Responses of archaeal, bacterial, and functional microbial communities to growth season and nitrogen fertilization in rice fields

  • Yang JiEmail author
  • Ralf Conrad
  • Hua Xu
Original Paper


Fertilization provides excess N to soil microorganisms, thus possibly affecting soil microbial abundance, activity, and community composition during rice cultivation. The abundance and diversity of archaeal, bacterial, and functional microbial communities in rice soils upon different N fertilization regimes (no fertilizer, urea, and controlled-release fertilizer) were investigated by sampling four seasonal growth stages (seedling, tillering, vegetative, maturing) under field conditions. The abundance of bacteria was significantly affected by fertilization and seasonal time, while that of the archaea was not significantly affected. Analysis of terminal restriction fragment polymorphism (T-RFLP) of 16S rRNA genes showed no effect of N fertilization on the archaeal and bacterial community composition, but changes with plant growth time. This result was confirmed by the patterns of pyrosequencing of bacterial 16S rRNA genes. The function of the methanogenic microbial community was assayed at maturing plant growth stage by determining CH4 production rates and stable isotope fractionation in the absence and presence of methyl fluoride, an inhibitor of acetoclastic methanogenesis. N fertilization had a pronounced effect on the CH4 production rate but not on the pathway of CH4 formation. Additionally, the abundance of functional microbial communities related to CH4 and N2O emissions was measured by qPCR of functional genes. Similarly to the taxonomic composition, rice growth season showed a significant effect on the abundance of the functional microbial communities represented by the mcrA, pmoA, nirK, nirS, and nosZ genes, while N addition had usually no significant effect. A similar result was also obtained by correlation analysis between CH4 and N2O emission rates and abundances of the functional microbial gene copies. In summary, rice growth time had pronounced effects on abundance, composition, and function of microbial communities in the rice soil, while the effect of N fertilization was negligible on the level of both specific functional genes and taxonomic 16S rRNA genes.


Archaea Bacteria Functional gene N fertilization Growth season Methanogenesis Nitrous oxide 



We thank Melanie Klose and Peter Claus for technical support.

Funding information

The study was financially supported by the National Natural Sciences Foundation of China (Grant No. 41401268), Jiangsu Province Science Foundation (Grant No. BK20191400), and the Research Fund of the State Key Laboratory of Soil and Sustainable Agriculture, Nanjing Institute of Soil Science, Chinese Academy of Science (Grant No. Y412201414).

Supplementary material

374_2019_1404_MOESM1_ESM.pptx (337 kb)
ESM 1 (PPTX 337 kb)


  1. Ahamadou B, Huang Q, Chen W, Wen S, Zhang J, Mohamed I, Cai P, Liang W (2009) Microcalorimetric assessment of microbial activity in long-term fertilization experimental soils of southern China. FEMS Microbiol Ecol 70:186–195CrossRefGoogle Scholar
  2. Ahn JH, Song J, Kim BY, Kim MS, Joa JH, Weon HY (2012) Characterization of the bacterial and archaeal communities in rice field soils subjected to long-term fertilization practices. J Microbiol 50:754–765CrossRefPubMedGoogle Scholar
  3. Angel R, Conrad R (2013) Elucidating the microbial resuscitation cascade in biological soil crusts following a simulated rain event. Environ Microbiol 15:2799–2815PubMedGoogle Scholar
  4. Angel R, Matthies D, Conrad R (2011) Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS One 6:e20453CrossRefPubMedPubMedCentralGoogle Scholar
