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Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil

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Abstract

Nitrification is essential to the nitrogen cycle in paddy soils. However, it is still not clear which group of ammonia-oxidizing microorganisms plays more important roles in nitrification in the paddy soils. The changes in the abundance and composition of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) were investigated by real-time PCR, terminal restriction fragment length polymorphism, and clone library approaches in an acid red paddy soil subjected to long-term fertilization treatments, including treatment without fertilizers (CT); chemical fertilizer nitrogen (N); N and potassium (NK); N and phosphorus (NP); N, P, and K (NPK); and NPK plus recycled crop residues (NPK+C). The AOA population size in NPK+C was higher than those in CT, while minor changes in AOB population sizes were detected among the treatments. There were also some changes in AOA community composition responding to different fertilization treatments. Still few differences were detected in AOB community composition among the treatments. Phylogenetic analysis showed that the AOA sequences fell into two main clusters: cluster A and cluster soil/sediment. The AOB composition in this paddy soil was dominated by Nitrosospira cluster 12. These results suggested that the AOA were more sensitive than AOB to different fertilization treatments in the acid red paddy soil.

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References

  • Bowatte S, Asakawa S, Okada M, Kobayashi K, Kimura M (2007) Effect of elevated atmospheric CO2 concentration on ammonia oxidizing bacteria communities inhabiting in rice roots. Soil Sci Plant Nutr 53:32–39

    Article  CAS  Google Scholar 

  • Bowatte S, Jia Z, Ishihara R, Nakajima Y, Asakawa S, Kimura M (2006) Molecular analysis of the ammonia oxidizing bacterial community in the surface soil layer of Japanese paddy field. Soil Sci Plant Nutr 52:427–431

    Article  CAS  Google Scholar 

  • Boyle-Yarwood SA, Bottomley PJ, Myrold DD (2008) Community composition of ammonia-oxidizing bacteria and archaea in soils under stands of red alder and Douglas fir in Oregon. Environ Microbiol 10:2956–2965

    Article  PubMed  CAS  Google Scholar 

  • Briones AM, Okabe S, Umemiya Y, Ramsing N-B, Reichardt W, Okuyama H (2002) Influence of different cultivars on populations of ammonia-oxidizing bacteria in the root environment of rice. Appl Environ Microbiol 68:3067–3075

    Article  PubMed  CAS  Google Scholar 

  • Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10:1978–1987

    Article  PubMed  CAS  Google Scholar 

  • Chu HY, Morimoto S, Fujii T, Yagi K, Nishimura S (2010) Soil ammonia-oxidizing bacterial communities in paddy rice fields as affected by upland conversion history. Soil Sci Soc Am J 73:2026–2031

    Article  Google Scholar 

  • Compton JE, Watrud LS, Porteous LA, Degrood S (2004) Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard Forest. For Ecol Manage 196:143–158

    Article  Google Scholar 

  • Conrad R, Rothfuss F (1991) Methane oxidation in the soil surface layer of a flooded rice field and the effect of ammonium. Biol Fertil Soils 12:28–32

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624

    Article  CAS  Google Scholar 

  • Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33:855–869

    Article  PubMed  CAS  Google Scholar 

  • Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688

    Article  PubMed  CAS  Google Scholar 

  • Fujii C, Nakagawa T, Onodera Y, Matsutani N, Sasada K, Takahashi R, Tokuyama T (2010) Succession and community composition of ammonia-oxidizing archaea and bacteria in bulk soil of a Japanese paddy field. Soil Sci Plant Nutr 56:212–219

    Article  CAS  Google Scholar 

  • He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374

    Article  PubMed  CAS  Google Scholar 

  • Jia ZJ, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  PubMed  CAS  Google Scholar 

  • Kettler TA, Doran JW, Gilbert TL (2001) Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci Soc Am J 65:849–852

    Article  CAS  Google Scholar 

  • Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  Google Scholar 

  • Lam P, Jensen MM, Lavik G, McGinnis DF, Müller B, Schubert CJ, Amann R, Thamdrup B, Kuypers MMM (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 104:7104–7109

    Article  PubMed  CAS  Google Scholar 

  • Laverman AM, Speksnijder AGCL, Braster M, Kowalchuk GA, Verhoef HA, van Verseveld HW (2001) Spatiotemporal stability of an ammonia-oxidizing community in a nitrogen-saturated forest soil. Microb Ecol 42:35–45

