermondii populations during alcoholic fermentation by fluorescence in situ hybridization, flow cytometry and quantitative PCR. Food Microbiol. 28, 1483-1491.
  13. Xufre, A., Albergaria, H., Inacio, J., Spencer-Martins, I. and Girio, F. (2006) Application of fluorescence in situ hybridisation (FISH) to the analysis of yeast population dynamics in winery and laboratory grape must fermentations. Int. J. Food Microbiol. 108, 376-384.
  14. Blasco, L., Ferrer, S. and Pardo, I. (2003) Development of specific fluorescent oligonucleotide probes for in situ identification of wine lactic acid bacteria. FEMS Microbiol. Lett. 225, 115-123.
  15. Yasuhara, T., Yuuki, T. and Kagami, N. (2001) Novel quantitative method for detection of Pectinatus using rRNA targeted fluorescent probes. J. Am. Soc. Brew. Chem. 59, 117-121.
  16. Babot, J. D., Hidalgo, M., Arganaraz-Martinez, E., Apella, M. C. and Perez Chaia, A. (2011) Fluorescence in situ hybridization for detection of classical propionibacteria with specific 16S rRNA-targeted probes and its application to enumeration in Gruyere cheese. Int. J. Food Microbiol. 145, 221-228.
  17. Bottari, B., Santarelli, M., Neviani, E. and Gatti, M. (2010) Natural whey starter for Parmigiano Reggiano: culture-independent approach. J. Appl. Microbiol. 108, 1676-1684.
  18. Mounier, J., Monnet, C., Jacques, N., Antoinette, A. and Irlinger, F. (2009) Assessment of the microbial diversity at the surface of Livarot cheese using culture-dependent and independent approaches. Int. J. Food Microbiol. 133, 31-37.
  19. Ercolini, D., Hill, P. J. and Dodd, C. E. (2003) Development of a fluorescence in situ hybridization method for cheese using a 16S rRNA probe. J. Microbiol. Methods 52, 267-271.
  20. Klug, B., Rodler, C., Koller, M., Wimmer, G., Kessler, H. H., Grube, M. and Santigli, E. (2011) Oral biofilm analysis of palatal expanders by fluorescence in-situ hybridization and confocal laser scanning microscopy. J. Vis. Exp. 20, 2967.
  21. Postollec, F., Falentin, H., Pavan, S., Combrisson, J. and Sohier, D. (2011) Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiol. 28, 848-861.
  22. Lucas, P. M., Claisse, O. and Lonvaud-Funel, A. (2008) High frequency of histamine-producing bacteria in the enological environment and instability of the histidine decarboxylase production phenotype. Appl. Environ. Microbiol. 74, 811-817.
  23. Arena, M. P., Romano, A., Capozzi, V., Beneduce, L., Ghariani, M., Grieco, F., Lucas, P. and Spano, G. (2011) Expression of Lactobacillus brevis IOEB 9809 tyrosine decarboxylase and agmatine deiminase genes in wine correlates with substrate availability. Lett. Appl. Microbiol. 53, 395-402.
  24. Ladero, V., Coton, M., Fernandez, M., Buron, N., Cruz Martin, M., Guichard, H., Coton, E. and Alvarez, M. A. (2011) Biogenic amines content in Spanish and French natural ciders: Application of qPCR for quantitative detection of biogenic amine-producers. Food Microbiol. 28, 554-561.
  25. Fernandez, M., del Rio, B., Linares, D. M., Martin, M. C. and Alvarez, M. A. (2006) Real-time polymerase chain reaction for quantitative detection of histamine-producing bacteria: use in cheese production. J. Dairy Sci. 89, 3763-3769.
  26. Torriani, S., Gatto, V., Sembeni, S., Tofalo, R., Suzzi, G., Belletti, N., Gardini, F. and Bover-Cid, S. (2008) Rapid detection and quantification of tyrosine decarboxylase gene (tdc) and its expression in gram-positive bacteria associated with fermented foods using PCR-based methods. J. Food Prot. 71, 93-101.
  27. Ibarburu, I., Aznar, R., Elizaquivel, P., Garcia-Quintans, N., Lopez, P., Munduate, A., Irastorza, A. and Duenas, M. T. (2010) A real-time PCR assay for detection and quantification of 2-branched (1,3)-$\beta$-D-glucan producing lactic acid bacteria in cider. Int. J. Food Microbiol. 143, 26-31.
  28. Mendes-Ferreira, A., Barbosa, C., Jimenez-Marti, E., Del Olmo, M. L. and Mendes-Faia, A. (2010) The wine yeast strain-dependent expression of genes implicated in sulfide production in response to nitrogen availability. J. Microbiol. Biotechnol. 20, 1314-1321.