  5. Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862CrossRefPubMedGoogle Scholar
  6. Atere CT, Ge T, Zhu ZK, Tong C, Jones DL, Shibistova O, Guggenberger G, Wu J (2017) Rice rhizodeposition and carbon stabilisation in paddy soil are regulated via drying-rewetting cycles and nitrogen fertilisation. Biol Fertil Soils 53:407–417CrossRefGoogle Scholar
  7. Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryzasativa L.) cultivars. Plant Biol 3:139–148. CrossRefGoogle Scholar
  8. Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl Environ Microbiol 77:3846–3852CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917CrossRefPubMedGoogle Scholar
  10. Beauchamp EG (1997) Nitrous oxide emission from agricultural soils. Can J Soil Sci 77:113–123CrossRefGoogle Scholar
  11. Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bodelier PLE, Roslev P, Henckel T, Frenzel P (2000) Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403:421–424CrossRefPubMedGoogle Scholar
  13. Boer WD, Duyt SH, Laanbrock HJ (1988) Autotrophic nitrification in a fertilized acid health soil. Soil Biol Biochem 20:845–850CrossRefGoogle Scholar
  14. Bossio DA, Scow KM (1995) Impact of carbon and flooding on the metabolic diversity of microbial communities in soils. Appl Environ Microbiol 61:4043–4050PubMedPubMedCentralGoogle Scholar
  15. Braker G, Conrad R (2011) Diversity, structure, and size of N2O-producing microbial communities in soils-what matters for their functioning? Adv Appl Microbiol 75:33–70CrossRefPubMedGoogle Scholar
  16. Breidenbach B, Conrad R (2015) Seasonal dynamics of bacterial and archaeal methanogenic communities in flooded rice fields and effect of drainage. Front Microbiol 5:752CrossRefPubMedPubMedCentralGoogle Scholar
  17. Breidenbach B, Blaser MB, Klose M, Conrad R (2016) Crop rotation of flooded rice with upland maize impacts the resident and active methanogenic microbial community. Environ Microbiol 18:2868–2885CrossRefPubMedGoogle Scholar
  18. Burggraf S, Huber H, Stetter KO (1997) Reclassification of the crenarchaeal orders and families in accordance with 16S rRNA sequence data. Int J Syst Bacteriol 47:657–660CrossRefPubMedGoogle Scholar
  19. Cai ZC, Xing GX, Yan XY, Xu H, Tsuruta H, Yagi K, Minami K (1997) Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilizers and water management. Plant Soil 196:7–14CrossRefGoogle Scholar
  20. Cassman KG, Peng S, Olks DC, Ladha JK, Reichardt W, Dobermann A, Singh U (1998) Opportunities for increased nitrogen-use efficiency from improved resource management in irrigated rice systems. Field Crop Res 56:7–39CrossRefGoogle Scholar
  21. Chen X, Zhang LM, Shen JP, Wei WX, He JZ (2011) Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil. Biol Fertil Soils 47:323–331. CrossRefGoogle Scholar
  22. Chen Z, Liu J, Wu M, Xie X, Wu J, Wei W (2012) Differentiated response of denitrifying communities to fertilization regime in paddy soil. Microb Ecol 63:446–459CrossRefPubMedGoogle Scholar
  23. Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202CrossRefGoogle Scholar
  24. Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Adv Agron 96:1–63CrossRefGoogle Scholar
  25. Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292CrossRefPubMedGoogle Scholar
  26. Conrad R, Klose M, Noll M (2009) Functional and structural response of the methanogenic microbial community in rice field soil to temperature change. Environ Microbiol 11:1844–1853CrossRefPubMedGoogle Scholar
  27. Conrad R, Claus P, Casper P (2010) Stable isotope fractionation during the methanogenic degradation of organic matter in the sediment of an acidic bog Lake, Lake Grosse Fuchskuhle. Limnol Oceanogr 55:1932–1942CrossRefGoogle Scholar