    PubMed  CAS  Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  PubMed  CAS  Google Scholar 

  • Mintie AT, Heichen RS, Cromack K, Myrold DD, Bottomley PJ (2003) Ammonia-oxidizing bacteria along meadow-to-forest transects in the Oregon Cascade Mountains. Appl Environ Microbiol 69:3129–3136

    Article  PubMed  CAS  Google Scholar 

  • Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978

    Article  PubMed  CAS  Google Scholar 

  • Nicolaisen MH, Risgaard-Petersen N, Revsbech NP, Reichardt W, Ramsing NB (2004) Nitrification–denitrification dynamics and community structure of ammonia oxidizing bacteria in a high yield irrigated Philippine rice field. FEMS Microbiol Ecol 49:359–369

    Article  PubMed  CAS  Google Scholar 

  • Nugroho RA, Röling WFM, Laverman AM, Zoomer HR, Verhoef HA (2005) Presence of Nitrosospira cluster 2 bacteria corresponds to N transformation rates in nine acid Scots pine forest soils. FEMS Microbiol Ecol 53:473–481

    Article  PubMed  CAS  Google Scholar 

  • Offre P, Prosser JI, Nicol GW (2009) Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol Ecol 70:99–108

    Article  PubMed  CAS  Google Scholar 

  • Park H-D, Wells GF, Bae H, Criddle CS, Francis CA (2006) Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol 72:5643–5647

    Article  PubMed  CAS  Google Scholar 

  • Prosser JI (1989) Autotrophic nitrification in bacteria. Adv Microb Physiol 30:125–181

    Article  PubMed  CAS  Google Scholar 

  • Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops H-P, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  PubMed  CAS  Google Scholar 

  • Revsbech NP, Pedersen O, Reichardt W, Briones A (1999) Microsensor analysis of oxygen and pH in the rice rhizosphere under field and laboratory conditions. Biol Fertil Soils 29:379–385

    Article  Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    PubMed  CAS  Google Scholar 

  • Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10:1068–1079

    Article  PubMed  CAS  Google Scholar 

  • Schauss K, Focks A, Leininger S, Kotzerke A, Heuer H, Thiele-Bruhn S, Sharma S, Wilke BM, Matthies M, Smalla K, Munch JC, Amelung W, Kaupenjohann M, Schloter M, Schleper C (2009) Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11:446–456

    Article  PubMed  CAS  Google Scholar 

  • Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10:1601–1611

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995

    Article  PubMed  CAS  Google Scholar 

  • Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5:316–323

    Article  PubMed  CAS  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  PubMed  CAS  Google Scholar 

  • Wang YN, Ke XB, Wu LQ, Lu YH (2009) Community composition of ammonia-oxidizing bacteria and archaea in rice field soil as affected by nitrogen fertilization. Syst Appl Microbiol 32:27–36

    Article  PubMed  CAS  Google Scholar 

  • Wuchter C, Abbas B, Coolen MJL, Herfort L, Van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S, Damste JSS (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103:12317–12322

    Article  PubMed  CAS  Google Scholar 

  • Ying JY, Zhang LM, He JZ (2010) Putative ammonia-oxidizing bacteria and archaea in an acidic red soil with different land utilization patterns. Environ Microbiol Rep 2:304–312

    Article  CAS  Google Scholar 

  • Zhang LM, Offre PR, He JZ, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci USA 107:17240–17245

    Article  PubMed  CAS  Google Scholar 

  • Zhang LM, Wang M, Prosser JI, Zheng YM, He JZ (2009) Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol Ecol 70:208–217

    Article  CAS  Google Scholar 

  • Zheng Y, Zhang LM, Zheng YM, Di HJ, He JZ (2008) Abundance and community composition of methanotrophs in a Chinese paddy soil under long-term fertilization practices. J Soils Sediment 8:406–414

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Natural Science Foundation of China (41090281, 50921064, 41025004) and the Chinese Academy of Sciences (KSCX2-YW-G-072, International Partnership Program for Creative Research Teams of “Ecosystem Processes and Services”).

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Correspondence to Ji-Zheng He.

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Chen, X., Zhang, LM., Shen, JP. et al. Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil. Biol Fertil Soils 47, 323–331 (2011). https://doi.org/10.1007/s00374-011-0542-8

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