  29. Haakensen, M. C., Butt, L., Chaban, B., Deneer, H., Ziola, B. and Dowgiert, T. (2007) horA-Speciric real-time PCR for detection of beer-spoilage lactic acid bacteria. J. Am. Soc. Brew. Chem. 65, 157-165.
  30. Cho, G. S., Krauss, S., Huch, M., Du Toit, M. and Franz, C. M. (2011) Development of a quantitative PCR for detection of Lactobacillus plantarum starters during wine malolactic fermentation. J. Microbiol. Biotechnol. 21, 1280-1286.
  31. Muyzer, G., Dewaal, E. C. and Uitterlinden, A. G. (1993) Profiling of complex microbial populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S ribosomal RNA. Appl. Environ. Microbiol. 59, 695-700.
  32. Kisand, V. and Wikner, J. (2003) Limited resolution of 16S rDNA DGGE caused by melting properties and closely related DNA sequences. J. Microbiol. Meth. 54, 183-191.
  33. Sekiguchi, H., Tomioka, N., Nakahara, T. and Uchiyama, H. (2001) A single band does not always represent single bacterial strains in denaturing gradient gel electrophoresis analysis. Biotechnol. Lett. 23, 1205-1208.
  34. Nubel, U., Engelen, B., Felske, A., Snaidr, J., Wieshuber, A., Amann, R. I., Ludwig, W. and Backhaus, H. (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J. Bacteriol. 178, 5636-5643.
  35. Polz, M. F. and Cavanaugh, C. M. (1998) Bias in template- to-product ratios in multitemplate PCR. Appl. Environ. Microbiol. 64, 3724-3730.
  36. Speksnijder, A., Kowalchuk, G. A., De Jong, S., Kline, E., Stephen, J. R. and Laanbroek, H. J. (2001) Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Appl. Environ. Microbiol. 67, 469-472.
  37. Tourlomousis, P., Kemsley, E. K., Ridgway, K. P., Toscano, M. J., Humphrey, T. J. and Narbad, A. (2010) PCR-denaturing gradient gel electrophoresis of complex microbial communities: a two-step approach to address the effect of gel-to-gel variation and allow valid comparisons across a large dataset. Microb. Ecol. 59, 776-786.
  38. Cocolin, L., Bisson, L. F. and Mills, D. A. (2000) Direct profiling of the yeast dynamics in wine fermentations. FEMS Microbiol. Lett. 189, 81-87.
  39. Renouf, V., Claisse, O., Miot-Sertier, C. and Lonvaud- Funel, A. (2006) Lactic acid bacteria evolution during winemaking: use of rpoB gene as a target for PCR-DGGE analysis. Food Microbiol. 23, 136-145.
  40. Ercolini, D. (2004) PCR-DGGE fingerprinting: novel strategies for detection of microbes in food. J. Microbiol. Meth. 56, 297-314.
  41. Kaplan, C. W. and Kitts, C. L. (2003) Variation between observed and true Terminal Restriction Fragment length is dependent on true TRF length and purine content. J. Microbiol. Meth. 54, 121-125.
  42. Marsh, T. L. (2005) Culture-independent microbial community analysis with terminal restriction fragment length polymorphism. Methods Enzymol. 397, 308-329.
  43. Hartmann, M., Enkerli, J. and Widmer, F. (2007) Residual polymerase activity-induced bias in terminal restriction fragment length polymorphism analysis. Env. Microbiol. 9, 555-559.
  44. Egert, M. and Friedrich, M. W. (2003) Formation of pseudo- terminal restriction fragments, a PCR-related bias affecting terminal restriction fragment length polymorphism analysis of microbial community structure. Appl. Environ. Microbiol. 69, 2555-2562.
  45. Bokulich, N. A. and Mills, D. A. (2012) Differentiation of mixed lactic acid bacteria communities in beverage fermentations using targeted terminal restriction fragment length polymorphism. Food Microbiol. 31, 126-132. doi:10.1016/
  46. Culman, S. W., Gauch, H. G., Blackwood, C. B. and Thies, J. E. (2008) Analysis of T-RFLP data using analysis of variance and ordination methods: A comparative study. J. Microbiol. Meth. 75, 55-63.
  47. Blackwood, C. B., Marsh, T. L., Kim, S. H. and Paul, E. A. (2003) Terminal restriction fragment length polymorphism data analysis for quantitative comparison of microbial communities. Appl. Environ. Microbiol. 69, 926-932.