  28. Conrad R, Ji Y, Noll M, Klose M, Claus P, Enrich-Prast A (2014) Response of the methanogenic microbial communities in Amazonian oxbow lake sediments to desiccation stress. Environ Microbiol 16:1682–1694CrossRefPubMedGoogle Scholar
  29. Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of Methanotrophs in Lake sediments. Appl Environ Microbiol 65:5066–5074PubMedPubMedCentralGoogle Scholar
  30. Cui PY, Fan FL, Yin C, Song AL, Huang PR, Tang YJ, Zhu P, Peng C, Li TQ, Wakelin SA, Liang YC (2016) Long-term organic and inorganic fertilization alters temperature sensitivity of N2O emissions and associated microbes. Soil Biol Biochem 93:131–141CrossRefGoogle Scholar
  31. Dong HB, Yao ZS, Zheng XH, Mei BL, Xie BH, Wang R, Deng J, Cui F, Zhu JG (2011) Effect of ammonium-based, nonsulfate fertilizers on CH4 emissions from a paddy field with a typical Chinese water management regime. Atmos Environ 45:1095–1101CrossRefGoogle Scholar
  32. Dunbar J, Ticknor LO, Kuske CR (2001) Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Appl Environ Microbiol 67:190–197CrossRefPubMedPubMedCentralGoogle Scholar
  33. Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71:8335–8343CrossRefPubMedPubMedCentralGoogle Scholar
  34. Erkel C, Kube M, Reinhardt R, Liesack W (2006) Genome of Rice cluster I archaea-the key methane producers in the rice rhizosphere. Science 313:370–372. CrossRefPubMedGoogle Scholar
  35. Fan XF, Yu HY, Wu QY, Ma J, Xu H, Yang JH, Zhuang Y (2016) Effects of fertilization on microbial abundance and emissions of greenhouse gases (CH4 and N2O) in rice paddy fields. Ecol Evol 6:1054–1063CrossRefPubMedPubMedCentralGoogle Scholar
  36. Fernandez Scavino A, Ji Y, Pump J, Klose M, Claus P, Conrad R (2013) Structure and function of the methanogenic microbial communities in Uruguayan soils shifted between pasture and irrigated rice fields. Environ Microbiol 15:2588–2602CrossRefGoogle Scholar
  37. Ge T, Li B, Zhu Z, Hu Y, Yuan H, Dorodnikov M, Jones D, Wu J, Kuzyakov Y (2017) Rice rhizodeposition and its utilization by microbial groups depends on N fertilization. Biol Fertil Soils 53:37–48CrossRefGoogle Scholar
  38. Grosskopf R, Janssen PH, Liesack W (1998) Diversity and structure of the methanogenic community in anoxic rice paddy soil microcosms as examined by cultivation and direct 16S rRNA gene sequence retrieval. Appl Environ Microbiol 64:960–969PubMedPubMedCentralGoogle Scholar
  39. Harter J, Krause HM, Schuettler S, Ruser R, Fromme M, Scholten T, Kappler A, Behrens S (2013) Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME J 8:660–674CrossRefPubMedPubMedCentralGoogle Scholar
  40. Henry S, Baudoin E, Lopez-Gutierrez JC, Martin-Laurent F, Brauman A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59:327–335CrossRefPubMedGoogle Scholar
  41. Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hussain Q, Liu YZ, Zhang AF, Pan GX, Li LQ, Zhang XH, Song XY, Cui LQ, Jin ZJ (2011) Variation of bacterial and fungal community structures in the rhizosphere of hybrid and standard rice cultivars and linkage to CO2 flux. FEMS Microbiol Ecol 78:116–128CrossRefPubMedGoogle Scholar
  43. Hutsch BW, Webster CP, Powlson DS (1994) Methane oxidation in soil as affected by land-use, soil-Ph and N-fertilization. Soil Biol Biochem 26:1613–1622CrossRefGoogle Scholar
  44. IPCC (2014) In: Core Writing Team, Pachauri RK, Meyer LA (eds) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland 151 ppGoogle Scholar
  45. Islam M, Singh Chauhan P, Kim Y, Kim M, Sa T (2011) Community level functional diversity and enzyme activities in paddy soils under different long-term fertilizer management practices. Biol Fertil Soils 47:599–604CrossRefGoogle Scholar
