Abstract
Previous studies have shown that phosphorus addition to P-limited soils increases gaseous N loss. A possible explanation for this phenomenon is element stoichiometry (specifically of C:N:P) modifying linked nutrient cycling, leading to enhanced nitrification and denitrification. In this study, we investigated how P stoichiometry influenced the dynamics of soil N-cycle functional genes. Rice seedlings were planted in P-poor soils and incubated with or without P application. Quantitative PCR was then applied to analyze the abundance of ammonia-oxidizing (amoA) and denitrifying (narG nirK, nirS, nosZ) genes in soil. P addition reduced bacterial amoA abundance but increased denitrifying gene abundance. We suggest this outcome is due to P-induced shifts in soil C:P and N:P ratios that limited ammonia oxidization while enhancing P availability for denitrification. Under P application, the rhizosphere effect raised ammonia-oxidizing bacterial abundance (amoA gene) and reduced nirK, nirS, and nosZ in rhizosphere soils. The change likely occurred through greater C input and O2 release from roots, thus altering C availability and redox conditions for microbes. Our results show that P application enhances gaseous N loss potential in paddy fields mainly through stimulating denitrifier growth. We conclude that nutrient availability and elemental stoichiometry are important in regulating microbial gene responses, thereby influencing key ecosystem processes such as denitrification.
Similar content being viewed by others
References
Armstrong W (1971) Radial oxygen losses from intact rice roots as affected by distance from apex, respiration and waterlogging. Physiol Plant 25:192–197
Bolan NS, Baskaran S, Thiagarajan S (1996) An evaluation of the methods of measurement of dissolved organic carbon in soils, manures, sludges, and stream water. Commun Soil Sci Plant Anal 27:2723–2737
Bouranis DL, Chorianopoulou SN, Kollias C, Maniou P, Protonotarios VE, Siyiannis VF, Hawkesford MJ (2006) Dynamics of aerenchyma distribution in the cortex of sulfate-deprived adventitious roots of maize. Ann Bot 97:695–704
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842
Buchkowski RW, Schmitz OJ, Bradford MA (2015) Microbial stoichiometry overrides biomass as a regulator of soil carbon and nitrogen cycling. Ecology 96:1139–1149
Chapin FS, Mooney H, Chapin M, Matson P (2002) Principles of terrestrial ecosystem ecology. Springer, New York
Cui SY, Xue JF, Chen F, Tang WG, Zhang HL, Tillage RL (2014) Effects on nitrogen leaching and nitrous oxide emission from double-cropped paddy fields. Agron J 106:15–23
Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252
Ding LJ, Wu JS, Xiao HA, Zhou P, Syers KJ (2012) Mobilisation of inorganic phosphorus induced by rice straw in aggregates of a highly weathered upland soil. J Sci Food Agric 92:1073–1079
Duan YH, Shi XJ, Li SL, Sun XF, He XH (2014) Nitrogen use efficiency as affected by phosphorus and potassium in long-term rice and wheat experiments. J Integr Agr 13:588–596
Elser JJ, Dobberfuhl DA, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry: towards a unified view of cellular and ecosystem processes. Bioscience 46:674–684
Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 6:540–550
Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Hogberg P, Linder S (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 5490:291–296
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 U S A 102:14683–14688
Ford H, Roberts A, Jones L (2016) Nitrogen and phosphorus co-limitation and grazing moderate nitrogen impacts on plant growth and nutrient cycling in sand dune grassland. Sci Total Environ 542:203–209
Fu YQ, Yang XJ, Shen H (2014) The physiological mechanism of enhanced oxidizing capacity of rice (Oryza sativa L.) roots induced by phosphorus deficiency. Acta Physiol Plant 36:179–190
Gama-Rodrigues AC, Sales MVS, Silva PSD, Comerford NB, Cropper WP, Gama-Rodrigues EF (2014) An exploratory analysis of phosphorus transformations in tropical soils using structural equation modeling. Biogeochemistry 118:453–469
Godwin GM, Cotner JB (2015) Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J 9:2324–2327
Ge TD, Yuan HZ, Zhu HH, Wu XH, Nie SA, Liu C, Tong CL, Wu JS, Brookes P (2012) Biological carbon assimilation and dynamics in a flooded rice-soil system. Soil Biol Biochem 48:39–46
Ge TD, Li BZ, Zhu ZK, Hu YJ, Yuan HZ, Dorodnikov M, Jones DL, Wu JS, Kuzyakov Y (2017) Rice rhizodeposition and its utilization by microbial groups depends on N fertilization. Biol Fertil Soils 53:37–48
Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999
Hartman WH, Richardson CJ (2013) Differential nutrient limitation of soil microbial biomass and metabolic quotients (qCO2): is there a biological stoichiometry of soil microbes? PLoS One 8:e57127
He MZ, Dijkstra FA (2015) Phosphorus addition enhances loss of nitrogen in a phosphorus-poor soil. Soil Biol Biochem 82:99–106
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 8:5181–5189
