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Successful Enrichment of Rarely Found Candidatus Anammoxoglobus propionicus from Leachate Sludge

  • Hsu, Shu-Chuan (Department of Environmental Engineering, National Chung Hsing University) ;
  • Lai, Yen-Chun (Department of Environmental Engineering, National Chung Hsing University) ;
  • Hsieh, Ping-Heng (Department of Environmental Engineering, National Chung Hsing University) ;
  • Cheng, Pun-Jen (Department of Environmental Engineering, National Chung Hsing University) ;
  • Wong, Suen-Shin (Department of Environmental Engineering, National Chung Hsing University) ;
  • Hung, Chun-Hsiung (Department of Environmental Engineering, National Chung Hsing University)
  • Received : 2014.01.09
  • Accepted : 2014.04.03
  • Published : 2014.07.28

Abstract

Bacteria that mediate the anaerobic oxidation of ammonium (anammox) have been detected in natural ecosystems, as well as various wastewater treatment systems. In this study, sludge from a particular landfill leachate anaerobic treatment system was selected as the incubation seed for anammox microorganism enrichment owing to its possible anammox activity. Transmission electron microscopy observation, denaturing gradient gel electrophoresis analysis, and cloning/sequencing techniques were applied to identify the diversity of anammox microorganisms throughout the incubation. During the early stage of operation, the diversity of anammox microorganisms was similar to the original complex microbes in the seed sludge. However, as incubation time increased, the anammox microorganism diversity within the system that was originally dominated by Candidatus (Ca.) Brocadia sp. was replaced by Ca. Anammoxoglobus propionicus. The domination of Ca. Anammoxoglobus propionicus produced a stable removal of ammonia (70 mg-N/l) and nitrite (90 mg-N/l), and the total nitrogen removal efficiency was maintained at nearly 95%. The fluorescence in situ hybridization results showed that Ca. Anammoxoglobus propionicus was successfully enriched from $1.8{\pm}0.6%$ initially to $65{\pm}5%$ after 481 days of operation. Therefore, the present results demonstrated the feasibility of enriching Ca. Anammoxoglobus propionicus from leachate sludge, even though the original cell count was extremely low. Application of this seldom found anammox organism could offer an alternative to current ammonia-nitrogen treatment.