  46. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728CrossRefPubMedPubMedCentralGoogle Scholar
  47. Janssen PH, Frenzel P (1997) Inhibition of methanogenesis by methyl fluoride studies of pure and defined mixed cultures of anaerobic bacteria and archaea. Appl Environ Microbiol 63:4552–4557PubMedPubMedCentralGoogle Scholar
  48. Ji Y, Liu G, Ma J, Zhang GB, Xu H, Yagi K (2013) Effect of controlled-release fertilizer (CRF) mitigating N2O emission from paddy field in South China: a multi-year field observation. Plant Soil 371:473–486CrossRefGoogle Scholar
  49. Ji Y, Liu G, Ma J, Zhang GB, Xu H (2014) Effects of urea and controlled release urea fertilizers on methane emission from paddy fields: a multi-year field study. Pedosphere 24:662–673CrossRefGoogle Scholar
  50. Ji Y, Scavino AF, Klose M, Claus P, Conrad R (2015) Functional and structural responses of methanogenic microbial communities in Uruguayan soils to intermittent drainage. Soil Biol Biochem 89:238–247CrossRefGoogle Scholar
  51. Jia Z, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671. CrossRefPubMedGoogle Scholar
  52. Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kikuchi H, Watanabe T, Jia Z, Kimura M, Asakawa S (2007) Molecular analyses reveal stability of bacterial communities in bulk soil of a Japanese paddy field: estimation by denaturing gradient gel electrophoresis of 16S rRNA genes amplified from DNA accompanied with RNA. Soil Sci Plant Nutr 53:448–458CrossRefGoogle Scholar
  54. Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Koelbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157: 1–14Google Scholar
  55. Krüger M, Frenzel P, Kemnitz D, Conrad R (2005) Activity, structure and dynamics of the methanogenic archaeal community in a flooded Italian rice field. FEMS Microbiol Ecol 51:323–331CrossRefPubMedGoogle Scholar
  56. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–147Google Scholar
  57. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415CrossRefGoogle Scholar
  58. 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. CrossRefPubMedGoogle Scholar
  59. Li XL, Yuan WP, Xu H, Cai ZC, Yagi K (2011) Effect of timing and duration of midseason aeration on CH4 and N2O emissions from irrigated lowland rice paddies in China. Nutr Cycl Agroecosyst 91:293–305CrossRefGoogle Scholar
  60. Linquist B, Groenigen KJ, Adviento-Borbe MA, Pittelkow C, Kessel C (2012) An agronomic assessment of greenhouse gas emissions from major cereal crops. Glob Chang Biol 18:194–209CrossRefGoogle Scholar
  61. Lu Y, Rosencrantz D, Liesack W, Conrad R (2006) Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ Microbiol 8:1351–1360CrossRefPubMedGoogle Scholar
  62. Lüdemann H, Arth I, Liesack W (2000) Spatial changes in the bacterial community structure along a vertical oxygen gradient in flooded paddy soil cores. Appl Environ Microbiol 66:754–762CrossRefPubMedPubMedCentralGoogle Scholar
  63. Lueders T, Friedrich M (2000) Archaeal population dynamics during sequential reduction processes in rice field soil. Appl Environ Microbiol 66:2732–2742CrossRefPubMedPubMedCentralGoogle Scholar
  64. Ma K, Conrad R, Lu Y (2012) Responses of methanogen mcrA genes and their transcripts to an alternate dry/wet cycle of paddy field soil. Appl Environ Microbiol 78:445–454CrossRefPubMedPubMedCentralGoogle Scholar
  65. Maeda K, Morioka R, Hanajima D, Osada T (2010) The impact of using mature compost on nitrous oxide emission and the denitrifier community in the cattle manure composting process. Microb Ecol 59:25–36CrossRefPubMedGoogle Scholar
  66. Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461CrossRefGoogle Scholar
