Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Anaerobic Ammonium-Oxidizing Bacteria in Cow Manure Composting

  • Wang, Tingting (College of Resources and Environment, Northeast Agricultural University) ;
  • Cheng, Lijun (College of Resources and Environment, Northeast Agricultural University) ;
  • Zhang, Wenhao (College of Resources and Environment, Northeast Agricultural University) ;
  • Xu, Xiuhong (College of Resources and Environment, Northeast Agricultural University) ;
  • Meng, Qingxin (College of Resources and Environment, Northeast Agricultural University) ;
  • Sun, Xuewei (College of Resources and Environment, Northeast Agricultural University) ;
  • Liu, Huajing (College of Resources and Environment, Northeast Agricultural University) ;
  • Li, Hongtao (College of Resources and Environment, Northeast Agricultural University) ;
  • Sun, Yu (College of Resources and Environment, Northeast Agricultural University)
  • Received : 2017.02.27
  • Accepted : 2017.05.11
  • Published : 2017.07.28
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Abstract

Composting is widely used to transform waste into valuable agricultural organic fertilizer. Anaerobic ammonium-oxidizing (anammox) bacteria play an important role in the global nitrogen cycle, but their role in composting remains poorly understood. In the present study, the community structure, diversity, and abundance of anammox bacteria were analyzed using cloning and sequencing methods by targeting the 16S rRNA gene and the hydrazine oxidase gene (hzo) in samples isolated from compost produced from cow manure and rice straw. A total of 25 operational taxonomic units were classified based on 16S rRNA gene clone libraries, and 14 operational taxonomic units were classified based on hzo gene clone libraries. The phylogenetic tree analysis of the 16S rRNA gene and deduced HZO protein sequences from the corresponding encoding genes indicated that the majority of the obtained clones were related to the known anammox bacteria Candidatus "Brocadia," Candidatus "Kuenenia," and Candidatus "Scalindua." The abundances of anammox bacteria were determined by quantitative PCR, and between $2.13{\times}10^5$ and $1.15{\times}10^6$ 16S rRNA gene copies per gram of compost were found. This study provides the first demonstration of the existence of anammox bacteria with limited diversity in cow manure composting.

