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Detection and Potential Abundances of Anammox Bacteria in the Paddy Soil

  • Khanal, Anamika (Department of Bioenvironmental Chemistry, College of Agriculture & Life Sciences, Jeonbuk National University) ;
  • Lee, Seul (Department of Bioenvironmental Chemistry, College of Agriculture & Life Sciences, Jeonbuk National University) ;
  • Lee, Ji-Hoon (Department of Bioenvironmental Chemistry, College of Agriculture & Life Sciences, Jeonbuk National University)
  • Received : 2020.02.09
  • Accepted : 2020.02.28
  • Published : 2020.03.31

Abstract

BACKGROUND: Microbes that govern a unique biochemical process of oxidizing ammonia into dinitrogen gas, such as anaerobic ammonium oxidation (anammox) have been reported to play a pivotal role in agricultural soils and in oceanic environments. However, limited information for anammox bacterial abundance and distribution in the terrestrial habitats has been known. METHODS AND RESULTS: Phylogenetic and next-generation sequencing analyses of bacterial 16S rRNA gene were performed to examine potential anammox bacteria in paddy soils. Through clone libraries constructed by using the anammox bacteria-specific primers, some clones showed sequence similarities with Planctomycetes (87% to 99%) and anammox bacteria (94% to 95%). Microbial community analysis for the paddy soils by using Illumina Miseq sequencing of 16S rRNA gene at phylum level was dominated by unclassified Bacteria at 33.2 ± 7.6%, followed by Chloroflexi at 20.4 ± 2.0% and Acidobacteria at 17.0 ± 6.5%. Planctomycetes that anammox bacteria are belonged to was 1.5% (± 0.3) on average from the two paddy soils. CONCLUSION: We suggest evidence of anammox bacteria in the paddy soil. In addition to the relatively well-known microbial processes for nitrogen-cycle, anammox can be a potential contributor on the cycle in terrestrial environments such as paddy soils.