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195
Ishii S, Ikeda S, Minamisawa K, Senoo K (2011) Nitrogen cycling in rice paddy environments: past achievements and future challenges. Microbes Environ 26:282–292
Jenkins SN, Murphy DV, Waite IS, Rushton SP, O'Donnell AG (2016) Ancient landscapes and the relationship with microbial nitrification. Sci Rep 6:30733
Keerthisinghe G, DeDatta SK, Mengel K (1985) Importance of exchangeable and nonexchangeable soil NH4 + in nitrogen nutrition of lowland rice. Soil Sci 140:194–201
Kirkby CA, Richardson AE, Wade LJ, Batten GD, Blanchard C, Kirkegaard JA (2013) Carbon-nutrient stoichiometry to increase soil carbon sequestration. Soil Biol Biochem 60:77–86
Kuzyakov Y, Xu XL (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669
Larsen M, Santner J, Oburger E, Wenzel WW, Glud RN (2015) O2 dynamics in the rhizosphere of young rice plants (Oryza sativa L.) as studied by planar optodes. Plant Soil 390:279–292
Lee GH, Kang UG, Park KD, Lee DK, Kim PJ (2008) Long-term fertilization effects on rice productivity and nutrient efficiency in Korean paddy. J Plant Nutr 31:1496–1506
Li J, Li Z, Wang FM, Zou B, Chen Y, Zhao J, Mo QF, Li Y, Li X, Xia H (2015) Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fertil Soils 51:207–215
Li YL, Zhang YL, Hu J, Shen QR (2007) Contribution of nitrification happened in rhizospheric soil growing with different rice cultivars to N nutrition. Soil Biol Biochem 43:417–425
Lin JS, Shi XZ, Lu XX, Yu DS, Wang HJ, Zhao YC, Sun WX (2009) Storage and spatial variation of phosphorus in paddy soils of china. Pedosphere 19:790–798
Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704
Meng FQ, Olesen JE, Sun XP, Wu WL (2014) Inorganic nitrogen leaching from organic and conventional rice production on a newly claimed calciustoll in Central Asia. PLoS One 9:e98138
Mori T, Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A (2010) Effects of phosphorus addition on N2O and NO emissions from soils of an Acacia mangium plantation. Soil Sci Plant Nutr 56:782–788
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci U S A 101:11001–11006
Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fin scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712
Sistla SA, Schimel JP (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196:68–78
Sistla SA, Appling AP, Lewandowska AM, Taylor BN, Wolf AA (2015) Stoichiometric flexibility in response to fertilization along gradients of environmental and organismal nutrient richness. Oikos 124:949–959
Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 11:3612–3622
Spohn M (2016) Element cycling as driven by stoichiometric homeostasis of soil microorganisms. Basic Appl Ecol 17:471–478
Tang YQ, Zhang XY, Li DD, Wang HM, Chen FS, Fu XL, Fang XM, Sun XM, Yu GR (2016) Impacts of nitrogen and phosphorus additions on the abundance and community structure of ammonia oxidizers and denitrifying bacteria in Chinese fir plantations. Soil Biol Biochem 103:284–293
Thion CE, Poirel JD, Cornulier T, De Vries FT, Bardgett RD, Prosser JI (2016) Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS Microbiol Ecol 92:fiw091
Wang FM, Li J, Wang XL, Zhang W, Zou B, Neher DA, Li ZA (2014) Nitrogen and phosphorus addition impact soil N2O emission in a secondary tropical forest of South China. Sci Rep 4:5615
Wei W, Isobe K, Nishizawa T, Zhu L, Shiratori Y, Ohte N, Koba K, Otsuka S, Senoo K (2015) Higher diversity and abundance of denitrifying microorganisms in environments than considered previously. ISME J 9:1954–1965
Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biol Biochem 22:1167–1169
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
Yuan HZ, Zhu ZK, Liu SL, Ge TD, Jing HZ, Li BZ, Liu Q, Lynn TM, Wu JS, Kuzyakov Y (2016) Microbial utilization of rice root exudates: C-13 labeling and PLFA composition. Biol Fertil Soils 52:615–627
Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Penuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monogr 85:133–155s
Zhu FF, Lu XK, Liu L, Mo JM (2015) Phosphate addition enhanced soil inorganic nutrients to a large extent in three tropical forests. Sci Rep 5:7923
Acknowledgements
This study was financially supported by the National Natural Science Foundation of China (41522107; 41430860), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020401), National key research and development program (2016YFE0101100), the Australia-China Joint Research Centre – Healthy Soils for Sustainable Food Production and Environmental Quality (ACSRF48165), and Youth Innovation Team Project of ISA, CAS (2017QNCXTD_GTD). We thank the Public Service Technology Center, Institute of Subtropical Agriculture, Chinese Academy of Sciences for technical assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Wei, X., Hu, Y., Peng, P. et al. Effect of P stoichiometry on the abundance of nitrogen-cycle genes in phosphorus-limited paddy soil. Biol Fertil Soils 53, 767–776 (2017). https://doi.org/10.1007/s00374-017-1221-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-017-1221-1