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

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Abstract

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.

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References

  • 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 70:186–195

    CAS  Google Scholar 

  • 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 50:754–765

    PubMed  Google Scholar 

  • Angel R, Conrad R (2013) Elucidating the microbial resuscitation cascade in biological soil crusts following a simulated rain event. Environ Microbiol 15:2799–2815

    CAS  PubMed  Google Scholar 

  • Angel R, Matthies D, Conrad R (2011) Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS One 6:e20453

    CAS  PubMed  PubMed Central  Google Scholar 

  • Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862

    CAS  PubMed  Google Scholar 

  • 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 53:407–417

    CAS  Google Scholar 

  • 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. https://doi.org/10.1055/s-2001-15205

    Article  CAS  Google Scholar 

  • 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 77:3846–3852

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 5:908–917

    CAS  PubMed  Google Scholar 

  • Beauchamp EG (1997) Nitrous oxide emission from agricultural soils. Can J Soil Sci 77:113–123

    CAS  Google Scholar 

  • Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219. https://doi.org/10.3389/fmicb.2014.00219

    Article  PubMed  PubMed Central  Google Scholar 

  • Bodelier PLE, Roslev P, Henckel T, Frenzel P (2000) Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403:421–424

    CAS  PubMed  Google Scholar 

  • Boer WD, Duyt SH, Laanbrock HJ (1988) Autotrophic nitrification in a fertilized acid health soil. Soil Biol Biochem 20:845–850

    Google Scholar 

  • Bossio DA, Scow KM (1995) Impact of carbon and flooding on the metabolic diversity of microbial communities in soils. Appl Environ Microbiol 61:4043–4050

    CAS  PubMed  PubMed Central  Google Scholar 

  • Braker G, Conrad R (2011) Diversity, structure, and size of N2O-producing microbial communities in soils-what matters for their functioning? Adv Appl Microbiol 75:33–70

    CAS  PubMed  Google Scholar 

  • Breidenbach B, Conrad R (2015) Seasonal dynamics of bacterial and archaeal methanogenic communities in flooded rice fields and effect of drainage. Front Microbiol 5:752

    PubMed  PubMed Central  Google Scholar 

  • 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 18:2868–2885

    CAS  PubMed  Google Scholar 

  • 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 47:657–660

    CAS  PubMed  Google Scholar 

  • 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 196:7–14

    CAS  Google Scholar 

  • 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 56:7–39

    Google Scholar 

  • 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. https://doi.org/10.1007/s00374-011-0542-8

    Article  CAS  Google Scholar 

  • 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 63:446–459

    PubMed  Google Scholar 

  • Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202

    CAS  Google Scholar 

  • Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Adv Agron 96:1–63

    CAS  Google Scholar 

  • Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292

    CAS  PubMed  Google Scholar 

  • 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 11:1844–1853

    CAS  PubMed  Google Scholar 

  • 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 55:1932–1942

    CAS  Google Scholar 

  • 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 16:1682–1694

    CAS  PubMed  Google Scholar 

  • Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of Methanotrophs in Lake sediments. Appl Environ Microbiol 65:5066–5074

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 93:131–141

    CAS  Google Scholar 

  • 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 45:1095–1101

    CAS  Google Scholar 

  • 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 67:190–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71:8335–8343

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1126/science.1127062

    Article  CAS  PubMed  Google Scholar 

  • 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 6:1054–1063

    PubMed  PubMed Central  Google Scholar 

  • 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 15:2588–2602

    Google Scholar 

  • 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 53:37–48

    CAS  Google Scholar 

  • 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 64:960–969

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:660–674

    PubMed  PubMed Central  Google Scholar 

  • 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 59:327–335

    CAS  PubMed  Google Scholar 

  • 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 72:5181–5189

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 78:116–128

    CAS  PubMed  Google Scholar 

  • Hutsch BW, Webster CP, Powlson DS (1994) Methane oxidation in soil as affected by land-use, soil-Ph and N-fertilization. Soil Biol Biochem 26:1613–1622

    Google Scholar 

  • 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 pp

    Google Scholar 

  • 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 47:599–604

    Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 63:4552–4557

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 371:473–486

    CAS  Google Scholar 

  • 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 24:662–673

    Google Scholar 

  • 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 89:238–247

    CAS  Google Scholar 

  • Jia Z, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671. https://doi.org/10.1111/j.1462-2920.2009.01891.x

    Article  CAS  PubMed  Google Scholar 

  • 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 72:5957–5962

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:448–458

    CAS  Google Scholar 

  • 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: 1–14

    Google Scholar 

  • 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 51:323–331

    PubMed  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–147

    Google Scholar 

  • 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 40:2407–2415

    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. https://doi.org/10.1038/nature04983