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References

  1. Jetten MS, Lv N, Strous M, Kartal B, Keltjens JT, Hj ODC. 2009. Biochemistry and molecular biology of anammox bacteria. Crit. Rev. Biochem. Mol. 44: 65-84. https://doi.org/10.1080/10409230902722783
  2. Mulder A, Graaf AAVD, Robertson LA, Kuenen JG. 1995. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol. Ecol. 16: 177-188. https://doi.org/10.1111/j.1574-6941.1995.tb00281.x
  3. Kartal B, Niftrik LV, Rattray J, Van De Vossenberg J, Schmid MC, Damste JS, et al. 2008. Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol. Ecol. 63: 46-55. https://doi.org/10.1111/j.1574-6941.2007.00408.x
  4. Schmidt I, Sliekers O, Schmid M, Cirpus I, Strous M, Bock E, et al. 2002. Aerobic and anaerobic ammonia oxidizing bacteria - competitors or natural partners? FEMS Microbiol. Ecol. 39: 175-181.
  5. Schmid M, Walsh K, Webb R, Rijpstra WIC, van de Pas-Schoonen K. 2003. Candidatus "Scalindua brodae", sp. nov., Candidatus "Scalindua wagneri", sp. nov., the two new species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol. 26: 529-538. https://doi.org/10.1078/072320203770865837
  6. Kartal B, Rattray J, Niftrik LAV, Vossenberg JVD, 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
  7. Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, et al. 2008. Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ. Microbiol. 10: 3130-3139. https://doi.org/10.1111/j.1462-2920.2008.01642.x
  8. Li M, Hong YG, Cao HL, Gu JD. 2013. Community structures and distribution of anaerobic ammonium oxidizing and nirS-encoding nitrite-reducing bacteria in surface sediments of the South China Sea. Microb. Ecol. 66: 281-296. https://doi.org/10.1007/s00248-012-0175-y
  9. Schmid MC, Nils RP, Jack VDV, 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
  10. Kuypers MM, 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
  11. Yoshinaga I, Amano T, Yamagishi T, Okada K, Ueda S, Sako Y, et al. 2011. Distribution and diversity of anaerobic ammonium oxidation (anammox) bacteria in the sediment of a eutrophic freshwater lake, Lake Kitaura, Japan. Microbes Environ. 26: 189-197. https://doi.org/10.1264/jsme2.ME10184
  12. Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM. 2006. Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ. Microbiol. 8: 1857-1863. https://doi.org/10.1111/j.1462-2920.2006.01074.x
  13. Sun W, Xu MY, Wu WM, Guo J, Xia CY, Sun GP, et al. 2013. Molecular diversity and distribution of anammox community in sediments of the Dongjiang River, a drinking water source of Hong Kong. J. Appl. Microbiol. 116: 464-476.
  14. Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J. 2010. Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J. 4: 450-454. https://doi.org/10.1038/ismej.2009.125
  15. Hu BL, Rush D, van der Biezen E, Zheng P, van Mullekom M, Schouten S, et al. 2011. New anaerobic, ammonium-oxidizing community enriched from peat soil. Appl. Environ. Microbiol. 77: 966-971. https://doi.org/10.1128/AEM.02402-10
  16. Bai R, Chen X, He JZ, Shen JP, Zhang LM. 2015. Erratum to: Candidatus brocadia and Candidatus kuenenia predominated in anammox bacterial community in selected Chinese paddy soils. J. Soil Sediment. 15: 1-10. https://doi.org/10.1007/s11368-014-0946-9
  17. Wang J, Gu JD. 2013. Dominance of Candidatus scalindua species in anammox community revealed in soils with different duration of rice paddy cultivation in northeast China. Appl. Microbiol. Biotechnol. 97: 1785-1798. https://doi.org/10.1007/s00253-012-4036-x
  18. Mahimairaja S, Bolan NS, Hedley MJ, Macgregor AN. 1994. Losses and transformation of nitrogen during composting of poultry manure with different amendments: an incubation experiment. Bioresour. Technol. 47: 265-273. https://doi.org/10.1016/0960-8524(94)90190-2
  19. Maeda K, Hanajima D, Toyoda S, Yoshida N, Morioka R, Osada T. 2011. Microbiology of nitrogen cycle in animal manure compost. Microb. Biotechnol. 4: 700-709. https://doi.org/10.1111/j.1751-7915.2010.00236.x
  20. De Gannes V, E udoxie G , Dyer D H, H ick ey WJ. 2012. Diversity and abundance of ammonia oxidizing archaea in tropical compost systems. Front. Microbiol. 3: 244.
  21. Zeng G, Yu Z, Chen Y, Zhang J, Li H, Yu M, Zhao M. 2011. Response of compost maturity and microbial community composition to pentachlorophenol (PCP)-contaminated soil during composting. Bioresour. Technol. 102: 5905-5911. https://doi.org/10.1016/j.biortech.2011.02.088