  48. Blackwood, C. B., Hudleston, D., Zak, D. R. and Buyer, J. S. (2007) Interpreting ecological diversity indices applied to terminal restriction fragment length polymorphism data: insights from simulated microbial communities. Appl. Environ. Microbiol. 73, 5276-5283.
  49. Schutte, U. M. E., Abdo, Z., Bent, S. J., Shyu, C., Williams, C. J., Pierson, J. D. and Forney, L. J. (2008) Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl. Microbiol. Biotechnol. 80, 365-380.
  50. Liu, W. T., Marsh, T. L., Cheng, H. and Forney, L. J. (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63, 4516-4522.
  51. Rademaker, J. L. W., Hoolwerf, J. D., Wagendorp, A. A. and te Giffel, M. C. (2006) Assessment of microbial population dynamics during yoghurt and hard cheese fermentation and ripening by DNA population fingerprinting. Int. Dairy J. 16, 457-466.
  52. Rademaker, J. L. W., Peinhopf, M., Rijnen, L., Bockelmann, W. and Noordman, W. H. (2005) The surface microflora dynamics of bacterial smear-ripened Tilsit cheese determined by T-RFLP DNA population fingerprint analysis. Int. Dairy J. 15, 785-794.
  53. Sanchez, J. I., Rossetti, L., Martinez, B., Rodriguez, A. and Giraffa, G. (2006) Application of reverse transcriptase PCR-based T-RFLP to perform semi-quantitative analysis of metabolically active bacteria in dairy fermentations. J. Microbiol. Meth. 65, 268-277.
  54. Bokulich, N. A., Hwang, C. F., Liu, S., Boundy-Mills, K. and Mills, D. A. (2012) Profiling the yeast communities of wine using terminal restriction fragment length polymorphism. Am. J. Enol. Vitic. 63, doi:10.5344/ajev.2011.11077.
  55. Bokulich, N. A., Bamforth, C. W. and Mills, D. A. (2012) Brewhouse-resident microbiota are responsible for multi- stage fermentation of american coolship ale. PLoS ONE 7, e35507. doi:10.1371/journal.pone.0035507.
  56. Bokulich, N. A., Joseph, C. M. L., Allen, G., Benson, A. K. and Mills, D. A. (2012) Next-Generation Sequencing Reveals Significant Bacterial Diversity of Botrytized Wine. PLoS ONE 7, e36357. doi:10.1371/journal.pone.0036357.
  57. Marcobal, A., Underwood, M. and Mills, D. A. (2008) Rapid determination of the bacterial composition of commercial probiotic products by terminal restriction fragment length polymorphism analysis. J. Pediatr. Gastroenterol. Nutr. 46, 608-611.
  58. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y. J., Chen, Z., Dewell, S. B., Du, L., Fierro, J. M., Gomes, X. V., Godwin, B. C., He, W., Helgesen, S., Ho, C. H., Irzyk, G. P., Jando, S. C., Alenquer, M. L., Jarvie, T. P., Jirage, K. B., Kim, J. B., Knight, J. R., Lanza, J. R., Leamon, J. H., Lefkowitz, S. M., Lei, M., Li, J., Lohman, K. L., Lu, H., Makhijani, V. B., McDade, K. E., McKenna, M. P., Myers, E. W., Nickerson, E., Nobile, J. R., Plant, R., Puc, B. P., Ronan, M. T., Roth, G. T., Sarkis, G. J., Simons, J. F., Simpson, J. W., Srinivasan, M., Tartaro, K. R., Tomasz, A., Vogt, K. A., Volkmer, G. A., Wang, S. H., Wang, Y., Weiner, M. P., Yu, P., Begley, R. F. and Rothberg, J. M. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380.
  59. Bennett, S. (2004) Solexa Ltd. Pharmacogenomics 5, 433-438.
  60. Kuczynski, J., Lauber, C. L., Walters, W. A., Parfrey, L. W., Clemente, J. C., Gevers, D. and Knight, R. (2012) Experimental and analytical tools for studying the human microbiome. Nat. Rev. Genet. 13, 47-58.
  61. Liu, Z., Lozupone, C. A., Hamady, M., Bushman, F. D. and Knight, R. (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids. Res. 35, e120.
  62. Kiyohara, M., Koyanagi, T., Matsui, H., Yamamoto, K., Take, H., Katsuyama, Y., Tsuji, A., Miyamae, H., Kondo, T., Nakamura, S., Katayama, T. and Kumagai, H. (2012) Changes in microbiota population during fermentation of narezushi as revealed by pyrosequencing analysis. Biosci. Biotechnol. Biochem. 76, 48-52.