    Article  CAS  PubMed  Google Scholar 

  • 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 91:293–305

    CAS  Google Scholar 

  • 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 18:194–209

    Google Scholar 

  • Lu Y, Rosencrantz D, Liesack W, Conrad R (2006) Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ Microbiol 8:1351–1360

    CAS  PubMed  Google Scholar 

  • 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 66:754–762

    PubMed  PubMed Central  Google Scholar 

  • Lueders T, Friedrich M (2000) Archaeal population dynamics during sequential reduction processes in rice field soil. Appl Environ Microbiol 66:2732–2742

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 78:445–454

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 59:25–36

    PubMed  Google Scholar 

  • Marschner P, Kandeler E, Marschner B (2003) Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461

    CAS  Google Scholar 

  • Mendiburu F (2015) Agricolae: statistical procedures for agricultural research ver.1.2-1. http://cran.fyxm.net/web/packages/agricolae/. Accessed May 2016

  • 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 40:2553–2562

    CAS  Google Scholar 

  • 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 2:465–473

    CAS  Google Scholar 

  • Mosier AR, Kroese C, Nevsion C (1998) Closing the global N2O budget: nitrogen oxide emissions through the agricultural nitrogen cycle. Nutr Cycl Agroecosyst 52:225–248

    CAS  Google Scholar 

  • 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 10:3093–3105

    CAS  PubMed  Google Scholar 

  • 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 6:861–867

    CAS  PubMed  Google Scholar 

  • 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 7:382–395

    CAS  PubMed  Google Scholar 

  • 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. http://cran.rproject.org/web/packages/vegan/index.html. Accessed May 2016

  • Oneill JG, Wilkinson JF (1977) Oxidation of ammonia by methane oxidizing bacteria and the effects of ammonia on methane oxidation. J Gen Microbiol 100:407–412

    CAS  Google Scholar 

  • 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 6:1058–1077

    CAS  PubMed  Google Scholar 

  • 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 35:7188–7196

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1007/s11104-014-2201-y

    Article  CAS  Google Scholar 

  • 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 54:885–895

    Google Scholar 

  • 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 1:283–290

    CAS  PubMed  Google Scholar 

  • 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 4:1340–1351

    PubMed  Google Scholar 

  • Schimel J (2000) Global change: rice, microbes and methane. Nature 403:375–377

    CAS  PubMed  Google Scholar 

  • 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 75:7537–7541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:485–489

    Google Scholar 

  • Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:296. https://doi.org/10.3389/fmicb.2012.00296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1038/ismej.2010.89

    Article  CAS  PubMed  Google Scholar 

  • Soil Survey Staff (1975) Soil taxonomy. U.S. Department of Agriculture Handbook, No. 436. USDA, Washington, DC

  • 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 14:105–111

    Google Scholar 

  • 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 612:739–749

    CAS  PubMed  Google Scholar 

  • Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart-how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484

    Google Scholar 

  • 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 56:831–838

    CAS  Google Scholar 

  • 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 7:1–13

    Google Scholar 

  • 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 53:601–611

    CAS  Google Scholar 

  • Watanabe T, Kimura M, Asakawa S (2006) Community structure of methanogenic archaea in paddy field soil under double cropping (rice-wheat). Soil Biol Biochem 38:1264–1274

    CAS  Google Scholar 

  • 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 56:705–715

    CAS  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1016/j.apsoil.2010.04.003

    Article  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. springer, Dordrecht, the Netherlands

    Google Scholar 

  • 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 48:261–271

    CAS  PubMed  Google Scholar 

  • Wu LQ, Ma K, Lu YH (2009) Prevalence of betaproteobacterial sequences in nifH gene pools associated with roots of modern rice cultivars. Microb Ecol 57:58–68

    CAS  PubMed  Google Scholar 

  • 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 47:397–405

    Google Scholar 

  • 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):51

    PubMed  PubMed Central  Google Scholar 

  • Yan XY, Yagi K, Akiyama H, Akimoto H (2005) Statistical analysis of the major variables controlling methane emission from rice fields. Glob Chang Biol 11:1131–1141

    Google Scholar 

  • 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 99:5719–5729

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Melanie Klose and Peter Claus for technical support.

Funding

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).

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Ji, Y., Conrad, R. & Xu, H. Responses of archaeal, bacterial, and functional microbial communities to growth season and nitrogen fertilization in rice fields. Biol Fertil Soils 56, 81–95 (2020). https://doi.org/10.1007/s00374-019-01404-4

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