Keywords

References

  1. Altschul SF, Gish W, Miller W, Meyers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2
  2. Amano T, Yoshinaga I, Okada K, Yamagishi T, Ueda S, Obuchi A, et al. 2007. Detection of anammox activity and diversity of anammox bacteria-related 16S rRNA genes in coastal marine sediment in Japan. Microb. Environ. 22: 232-242. https://doi.org/10.1264/jsme2.22.232
  3. APHA. 1995. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC, USA.
  4. Daverey A, Su S-H, Huang Y-T, Lin J-G. 2012. Nitrogen removal from opto-electronic wastewater using the simultaneous partial nitrification, anaerobic ammonium oxidation and denitrification (SNAD) process in sequencing batch reactor. Bioresour. Technol. 113: 225-231. https://doi.org/10.1016/j.biortech.2011.12.004
  5. Egli K, Fanger U, Alvarez PJJ, Siegrist H, van der Meer JR, Zehnder AJB. 2001. Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch. Microbiol. 175: 198-207. https://doi.org/10.1007/s002030100255
  6. Güven D, Dapena A, Kartal B, Schmid MC, Maas B, van de Pas-Schoonen K, et al. 2005. Propionate oxidation by and methanol inhibition of anaerobic ammonium-oxidizing bacteria. Appl. Environ. Microbiol. 71: 1066-1071. https://doi.org/10.1128/AEM.71.2.1066-1071.2005
  7. Humbert S, Tarnawski S, Fromin N, Mallet M-P, Aragno M, Zopfi J. 2010. Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. Int. Soc. Microb. Ecol. J. 4: 450-454.
  8. Innerebner G, Insam H, Franke-Whittle IH, Wett B. 2007. Identification of anammox bacteria in a full-scale deammonification plant making use of anaerobic ammonia oxidation. Syst. Appl. Microbiol. 30: 408-412. https://doi.org/10.1016/j.syapm.2007.02.001
  9. Jaeschke A, Op den Camp HJM, Harhangi H, Klimiuk A, Hopmans EC, Jetten MSM, et al. 2009. 16S rRNA gene and lipid biomarker evidence for anaerobic ammonium-oxidizing bacteria (anammox) in California and Nevada hot springs. FEMS Microbiol. Ecol. 67: 343-350. https://doi.org/10.1111/j.1574-6941.2008.00640.x
  10. Kartal B, Kuypers MMM, Lavik G, Schalk J, Op den Camp HJM, Jetten MSM, Strous M. 2007. Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ. Microbiol. 9: 635-642. https://doi.org/10.1111/j.1462-2920.2006.01183.x
  11. Kartal B, Rattray J, van Niftrik L, van de Vossenberg J, Schmid MC, Webb RI, et al. 2007. Candidatus "Anammoxoglobus propionicus" a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol. 30: 39-49. https://doi.org/10.1016/j.syapm.2006.03.004
  12. Kuai L, Verstraete W. 1998. Ammonium removal by the oxygen-limited autotrophic nitrification-denitrification system. Appl. Environ. Microbiol. 64: 4500-4506.
  13. Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, et al. 2005. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102: 6478-6483. https://doi.org/10.1073/pnas.0502088102
  14. Long A, Heitman J, Tobias C, Philips R, Song B. 2013. Cooccurring anammox, denitrification, and codenitrification in agricultural soils. Appl. Environ. Microbiol. 79: 168-176. https://doi.org/10.1128/AEM.02520-12
  15. Mulder JW, Van Loosdrecht MCM, Hellinga C, Van Kempen R. 2001. Full-scale application of the SHARON process for treatment of rejection water of digested sludge dewatering. Water Sci. Technol. 43: 127-134.
  16. Neef A, Amann R, Schlesner H, Schleifer K-H. 1998. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 144: 3257-3266. https://doi.org/10.1099/00221287-144-12-3257
  17. Park H, Rosenthal A, Ramalingam K, Fillos J, Chandran K. 2010. Linking community profiles, gene expression and Nremoval in anammox bioreactors treating municipal anaerobic digestion reject water. Environ. Sci. Technol. 44: 6110-6116. https://doi.org/10.1021/es1002956
  18. Penton CR, Devol AH, Tiedje JM. 2006. Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl. Environ. Microbiol. 72: 6829-6832. https://doi.org/10.1128/AEM.01254-06
  19. Rattray J, van de Vossenberg J, Hopmans E, Kartal B, van Niftrik L, Rijpstra W, et al. 2008. Ladderane lipid distribution in four genera of anammox bacteria. Arch. Microbiol. 190: 51-66. https://doi.org/10.1007/s00203-008-0364-8
