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Comparison of the abundance and community structure of ammonia oxidizing prokaryotes in rice rhizosphere under three different irrigation cultivation modes

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Abstract

The abundance, diversity and community structure of ammonia oxidizing archaea (AOA) and bacteria (AOB) in rice rhizosphere soils under three different irrigation cultivated modes, named continuous irrigation mode (C), intermittent irrigation mode (I) and semi-arid mode (M), respectively, were investigated using amoA gene as a molecular biomarker. Clone libraries and quantitative polymerase chain reaction results indicated the highest number of archaeal amoA gene copy was detected in M cultivation mode, then in I and C, whereas, their order of amoA gene copy numbers were I > M > C for AOB, and those were obvious higher than in the bulk soil. The ratios of AOA/AOB were greater than 1 for all samples, suggested the predominance of AOA throughout the period of rice growth in the three different irrigation cultivation modes. Diversity index (SChao1 and Shannon H) have an obvious variation in three different irrigation cultivation modes. For AOA, SChao1 was highest in M and lowest in I mode, whereas, Shannon H was highest in M cultivation mode and lowest in C mode. For AOB, mode M exhibited the highest diversity index (SChao1 and Shannon H), while C showed the lowest highest diversity, suggested long-term water input (continuous mode) may decrease diversity of ammonia oxidizers, whereas mode M may be more appropriate for them. In addition, AOA sequences fall within Nitrososphaera, Nitrosopumilus and Nitrosotalea cluster with proportion of 89.38, 8.85 and 1.77 %, respectively. AOB gene sequences belonged to the Nitrosomonas and Nitrosospira genera with proportion of 90.97 and 9.03 %, respectively. In addition, the abundances, diversity and community structure had an obvious temporal variation in three developmental stages of rice, further suggested rice growth obviously affected the ammonia oxidizing prokaryotes in their rhizosphere soil.

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References

  • Ai C, Liang G, Sun J, Wang X, He P, Zhou W (2013) Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvoaquic soil. Soil Biol Biochem 57:30–42

    Article  CAS  Google Scholar 

  • Allison S, Prosser J (1993) Ammonia oxidation at low pH by attached populations of nitrifying bacteria. Soil Biol Biochem 25:935–941

    Article  CAS  Google Scholar 

  • Alvey S, Yan CH, Buerkert A, Crowley DE (2003) Cereal/legume rotation effects on rhizosphere bacterial community structure in West African soils. Biol Fertil Soils 37:73–82

    Google Scholar 

  • Avrahami S, Conrad R, Braker G (2002) Effect of soil ammonium concentration on N2O release and on the community structure of ammonia oxidizers and denitrifiers. Appl Environ Microbiol 68:5685–5692

    Article  CAS  Google Scholar 

  • Belder P, Bouman BAM, Cabangon R, Lu GA, Quilang EJP, Li YH, Spiertz JHJ, Tuong TP (2004) Effect of water-saving irrigation on rice yield and water use in typical lowland conditions in Asia. Agric Water Manag 65:193–210

    Article  Google Scholar 

  • Bissett A, Richardson AE, Baker G, Thrall PH (2011) Long-term land use effects on soil microbial community structure and function. Appl Soil Ecol 51:66–78

    Article  Google Scholar 

  • Bissett A, Abell GCJ, Brown M, Thrall PH, Bodrossy L, Smit MC, Baker GH, Richardsson AE (2014) Land-use and management practices affect soil ammonia oxidiser community structure, activity and connectedness. Soil Biol Biochem 78:138–148

    Article  CAS  Google Scholar 

  • Briones AM, Okabe S, Umemiya Y, Ramsing NB, 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  CAS  Google Scholar 

  • Bruns MA, Stephen JR, Kowalchuk GA, Prosser JI, Paul EA (1999) Comparative diversity of ammonia oxidizer 16S rRNA gene sequences in native, tilled, and successional soils. Appl Environ Microbiol 65:2994–3000

    CAS  Google Scholar 

  • Bürgmann H, Meier S, Bunge M, Widmer F, Zeyer J (2005) Effects of model root exudates on structure and activity of a soil diazotroph community. Environ Microbiol 7:1711–1724

    Article  Google Scholar 

  • Burton SA, Prosser JI (2001) Autotrophic ammonia oxidation at low pH through urea hydrolysis. Appl Environ Microbiol 67:2952–2957

    Article  CAS  Google Scholar 

  • Cao HL, Li M, Hong YG, Gu JD (2011a) Diversity and abundance of ammonia-oxidizing archaea and bacteria in polluted mangrove sediment. Syst Appl Microbiol 34:513–523

    Article  CAS  Google Scholar 

  • Cao HL, Hong YG, Li M, Gu JD (2011b) Diversity and abundance of ammonia-oxidizing prokaryotes in sediments from the coastal Pearl River estuary to the South China Sea. Antonie Van Leeuwenhoek 100:545–556

    Article  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  CAS  Google Scholar 