  67. Mendiburu F (2015) Agricolae: statistical procedures for agricultural research ver.1.2-1. Accessed May 2016
  68. Miller MN, Zebarth BJ, Dandie CE, Burton DL, Goyer C, Trevors JT (2008) Crop residue influence on the denitrification, N2O emissions and denitrifiers community abundance. Soil Biol Biochem 40:2553–2562CrossRefGoogle Scholar
  69. Mosier AR, Kroese C (2000) Potential impact on the global atmospheric N2O budget of the increased nitrogen input required to meet future global food demands. Chemosphere Global Change Sci 2:465–473CrossRefGoogle Scholar
  70. Mosier AR, Kroese C, Nevsion C (1998) Closing the global N2O budget: nitrogen oxide emissions through the agricultural nitrogen cycle. Nutr Cycl Agroecosyst 52:225–248CrossRefGoogle Scholar
  71. Nemergut DR, Townsend AR, Sattin SR, Freeman KR, Fierer N, Neff JC, Bowman WD, Schadt CW, Weintraub MN, Schmidt SK (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ Microbiol 10:3093–3105CrossRefPubMedGoogle Scholar
  72. Nicol GW, Webster G, Glover LA, Prosser JI (2004) Differential response of archaeal and bacterial communities to nitrogen inputs and pH changes in upland pasture rhizosphere soil. Environ Microbiol 6:861–867CrossRefPubMedGoogle Scholar
  73. Noll M, Matthies D, Frenzel P, Derakshani M, Liesack W (2005) Succession of bacterial community structure and diversity in a paddy soil oxygen gradient. Environ Microbiol 7:382–395CrossRefPubMedGoogle Scholar
  74. Oksanen J, Blanchet GF, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Szoecs E, Wagner H (2015) Vegan: community ecology package ver.2.3-0. Accessed May 2016
  75. Oneill JG, Wilkinson JF (1977) Oxidation of ammonia by methane oxidizing bacteria and the effects of ammonia on methane oxidation. J Gen Microbiol 100:407–412CrossRefGoogle Scholar
  76. Palmer K, Biasi C, Horn MA (2012) Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra. ISME J 6:1058–1077CrossRefPubMedGoogle Scholar
  77. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196CrossRefPubMedPubMedCentralGoogle Scholar
  78. Pump J, Conrad R (2014) Rice biomass production and carbon cycling in 13CO2 pulse-labeled microcosms with different soils under submerged conditions. Plant Soil 384:213–229. CrossRefGoogle Scholar
  79. Qin HL, Tang YF, Shen JL, Wang C, Chen CL, Yang J, Liu Y, Chen X, Li Y, Hou H (2018) Abundance of transcripts of functional gene reflects the inverse relationship between CH4 and N2O emissions during mid-season drainage in acidic paddy soil. Biol Fertil Soils 54:885–895CrossRefGoogle Scholar
  80. Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290CrossRefPubMedPubMedCentralGoogle Scholar
  81. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351CrossRefPubMedGoogle Scholar
  82. Schimel J (2000) Global change: rice, microbes and methane. Nature 403:375–377CrossRefPubMedGoogle Scholar
  83. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  84. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310CrossRefPubMedPubMedCentralGoogle Scholar
  85. Scholer A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489CrossRefGoogle Scholar
  86. Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:296. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Shrestha M, Shrestha PM, Frenzel P, Conrad R (2010) Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizosphere. ISME J 4:1545–1556. CrossRefPubMedGoogle Scholar
  88. Soil Survey Staff (1975) Soil taxonomy. U.S. Department of Agriculture Handbook, No. 436. USDA, Washington, DCGoogle Scholar
  89. Sun H, Zhang H, Min J, Feng Y, Shi W (2016) Controlled-release fertilizer, floating duckweed, and biochar affect ammonia volatilization and nitrous oxide emission from rice paddy fields irrigated with nitrogen-rich wastewater. Paddy Water Environ 14:105–111CrossRefGoogle Scholar
