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BioMed Research International
Volume 2015 (2015), Article ID 892013, 12 pages
http://dx.doi.org/10.1155/2015/892013
Research Article

454-Pyrosequencing Analysis of Bacterial Communities from Autotrophic Nitrogen Removal Bioreactors Utilizing Universal Primers: Effect of Annealing Temperature

1Department of Civil Engineering, University of Granada, Campus de Fuentenueva, s/n, 18071 Granada, Spain
2Institute of Water Research, University of Granada, C/Ramón y Cajal 4, 18071 Granada, Spain
3Department of Biotechnology, Technical University of Delft, Julianalaan 67, 2628 BC Delft, Netherlands

Received 20 October 2014; Accepted 26 February 2015

Academic Editor: Weixing Feng

Copyright © 2015 Alejandro Gonzalez-Martinez et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Strous, J. A. Fuerst, E. H. M. Kramer et al., “Missing lithotroph identified as new planctomycete,” Nature, vol. 400, no. 6743, pp. 446–449, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Dalsgaard, B. Thamdrup, and D. E. Canfield, “Anaerobic ammonium oxidation (anammox) in the marine environment,” Research in Microbiology, vol. 156, no. 4, pp. 457–464, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. M. M. M. Kuypers, A. O. Silekers, G. Lavik et al., “Anaerobic ammonium oxidation by anammox bacteria in the Black Sea,” Nature, vol. 422, no. 6932, pp. 608–611, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Thamdrup, T. Dalsgaard, M. M. Jensen, O. Ulloa, L. Farías, and R. Escribano, “Anaerobic ammonium oxidation in the oxygen-deficient waters off Northern Chile,” Limnology and Oceanography, vol. 51, no. 5, pp. 2145–2156, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Ganesh, D. J. Parris, E. F. Delong, and F. J. Stewart, “Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone,” ISME Journal, vol. 8, no. 1, pp. 187–211, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. L.-D. Shen, S. Liu, L.-P. Lou et al., “Broad distribution of diverse anaerobic ammonium-oxidizing bacteria in Chinese agricultural soils,” Applied and Environmental Microbiology, vol. 79, no. 19, pp. 6167–6172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. S. M. Kotay, B. L. Mansell, M. Hogsett, H. Pei, and R. Goel, “Anaerobic ammonia oxidation (ANAMMOX) for side-stream treatment of anaerobic digester filtrate process performance and microbiology,” Biotechnology and Bioengineering, vol. 110, no. 4, pp. 1180–1192, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. A. González-Martínez, J. M. Poyatos, E. Hontoria, J. Gonzalez-Lopez, and F. Osorio, “Treatment of effluents polluted by nitrogen with new biological technologies based on autotrophic nitrification-denitrification processes,” Recent Patents on Biotechnology, vol. 5, no. 2, pp. 74–84, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. M. S. M. Jetten, M. Wagner, J. Fuerst, M. C. M. van Loosdrecht, G. Kuenen, and M. Strous, “Microbiology and application of the anaerobic ammonium oxidation (‘anammox’) process,” Current Opinion in Biotechnology, vol. 12, no. 3, pp. 283–288, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Sri Shalini and K. Joseph, “Nitrogen management in landfill leachate: application of SHARON, ANAMMOX and combined SHARON-ANAMMOX process,” Waste Management, vol. 32, no. 12, pp. 2385–2400, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Liu, D. Li, H. Zeng et al., “Biodiversity and quantification of functional bacteria in completely autotrophic nitrogen-removal over nitrite (CANON) process,” Bioresource Technology, vol. 118, pp. 399–406, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. Z.-X. Quan, S.-K. Rhee, J.-E. Zuo et al., “Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor,” Environmental Microbiology, vol. 10, no. 11, pp. 3130–3139, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. Hu, D. R. Speth, K.-J. Francoijs, Z.-X. Quan, and M. S. M. Jetten, “Metagenome analysis of a complex community reveals the metabolic blueprint of anammox bacterium ‘Candidatus Jettenia asiatica’,” Frontiers in Microbiology, vol. 3, article 366, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. Q. Yang, Z. Jia, R. Liu, and J. Chen, “Molecular diversity and anammox activity of novel planctomycete-like bacteria in the wastewater treatment system of a full-scale alcohol manufacturing plant,” Process Biochemistry, vol. 42, no. 2, pp. 180–187, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. X.-R. Li, B. Du, H.-X. Fu et al., “The bacterial diversity in an anaerobic ammonium-oxidizing (anammox) reactor community,” Systematic and Applied Microbiology, vol. 32, no. 4, pp. 278–289, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. B.-J. Ni, B.-L. Hu, F. Fang et al., “Microbial and physicochemical characteristics of compact anaerobic ammonium-oxidizing granules in an upflow anaerobic sludge blanket reactor,” Applied and Environmental Microbiology, vol. 76, no. 8, pp. 2652–2656, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Han, Y.-T. Huang, J.-G. Lin, and J.-D. Gu, “A comparison of two 16S rRNA gene-based PCR primer sets in unraveling anammox bacteria from different environmental samples,” Applied Microbiology and Biotechnology, vol. 97, no. 24, pp. 10521–10529, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Xie, Z. Lv, C. Hu, X. Yang, and X. Li, “Nitrogen removal through different pathways in an aged refuse bioreactor treating mature landfill leachate,” Applied Microbiology and Biotechnology, vol. 97, no. 20, pp. 9225–9234, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. M. S. M. Jetten, L. van Niftrik, M. Strous, B. Kartal, J. T. Keltjens, and H. J. M. Op Den Camp, “Biochemistry and molecular biology of anammox bacteria,” Critical Reviews in Biochemistry and Molecular Biology, vol. 44, no. 2-3, pp. 65–84, 2009. View at Google Scholar · View at Scopus