  • Chu H, Morimoto S, Fujii T, Yagi K, Nishimura S (2009) Soil ammonia-oxidizing bacterial communities in paddy rice fields as affected by upland conversion history. Soil Sci Soc Am J 73:2026–2031

    Article  CAS  Google Scholar 

  • Dang H, Li J, Zhang X, Li T, Tian F, Jin W (2009) Diversity and spatial distribution of amoA-encoding archaea in the deep-sea sediments of the tropical West Pacific Continental Margin. J Appl Microbiol 106:1482–1493

    Article  CAS  Google Scholar 

  • de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818

    Article  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394

    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  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 Nat Acad Sci USA 102:14683–14688

    Article  CAS  Google Scholar 

  • Glaser K, Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S, Sessitsch A (2010) Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol Ecol 74:575–591

    Article  CAS  Google Scholar 

  • Gong P, Zhang LL, Wu ZJ, Chen ZH, Chen LJ (2013) Responses of ammonia-oxidizing bacteria and archaea in two agricultural soils to nitrification inhibitors DCD and DMPP: a Pot experiment. Pedosphere 23(6):729–739

    Article  CAS  Google Scholar 

  • Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574

    Article  CAS  Google Scholar 

  • He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di H (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  CAS  Google Scholar 

  • Hinsinger P, Plassard C, Jaillard B (2006) Rhizosphere: a new frontier for soil biogeochemistry. J Geochem Explor 88:210–213

    Article  CAS  Google Scholar 

  • Hussain Q, Liu YZ, Jin ZJ, Zhang AF, Pan GX, Li LQ, Crowley D, Zhang XH, Song XY, Cui LQ (2011) Temporal dynamics of ammonia oxidizer (amoA) and denitrifier (nirK) communities in the rhizosphere of a rice ecosystem from Tai Lake region, China. Appl Soil Ecol 48:210–218

    Article  Google Scholar 

  • Hussain Q, Pan GX, Liu YZ, Zhang A, Li LQ, Zhang XH, Jin ZJ (2012) Microbial community dynamics and function associated with rhizosphere over periods of rice growth. Plant Soil Environ 58(2):55–61

    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  CAS  Google Scholar 

  • Jiang XJ, Hou XY, Zhou X, Xin XP, Wright A, Jia ZJ (2015) pH regulates key players of nitrification in paddy soils. Soil Biol Biochem 81:9–16

    Article  CAS  Google Scholar 

  • Kemmitt SJ, Wright D, Goulding KW, Jones DL (2006) pH regulation of carbon and nitrogen dynamics in two agricultural soils. Soil Biol Biochem 38:898–911

    Article  CAS  Google Scholar 

  • Kennedy AC, Smith KL (1995) Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170:75–86

    Article  CAS  Google Scholar 

  • Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Liesack W, Schnell S, Revsbech NP (2000) Microbiology of flooded rice paddies. FEMS Microbiol Rev 24:625–645

    Article  CAS  Google Scholar 

  • Liu ZH, Huang SB, Sun GP, Xu ZC, Xu MY (2011) Diversity and abundance of ammonia-oxidizing archaea in the Dongjiang River, China. Microbiol Res 166:337–345

    Article  CAS  Google Scholar 

  • Liu B, Li YM, Zhang JP, Zhou XH, Wu CD (2014) Abundance and diversity of ammonia-oxidizing microorganisms in the sediments of Jinshan Lake. Curr Microbiol 69:751–757

    Article  CAS  Google Scholar 

  • Liu Y, Zhou HM, Wang JQ, Liu XY, Cheng K, Li LQ, Zheng JW, Zhang XH, Zheng JF, Pan GX (2015) Short-term response of nitrifier communities and potential nitrification activity to elevated CO2 and temperature interaction in a Chinese paddy field. Appl Soil Ecol 96:88–98

    Article  Google Scholar 

  • Lu RK (1999) Soil agricultural chemical analysis method. China Agricultural Technology Press, Beijing

    Google Scholar 

  • Martens-Habbena W, Berube PM, Urakawa H, de la Torre JR, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979

    Article  CAS  Google Scholar 

  • Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol 170:165–175

    Article  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  CAS  Google Scholar 

  • Norman JS, Barrett JE (2014) Substrate and nutrient limitation of ammonia-oxidizing bacteria and archaea in temperate forest soil. Soil Biol Biochem 69:141–146

    Article  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  CAS  Google Scholar 

  • Phillips CJ, Harris D, Dollhopf SL, Gross KL, Prosser JI, Paul EA (2000) Effects of agronomic treatments on structure and function of ammonia-oxidizing communities. Appl Environ Microbiol 66:5410–5418

    Article  CAS  Google Scholar 

  • Prosser JI, Embley TM (2002) Cultivation-based and molecular approaches to characterisation of terrestrial and aquatic nitrifiers. Antonie Van Leeuwenhoek 81:165–179

    Article  CAS  Google Scholar 

  • Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10:2931–2941

    Article  CAS  Google Scholar 

  • Ramasamy S, ten Berge HFM, Purushothaman S (1997) Yield formation in rice in response to drainage and nitrogen application. Field Crops Res 51:65–82