  22. Abad M, Noguera P, Puchades R, Maquieira A, Noguera V. 2002. Physico-chemical and chemical properties of some coconut coir dusts for use as a peat substitute for containerised ornamental plants. Bioresour. Technol. 82: 241-245. https://doi.org/10.1016/S0960-8524(01)00189-4
  23. Kimberly AE, Roberts MG. 1905. A method for the direct determination of organic nitrogen by the Kjeldahl process. Public Health Pap. Rep. 31: 109-122.
  24. Li M, Gu JD. 2011. Advances in methods for detection of anaerobic ammonium oxidizing (anammox) bacteria. Appl. Microbiol. Biotechnol. 90: 1241-1252. https://doi.org/10.1007/s00253-011-3230-6
  25. 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: 309-320.
  26. Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MMM, et al. 2008. Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ. Microbiol. 10: 3140-3149. https://doi.org/10.1111/j.1462-2920.2008.01732.x
  27. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013.MEGA6: molecular evolutionary genetics analysis version6.0. Mol. Biol. Evol. 30: 2725-2729. https://doi.org/10.1093/molbev/mst197
  28. Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, et al. 2007. Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol. Oceanogr. 52: 923-933. https://doi.org/10.4319/lo.2007.52.3.0923
  29. Schloss PD, Westcott SL, Ryabin T. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541. https://doi.org/10.1128/AEM.01541-09
  30. Good IJ. 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40: 237-264. https://doi.org/10.1093/biomet/40.3-4.237
  31. Mathur SP, Owen G, Dinel H, Schnitzer M. 1993. Determination of compost bio maturity: literature review. Biol. Agric. Hortic. 10: 65-85. https://doi.org/10.1080/01448765.1993.9754655
  32. Hirsch MD, Long ZT, Song B. 2011. Anammox bacterial diversity in various aquatic ecosystems based on the detection of hidrazine oxidase genes (hzoA/ hzoB). Microb. Ecol. 61: 264-276. https://doi.org/10.1007/s00248-010-9743-1
  33. Hu BL, Shen LD, Xu XY, Zheng P, Hu AH, Chen TT, et al. 2011. Anaerobic ammonium oxidation (anammox) in different natural ecosystems. Biochem. Soc. Trans. 39: 1811-1816. https://doi.org/10.1042/BST20110711
  34. Jaeschke A, Op den Camp HJ, Harhangi MH, Klimiuk A, Hopmans EC, Jetten MS, 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
  35. Li H, Chen S, Mu BZ, Gu JD. 2010. Molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in hightemperature petroleum reservoirs. Microb. Ecol. 60: 771-783. https://doi.org/10.1007/s00248-010-9733-3
  36. Byrne N, Strous M, Crepeau V, Kartal B, Birrien JL, Schmid M, et al. 2009. Presence and activity of anaerobic ammoniumoxidizing bacteria at deep-sea hydrothermal vents. ISME J. 3: 117-123. https://doi.org/10.1038/ismej.2008.72
  37. Klotz MG, Schmid MC, Strous M, op den Camp HJ, Jetten MS, Hooper AB. 2008. Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ. Microbiol. 10: 3150-3163. https://doi.org/10.1111/j.1462-2920.2008.01733.x
  38. Yamada T, Araki S, Ikeda-Ohtsubo W, Okamura K, Hiraishi A, Ueda H, et al. 2013. Community structure and population dynamics of ammonia oxidizers in composting processes of ammonia-rich livestock waste. Syst. Appl. Microbiol. 36: 359-367. https://doi.org/10.1016/j.syapm.2013.02.001
  39. Li M, Hong Y, Klotz MG, Gu JD. 2010. A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl. Microbiol. Biotechnol. 86: 781-790. https://doi.org/10.1007/s00253-009-2361-5
  40. Neef A, Amann R, Schlesner H, Schleifer KH. 1999. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology. 144: 3257-3266.
  41. Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K, et al. 2007. Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl. Environ. Microbiol. 73: 1065-1072. https://doi.org/10.1128/AEM.01978-06
  42. Muyzer G, de Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59: 695.
  43. Neef A, Amann R, Schlesner H, Schleifer KH. 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
  44. Brosius J, Dull TJ, Noller HF. 1978. Complete nucleotide sequence of a 23s ribosomal RNA gene from Escherichia coli. Proc. Natl. Acad. Sci. USA 75: 4801-4805. https://doi.org/10.1073/pnas.75.10.4801
  45. Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Roser A, Koops HP, et al. 1998. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl. Environ. Microbiol. 64: 3042-3051.

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