Keywords

References

  1. Shi Y, Hu SH, Lou JQ, Lu PL, Keller J, Yuan ZG (2013) Nitrogen removal from wastewater by coupling anammox and methane-dependent denitrification in a membrane biofilm reactor. Environmental Science & Technology, 47, 11577-11583. https://doi.org/10.1021/es402775z.
  2. deGraaf AAV, deBruijn P, Robertson LA, Jetten MSM, Kuenen JG (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology-UK, 142, 2187-2196. https://doi.org/10.1099/13500872-142-8-2187.
  3. Kartal B, Maalcke WJ, de Almeida NM, Cirpus I, Gloerich J, Geerts W, den Camp H, Harhangi HR, Janssen-Megens EM et al. (2011) Molecular mechanism of anaerobic ammonium oxidation. Nature, 479, 127-130. https://doi.org/10.1038/nature10453.
  4. Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D et al. (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 440, 790-794. https://doi.org/10.1038/nature04647.
  5. Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature, 400, 446-449. https://doi.org/10.1038/22749.
  6. Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nature Reviews Microbiology, 9, 403-413. https://doi.org/10.1038/nrmicro2578.
  7. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer K-H, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Systematic and Applied Microbiology, 23, 93-106. https://doi.org/10.1016/S0723-2020(00)80050-8.
  8. Kartal B, van Niftrik L, Rattray J, de Vossenberg J, Schmid MC, Damste JSS, Jetten MSM, Strous M (2008) Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiology Ecology, 63, 46-55. https://doi.org/10.1111/j.1574-6941.2007.00408.x.
  9. Kartal B, Kuypers MMM, Lavik G, Schalk J, den Camp H, Jetten MSM, Strous M (2007) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environmental Microbiology, 9, 635-642. https://doi.org/10.1111/j.1462-2920.2006.01183.x.
  10. Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee ST, Park YH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environmental Microbiology, 10, 3130-3139. https://doi.org/10.1111/j.1462-2920.2008.01642.x.
  11. Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jorgensen BB, Kuenen JG, Sinninghe Damste JS, Strous M, Jetten MSM (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature, 422, 608-611. https://doi.org/10.1038/nature01472.
  12. van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, Damste JSS, Strous M, Jetten MSM (2008) Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environmental Microbiology, 10, 3120-3129. https://doi.org/10.1111/j.1462-2920.2008.01643.x.
  13. Hong YG, Yin B, Zheng TL (2011) Diversity and abundance of anammox bacterial community in the deep-ocean surface sediment from equatorial Pacific. Applied Microbiology and Biotechnology, 89, 1233-1241. https://doi.org/10.1007/s00253-010-2925-4.
  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. The ISME Journal, 4, 450-454. https://doi.org/10.1038/ismej.2009.125.
  15. Sonthiphand P, Neufeld JD (2013) Evaluating primers for profiling anaerobic ammonia oxidizing bacteria within freshwater environments. PLoS ONE, 8, e57242. https://doi.org/10.1371/journal.pone.0057242.
  16. Harhangi HR, Le Roy M, van Alen T, Hu BL, Groen J, Kartal B, Tringe SG, Quan ZX, Jetten MSM et al. (2012) Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria. Applied and Environmental Microbiology, 78, 752-758. https://doi.org/10.1128/aem.07113-11.
  17. Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, Fuerst JA (2001) Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Archives of Microbiology, 175, 413-429. https://doi.org/10.1007/s002030100280.
  18. Kartal B, Koleva M, Arsov R, van der Star W, Jetten MSM, Strous M (2006) Adaptation of a freshwater anammox population to high salinity wastewater. Journal of Biotechnology, 126, 546-553. https://doi.org/10.1016/j.jbiotec.2006.05.012.
  19. Li M, Gu JD (2011) Advances in methods for detection of anaerobic ammonium oxidizing (anammox) bacteria. Applied Microbiology and Biotechnology, 90, 1241-1252. https://doi.org/10.1007/s00253-011-3230-6.
  20. Zhu GB, Wang SY, Wang WD, Wang Y, Zhou LL, Jiang B, Op den Camp HJM, Risgaard-Petersen N, Schwark L et al. (2013) Hotspots of anaerobic ammonium oxidation at land-freshwater interfaces. Nature Geoscience, 6, 103-107. https://doi.org/10.1038/ngeo1683.
  21. Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature, 437, 349-355. https://doi.org/10.1038/nature04159.
  22. Nie SA, Li H, Yang XR, Zhang ZJ, Weng BS, Huang FY, Zhu GB, Zhu YG (2015) Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. The ISME Journal, 9, 2059-2067. https://doi.org/10.1038/ismej.2015.25.
  23. Kuenen JG (2008) Anammox bacteria: from discovery to application. Nature Reviews Microbiology, 6, 320-326. https://doi.org/10.1038/nrmicro1857.
  24. Schulte E, Hopkins B (1996) Estimation of soil organic matter by weight loss-on-ignition. In: Soil organic matter: analysis and interpretation. pp 21-31.
  25. Dahnke W, Johnson GV (1990) Testing soils for available nitrogen. In: Soil Testing and Plant Analysis. pp 128-139.
  26. Heanes DL (1984) Determination of total organic-C in soils by an improved chromic-acid digestion and spectrophotometric procedure. Communications in Soil Science and Plant Analysis, 15, 1191-1213. https://doi.org/10.1080/00103628409367551.
  27. 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-UK, 144, 3257-3266. https://doi.org/10.1099/00221287-144-12-3257.
  28. Schmid M, Walsh K, Webb R, Rijpstra WIC, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J et al. (2003) Candidatus "Scalindua brodae", sp. nov., Candidatus "Scalindua wagneri", sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Systematic and Applied Microbiology, 26, 529-538. https://doi.org/10.1078/072320203770865837.
  29. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410. https://doi.org/10.1006/jmbi.1990.9999.
  30. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870-1874. https://doi.org/10.1093/molbev/msw054.
  31. Saitou N, Nei M (1987) The neighbor-joining methodA new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406-425. https://doi.org/10.1093/oxfordjournals.molbev.a040454.
  32. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America, 101, 11030-11035. https://doi.org/10.1073/pnas.0404206101.
  33. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537-7541. https://doi.org/10.1128/aem.01541-09.
  34. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-Index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environmental Microbiology, 79, 5112-5120. https://doi.org/10.1128/aem.01043-13.
  35. Rognes T, Flouri T, Nichols B, Quince C, Mahe F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4, e2584. https://doi.org/10.7717/peerj.2584.
  36. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41, D590-D596. https://doi.org/10.1093/nar/gks1219.
  37. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR et al. (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Research, 42, D633-D642. https://doi.org/10.1093/nar/gkt1244.
  38. Faoro H, Alves AC, Souza EM, Rigo LU, Cruz LM, Al-Janabi SM, Monteiro RA, Baura VA, Pedrosa FO (2010) Influence of Soil Characteristics on the Diversity of Bacteria in the Southern Brazilian Atlantic Forest. Applied and Environmental Microbiology, 76, 4744-4749. https://doi.org/10.1128/aem.03025-09.
  39. 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. Applied Microbiology and Biotechnology, 97, 1785-1798. https://doi.org/10.1007/s00253-012-4036-x.
  40. Jin RC, Yang GF, Yu JJ, Zheng P (2012) The inhibition of the anammox process: A review. Chemical Engineering Journal, 197, 67-79. https://doi.org/10.1016/j.cej.2012.05.014.
  41. Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, von Mering C, Vorholt JA (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. The ISME Journal, 6, 1378-1390. https://doi.org/10.1038/ismej.2011.192.