    Article  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 

  • Rice CW, Smith MS (1982) Denitrification in no-till and plowed soils 1. Soil Sci Soc Am J 46:1168–1173

    Article  CAS  Google Scholar 

  • Roger PA (1995) Biological N2-fixation and its management in wetland rice cultivation. Fertil Res 42:261–276

    Article  CAS  Google Scholar 

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

    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  CAS  Google Scholar 

  • Schramm A, de Beer D, Wagner M, Amann R (1998) Identification and activities in situ of Nitrosospira and Nitrospira spp. as dominant populations in a nitrifying fluidized bed reactor. Appl Environ Microbiol 64:3480–3485

    CAS  Google Scholar 

  • Schramm A, de Beer D, van den Heuvel J, Ottengraf S, Amann R (1999) Microscale distribution of populations and activities of Nitrosospira and Nitrospira spp. along a macroscale gradient in a nitrifying bioreactor: quantification by in situ hybridization and the use of microsensors. Appl Environ Microbiol 65:3690–3696

    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  CAS  Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Article  CAS  Google Scholar 

  • Song YN, Lin ZM (2014) Abundance and community composition of ammonia-oxidizers in paddy soil at different nitrogen fertilizer rates. J Integr Agric 13(4):870–880

    Article  CAS  Google Scholar 

  • Strauss SL, Reardon CL, Mazzola M (2014) The response of ammonia-oxidizer activity and community structure to fertilizer amendment of orchard soils. Soil Biol Biochem 68:410–418

    Article  CAS  Google Scholar 

  • Sun YJ, Ma J, Sun YY, Xu H, Yang ZY, Liu SJ, Jia XW, Zheng HZ (2012) The effects of different water and nitrogen managements on yield and nitrogen use efficiency in hybrid rice of China. Field Crops Res 127:85–98

    Article  Google Scholar 

  • Suzuki I, Dular U, Kwok S (1974) Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J Bacteriol 120:556–558

    CAS  Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Nat Acad Sci USA 108:8420–8425

    Article  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  CAS  Google Scholar 

  • Vanegas J, Landazabal G, Melgarejo LM, Beltran M, Uribe-Vélez D (2013) Structural and functional characterization of the microbial communities associated with the upland and irrigated rice rhizospheres in a neotropical Colombian savannah. Eur J Soil Biol 55:1–8

    Article  CAS  Google Scholar 

  • Wang XY, Wang C, Bao LL, Xie SG (2014) Abundance and community structure of ammonia-oxidizing microorganisms in reservoir sediment and adjacent soils. Appl Microbiol Biotechnol 98:1883–1892

    Article  CAS  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

    Article  Google Scholar 

  • Wheatley RE, Caul S, Crabb D, Daniell TJ, Griffiths BS, Ritz K (2003) Microbial population dynamics related to temporal variations in nitrification in three arable fields. Eur J Soil Sci 54:707–714

    Article  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    Article  CAS  Google Scholar 

  • Wu Y, Lu L, Wang B, Lin J, Cai Z, Yan X, Jia Z (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75:1405–1413

    Article  Google Scholar 

  • Yang JC, Liu K, Wang ZQ, Du Y, Zhang J (2007) Water-saving and high-yielding irrigation for lowland rice by controlling limiting values of soil water potential. J Integr Plant Biol 49:1445–1454

    Article  Google Scholar 

  • Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625

    Article  CAS  Google Scholar 

  • Ying JY, Zhang LM, He JZ (2010) Putative ammonia-oxidizing bacteria and archaea in an acid red soil with different land utilization patterns. Environ Microbiol Rep 2:302–312

    Article  Google Scholar 

  • Zhang K, Lv XG, Tian K (2008) Response of soil organic matters to water contents in Napahai Plateau wetlands. J Yunnan 30:424–427

    CAS  Google Scholar 

  • Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045

    Article  CAS  Google Scholar 

  • Zhou ZF, Shi XJ, Zheng Y, Qin ZX, Xie DT, Li ZL, Guo T (2014) Abundance and community structure of ammonia-oxidizing bacteria and archaea in purple soil under long-term fertilization. Eur J Soil Biol 60:24–33

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (51109097), Jiangsu Province basic research program (Natural Science Foundation funded project) (BK2011520), China Postdoctoral Science Foundation funded project (2012T50464) and Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment. The authors would like to thank the financial support.

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  1. Department of Environment Engineering, School of the Environment and Safety Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang, 212013, Jiangsu, People’s Republic of China

    Jinping Zhang, Xiaohong Zhou, Lei Chen, Zhigang Chen, Jinyu Chu & Yimin Li

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  1. Jinping Zhang
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  2. Xiaohong Zhou
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  3. Lei Chen
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Correspondence to Xiaohong Zhou.

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Zhang, J., Zhou, X., Chen, L. et al. Comparison of the abundance and community structure of ammonia oxidizing prokaryotes in rice rhizosphere under three different irrigation cultivation modes. World J Microbiol Biotechnol 32, 85 (2016). https://doi.org/10.1007/s11274-016-2042-3

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