  20. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, et al. 2000. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst. Appl. Microbiol. 23: 93-106 https://doi.org/10.1016/S0723-2020(00)80050-8
  21. Schmid M, Walsh K, Webb R, Rijpstra WI, van de Pas- Schoonen K, Verbruggen MJ, et al. 2003. Candidatus "Scalindua brodae", sp. nov., Candidatus "Scalindua wagneri", sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol. 26: 529-538. https://doi.org/10.1078/072320203770865837
  22. Schmid MC, Maas B, Dapena A, van de Pas-Schoonen K, van de Vossenberg J, Kartal B, et al. 2005. Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl. Environ. Microbiol. 71: 1677-1684. https://doi.org/10.1128/AEM.71.4.1677-1684.2005
  23. Schmid MC, Risgaard-Petersen N, Van De Vossenberg J, Kuypers MMM, Lavik G, Petersen J, et al. 2007. Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ. Microbiol. 9: 1476-1484. https://doi.org/10.1111/j.1462-2920.2007.01266.x
  24. Sinninghe Damsté JS, Rijpstra WIC, Geenevasen JAJ, Strous M, Jetten MSM. 2005. Structural identification of ladderane and other membrane lipids of planctomycetes capable of anaerobic ammonium oxidation (anammox). FEBS J. 272: 4270-4283. https://doi.org/10.1111/j.1742-4658.2005.04842.x
  25. Strous M, Heijnen JJ, Kuenen JG, Jetten MSM. 1998. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Microbiol. Biotechnol. 50: 589-596. https://doi.org/10.1007/s002530051340
  26. Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, et al. 2 006. D eciphering the evolution a nd metabolism of an anammox bacterium from a community genome. Nature 440: 790-794. https://doi.org/10.1038/nature04647
  27. Third KA, Paxman J, Schmid M, Strous M, Jetten MSM, and Cord-Ruwisch R. 2005. Enrichment of anammox from activated sludge and its application in the CANON process. Microb. Ecol. 49: 236-244. https://doi.org/10.1007/s00248-004-0186-4
  28. Van de Graaf AA, de Bruijn P, Robertson LA, Jetten MSM, Kuenen JG. 1996. Autotrophic growth of anaerobic ammonium-oxidizing microorganisms in a fluidized bed reactor. Microbiology 142: 2187-2196. https://doi.org/10.1099/13500872-142-8-2187
  29. Van De Vossenberg J, Rattray JE, Geerts W, Kartal B, Van Niftrik L, Van Donselaar EG, et al. 2008. Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ. Microbiol. 10: 3120-3129. https://doi.org/10.1111/j.1462-2920.2008.01643.x
  30. Van Dongen U, Jetten MSM, Van Loosdrecht MCM. 2001. The SHARON-anammox process for treatment of ammonium rich wastewater. Water Sci. Technol. 44: 153-160.
  31. van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Webb RI, Fuerst JA, et al. 2008. Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome C proteins. J. Bacteriol. 190: 708-717. https://doi.org/10.1128/JB.01449-07
  32. Wang C-C, Lee P-H, Kumar M, Huang Y-T, Sung S, Lin J-G. 2010. Simultaneous partial nitrification, anaerobic ammonium oxidation and denitrification (SNAD) in a full-scale landfillleachate treatment plant. J. Hazard. Mater. 175: 622-628. https://doi.org/10.1016/j.jhazmat.2009.10.052
  33. Winkler MKH, Yang J, Kleerebezem R, Plaza E, Trela J, Hultman B, van Loosdrecht MCM. 2012. Nitrate reduction by organotrophic anammox bacteria in a nitritation/anammox granular sludge and a moving bed biofilm reactor. Bioresour. Technol. 114: 217-223. https://doi.org/10.1016/j.biortech.2012.03.070
  34. Xiao Y, Zeng G, Yang Z, Liu YS, Ma Y, Yang L, et al. 2009. Coexistence of nitrifiers, denitrifiers and anammox bacteria in a sequencing batch biofilm reactor as revealed by PCRDGGE. J. Appl. Microbiol. 106: 496-505. https://doi.org/10.1111/j.1365-2672.2008.04017.x
  35. Yapsakli K, Aliyazicioglu C, Mertoglu B. 2011. Identification and quantitative evaluation of nitrogen-converting organisms in a full-scale leachate treatment plant. J. Environ. Manag. 92: 714-723. https://doi.org/10.1016/j.jenvman.2010.10.017
  36. Zilles JL, Peccia J, Kim M-W, Hung C-H, Noguera DR. 2002. Involvement of Rhodocyclus-related organisms in phosphorus removal in full-scale wastewater treatment plants. Appl. Environ. Microbiol. 68: 2763-2769. https://doi.org/10.1128/AEM.68.6.2763-2769.2002

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