  20. P. Junier, V. Molina, C. Dorador et al., “Phylogenetic and functional marker genes to study ammonia-oxidizing microorganisms (AOM) in the environment,” Applied Microbiology and Biotechnology, vol. 85, no. 3, pp. 425–440, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. S. E. Dowd, T. R. Callaway, R. D. Wolcott et al., “Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP),” BMC Microbiology, vol. 8, article 125, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Rychlik, W. J. Spencer, and R. E. Rhoads, “Optimization of the annealing temperature for DNA amplification in vitro,” Nucleic Acids Research, vol. 18, no. 21, pp. 6409–6412, 1990. View at Publisher · View at Google Scholar · View at Scopus
  23. X. Chen, P. Liu, and H.-H. Chou, “Whole-genome thermodynamic analysis reduces siRNA off-target effects,” PLoS ONE, vol. 8, no. 3, Article ID e58326, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Dobrijevic, G. Di Liberto, K. Tanaka et al., “High-throughput system for the presentation of secreted and surface-exposed proteins from Gram-positive bacteria in functional metagenomic studies,” PLoS ONE, vol. 8, no. 6, Article ID e65956, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Nakano, Y. Morizane, N. Makisaka et al., “Development of a highly sensitive immuno-PCR assay for the measurement of α-galactosidase A protein levels in serum and plasma,” PLoS ONE, vol. 8, no. 11, Article ID e78588, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. R. C. Edgar, “Search and clustering orders of magnitude faster than BLAST,” Bioinformatics, vol. 26, no. 19, pp. 2460–2461, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. R. C. Edgar, B. J. Haas, J. C. Clemente, C. Quince, and R. Knight, “UCHIME improves sensitivity and speed of chimera detection,” Bioinformatics, vol. 27, no. 16, pp. 2194–2200, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. D. E. Wood and S. L. Salzberg, “Kraken: ultrafast metagenomic sequence classification using exact alignments,” Genome Biology, vol. 15, no. 3, article R46, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. R. K. Colwell, A. Chao, N. J. Gotelli et al., “Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages,” Journal of Plant Ecology, vol. 5, no. 1, pp. 3–21, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. R Development Core Team, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2008, http://www.R-project.org.
  31. B. Haegeman, J. Hamelin, J. Moriarty, P. Neal, J. Dushoff, and J. S. Weitz, “Robust estimation of microbial diversity in theory and in practice,” The ISME Journal, vol. 7, no. 6, pp. 1092–1101, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Malhotra, L. Foltz, W. C. Mahoney, and P. A. Schueler, “Interaction and effect of annealing temperature on primers used in differential display RT-PCR,” Nucleic Acids Research, vol. 26, no. 3, pp. 854–856, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Bru, F. Martin-Laurent, and L. Philippot, “Quantification of the detrimental effect of a single primer-template mismatch by real-time PCR using the 16S rRNA gene as an example,” Applied and Environmental Microbiology, vol. 74, no. 5, pp. 1660–1663, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. W. R. L. van der Star, A. I. Miclea, U. G. J. M. van Dongen, G. Muyzer, C. Picioreanu, and M. C. M. van Loosdrecht, “The membrane bioreactor: a novel tool to grow anammox bacteria as free cells,” Biotechnology and Bioengineering, vol. 101, no. 2, pp. 286–294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Lotti, Monitoraggio del proceso anammox: aspetti fisiologici per unutilizzo in piena scala, Università degli Studi della Basilicata, Potenza, Italy, 2011.
  36. Z. Hu, T. Lotti, M. de Kreuk et al., “Nitrogen removal by a nitritation-anammox bioreactor at low temperature,” Applied and Environmental Microbiology, vol. 79, no. 8, pp. 2807–2812, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. M. J. Sergeant, C. Constantinidou, T. Cogan, C. W. Penn, and M. J. Pallen, “High-throughput sequencing of 16s rRNA gene amplicons: Effects of extraction procedure, primer length and annealing temperature,” PLoS ONE, vol. 7, no. 5, Article ID e38094, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Wang and R. E. Levin, “Thermal factors influencing detection of Vibrio vulnificus using real-time PCR,” Journal of Microbiological Methods, vol. 69, no. 2, pp. 358–363, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. J. T. Hsu, S. Das, and S. Mohapatra, “Polymerase chain reaction engineering,” Biotechnology and Bioengineering, vol. 55, no. 2, pp. 359–366, 1997. View at Publisher · View at Google Scholar
  40. M. J. Claesson, Q. Wang, O. O'Sullivan et al., “Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions,” Nucleic Acids Research, vol. 38, article e200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Ishii and M. Fukui, “Optimization of annealing temperature to reduce bias caused by a primer mismatch in multitemplate PCR,” Applied and Environmental Microbiology, vol. 67, no. 8, pp. 3753–3755, 2001. View at Publisher · View at Google Scholar
  42. R. Sipos, A. J. Székely, M. Palatinszky, S. Révész, K. Márialigeti, and M. Nikolausz, “Effect of primer mismatch, annealing temperature and PCR cycle number on 16S rRNA gene-targetting bacterial community analysis,” FEMS Microbiology Ecology, vol. 60, no. 2, pp. 341–350, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. K. H. Hecker and K. H. Roux, “High and low annealing temperatures increase both specificity and yield in touchdown and stepdown PCR,” BioTechniques, vol. 20, no. 3, pp. 478–485, 1996. View at Google Scholar · View at Scopus
  44. K. Malhotra, L. Foltz, W. C. Mahoney, and P. A. Schueler, “Interaction and effect of annealing temperature on primers used in differential display RT-PCR,” Nucleic Acids Research, vol. 26, no. 3, pp. 854–856, 1998. View at Publisher · View at Google Scholar · View at Scopus