  63. Koyanagi, T., Kiyohara, M., Matsui, H., Yamamoto, K., Kondo, T., Katayama, T. and Kumagai, H. (2011) Pyrosequencing survey of the microbial diversity of 'narezushi', an archetype of modern Japanese sushi. Lett. Appl. Microbiol. 53, 635-640.
  64. Sakamoto, N., Tanaka, S., Sonomoto, K. and Nakayama, J. (2011) 16S rRNA pyrosequencing-based investigation of the bacterial community in nukadoko, a pickling bed of fermented rice bran. Int. J. Food Microbiol. 144, 352-359.
  65. Li, X. R., Ma, E. B., Yan, L. Z., Meng, H., Du, X. W., Zhang, S. W. and Quan, Z. X. (2011) Bacterial and fungal diversity in the traditional Chinese liquor fermentation process. Int. J. Food Microbiol. 146, 31-37.
  66. Alegria, A., Szczesny, P., Mayo, B., Bardowski, J. and Kowalczyk, M. (2012) Biodiversity in Oscypek, a traditional Polish cheese, determined by culture-dependent and -independent approaches. Appl. Environ. Microbiol. 78, 1890-1898.
  67. Humblot, C. and Guyot, J. P. (2009) Pyrosequencing of tagged 16S rRNA gene amplicons for rapid deciphering of the microbiomes of fermented foods such as pearl millet slurries. Appl. Environ. Microbiol. 75, 4354-4361.
  68. Roh, S. W., Kim, K. H., Nam, Y. D., Chang, H. W., Park, E. J. and Bae, J. W. (2010) Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequencing. ISME J. 4, 1-16.
  69. Jung, M. J., Nam, Y. D., Roh, S. W. and Bae, J. W. (2012) Unexpected convergence of fungal and bacterial communities during fermentation of traditional Korean alcoholic beverages inoculated with various natural starters. Food Microbiol. 30, 112-123.
  70. Kim, Y. S., Kim, M. C., Kwon, S. W., Kim, S. J., Park, I. C., Ka, J. O. and Weon, H. Y. (2011) Analyses of bacterial communities in meju, a Korean traditional fermented soybean bricks, by cultivation-based and pyrosequencing methods. J. Microbiol. 49, 340-348.
  71. Nam, Y. D., Lee, S. Y. and Lim, S. I. (2012) Microbial community analysis of Korean soybean pastes by next-generation sequencing. Int. J. Food Microbiol. 155, 36-42.
  72. Nam, Y. D., Park, S. L. and Lim, S. I. (2012) Microbial Composition of the Korean Traditional Food "kochujang" Analyzed by a Massive Sequencing Technique. J. Food Sci. 77, M250-256.
  73. Park, E. J., Chun, J., Cha, C. J., Park, W. S., Jeon, C. O. and Bae, J. W. (2012) Bacterial community analysis during fermentation of ten representative kinds of kimchi with barcoded pyrosequencing. Food Microbiol. 30, 197-204.
  74. Park, E. J., Kim, K. H., Abell, G. C., Kim, M. S., Roh, S. W. and Bae, J. W. (2011) Metagenomic analysis of the viral communities in fermented foods. Appl. Environ Microbiol. 77, 1284-1291.
  75. Lozupone, C. A. and Knight, R. (2005) UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228-8235.
  76. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Gonzalez Pena, A., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J. and Knight, R. (2010) Qiime allows analysis of high-throughput community sequence data. Nat. Methods 7, 335-336.
  77. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J. and Weber, C. F. (2009) Introducing mothur: open-source, platform- independent, community-supported software for describing and comparing microbial communities. Appl. Environ Microbiol. 75, 7537-7541.
  78. Zaneveld, J. R., Parfrey, L. W., Van Treuren, W., Lozupone, C., Clemente, J. C., Knights, D., Stombaugh, J., Kuczynski, J. and Knight, R. (2011) Combined phylogenetic and genomic approaches for the high-throughput study of microbial habitat adaptation. Trends Microbiol. 19, 472-482.
  79. Nilsson, R. H., Ryberg, M., Kristiansson, E., Abarenkov, K., Larsson, K. H. and Koljalg, U. (2006) Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE 1, e59.
  80. Tedersoo, L., Abarenkov, K., Nilsson, R. H., Schussler, A., Grelet, G. A., Kohout, P., Oja, J., Bonito, G. M., Veldre, V., Jairus, T., Ryberg, M., Larsson, K. H. and Koljalg, U. (2011) Tidying up international nucleotide sequence databases: ecological, geographical and sequence quality annotation of its sequences of mycorrhizal fungi. PLoS ONE 6, e24940.