  90. Tao R, Wakelin SA, Liang Y, Hu B, Chu G (2018) Nitrous oxide emission and denitrifier communities in drip-irrigated calcareous soil as affected by chemical and organic fertilizers. Sci Total Environ 612:739–749CrossRefPubMedGoogle Scholar
  91. Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart-how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484CrossRefGoogle Scholar
  92. Wang G, Watanabe T, Jin J, Liu X, Kimura M, Asakawa S (2010) Methanogenic archaeal communities in paddy field soils in north-East China as evaluated by PCR-DGGE, sequencing and real-time PCR analyses. Soil Sci Plant Nutr 56:831–838CrossRefGoogle Scholar
  93. Wang JC, Xue C, Song Y, Wang L, Huang QW, Shen QR (2016) Wheat and rice growth stages and fertilization regimes alter soil bacterial community structure, but not diversity. Front Microbiol 7:1–13Google Scholar
  94. Wang Q, Liu YR, Zhang, Zhang CJ, Zhang LM, Han LL, Shen JP, He JZ (2017) Responses of soil nitrous oxide production and abundances and composition of associated microbial communities to nitrogen and water amendment. Biol Fertil Soils 53:601–611CrossRefGoogle Scholar
  95. Watanabe T, Kimura M, Asakawa S (2006) Community structure of methanogenic archaea in paddy field soil under double cropping (rice-wheat). Soil Biol Biochem 38:1264–1274CrossRefGoogle Scholar
  96. Watanabe T, Wang G, Taki K, Ohashi Y, Kimura M, Asakawa S (2010) Vertical changes in bacterial and archaeal communities with soil depth in Japanese paddy fields. Soil Sci Plant Nutr 56:705–715CrossRefGoogle Scholar
  97. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703CrossRefPubMedPubMedCentralGoogle Scholar
  98. Wessén E, Nyberg K, Jansson JK, Hallin S (2010) Responses of bacterial and archaeal ammonia oxidizers to soil organic and fertilizer amendments under long-term management. Appl Soil Ecol 45:193–200. CrossRefGoogle Scholar
  99. Wickham H (2009) ggplot2: elegant graphics for data analysis. springer, Dordrecht, the NetherlandsCrossRefGoogle Scholar
  100. Wolsing M, Priemé A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiol Ecol 48:261–271CrossRefPubMedGoogle Scholar
  101. Wu LQ, Ma K, Lu YH (2009) Prevalence of betaproteobacterial sequences in nifH gene pools associated with roots of modern rice cultivars. Microb Ecol 57:58–68CrossRefPubMedGoogle Scholar
  102. Wu M, Qin H, Chen Z, Wu J, Wei W (2011) Effect of long term fertilization on bacterial composition in rice paddy soil. Biol Fertil Soils 47:397–405CrossRefGoogle Scholar
  103. Wu ZH, Liu QS, Li ZY, Cheng W, Sun JM, Guo ZH, Li YM, Zhou JQ, Meng DL, Li HB, Lei P, Yin HQ (2018) Environmental factors shaping the diversity of bacterial communities that promote rice production. BMC Microbiol 18(1):51CrossRefPubMedPubMedCentralGoogle Scholar
  104. Yan XY, Yagi K, Akiyama H, Akimoto H (2005) Statistical analysis of the major variables controlling methane emission from rice fields. Glob Chang Biol 11:1131–1141CrossRefGoogle Scholar
  105. Yin C, Fan FL, Song AL, Cui PY, Li TQ, Liang YC (2015) Denitrification potential under different fertilization regimes is closely coupled with changes in the denitrifying community in a black soil. Appl Microbiol Biotechnol 99:5719–5729CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Applied MeteorologyNanjing University of Information Science & TechnologyNanjingChina
  2. 2.Max Planck Institute for Terrestrial MicrobiologyMarburgGermany
  3. 3.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil SciencesChinese Academy of SciencesNanjingChina

Personalised recommendations