  81. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., Andersen, G. L., Knight, R. and Hugenholtz, P. (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618.
  82. De Santis, T., Hugenholtz, P., Larsen, N., Rojas, N., Brodie, E., Keller, K., Huber, T., Dalevi, D., Hu, P. and Andersen, G. L. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072.
  83. Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J. and Glockner, F. O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids. Res. 35, 7188-7196.
  84. Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A. S., McGarrel, D. M., Marsh, T. L., Garrity, G. M. and Tiedje, J. M. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids. Res. 37, D141-D145.
  85. Abarenkov, K., Nilsson, R. H., Larsson, K.-H., Alexander, I. J., Eberhardt, U., Erland, S., Høiland, K., Kjøller, R., Larsson, E., Pennanen, T., Sen, R., Taylor, A. F. S., Tedersoo, L., Ursing, B. M., Vrålstad, T., Liimatainen, K., Peintner, U. and Kõljalg, U. (2010) The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytol. 186, 1447-1452.
  86. Soergel, D. A. W., Dey, N., Knight, R. and Brenner, S. E. (2012) Selection of primers for optimal taxonomic classification of environmental 16S rRNA gene sequences. ISME J. 7, doi: 10.1038/ismej.2011.208.
  87. Nilsson, R. H., Kristiansson, E., Ryberg, M., Hallenberg, N. and Larsson, K. H. (2008) Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol. Bioinform. Online 4, 193-201.
  88. Simon, C. and Daniel, R. (2011) Metagenomic analyses: past and future trends. Appl. Environ. Microbiol. 77, 1153-1161.
  89. Lauber, C. L., Zhou, N., Gordon, J. I., Knight, R. and Fierer, N. (2010) Effect of storage conditions on the assessment of bacterial community structure in soil and human-associated samples. FEMS Microbiol. Lett. 307, 80-86.
  90. Li, F., Hullar, M. A. and Lampe, J. W. (2007) Optimization of terminal restriction fragment polymorphism (TRFLP) analysis of human gut microbiota. J. Microbiol. Meth. 68, 303-311.
  91. Rossen, L., Norskov, P., Holmstrom, K. and Rasmussen, O. F. (1992) Inhibition of PCR by components of food samples, microbial diagnostic assays and DNA-extraction solutions. Int. J. Food Microbiol. 17, 37-45.
  92. Nocker, A., Cheung, C. Y. and Camper, A. K. (2006) Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J. Microbiol. Meth. 67, 310-320.
  93. Nocker, A., Richter-Heitmann, T., Montijn, R., Schuren, F. and Kort, R. (2010) Discrimination between live and dead cells in bacterial communities from environmental water samples analyzed by 454 pyrosequencing. Int. Microbiol. 13, 59-65.
  94. Andorra, I., Esteve-Zarzoso, B., Guillamon, J. M. and Mas, A. (2010) Determination of viable wine yeast using DNA binding dyes and quantitative PCR. Int. J. Food Microbiol. 144, 257-262.
  95. Anderson, I. C. and Cairney, J. W. G. (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Env. Microbiol. 6, 769-779.
  96. Kurtzman, C. and Robnett, C. J. (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek 73, 331-371.
  97. Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A. and Chen, W. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109, 6241-6246.
  98. Nilsson, R. H., Ryberg, M., Abarenkov, K., Sjokvist, E. and Kristiansson, E. (2009) The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol. Lett. 296, 97-101.
  99. Bellemain, E., Carlsen, T., Brochmann, C., Coissac, E., Taberlet, P. and Kauserud, H. (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol. 10, 189.
  100. Sakai, M., Matsuka, A., Komura, T. and Kanazawa, S. (2004) Application of a new PCR primer for terminal restriction fragment length polymorphism analysis of the bacterial communities in plant roots. J. Microbiol. Methods. 59, 81-89.
  101. Martin, K. J. and Rygiewicz, P. T. (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol. 5, 28.
  102. Sakamoto, N., Tanaka, S., Sonomoto, K. and Nakayama, J. (2011) 16S rRNA pyrosequencing-based investigation of the bacterial community in nukadoko, a pickling bed of fermented rice bran. Int. J. Food Microbiol. 144, 352-359.
  103. Kruger, D., Kapturska, D., Fischer, C., Daniel, R. and Wubet, T. (2012) Diversity Measures in Environmental Sequences Are Highly Dependent on Alignment Quality-Data from ITS and New LSU Primers Targeting Basidiomycetes. PLoS ONE 7, e32139.

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