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Roles of bulk and rhizosphere denitrifying bacteria in denitrification from paddy soils under straw return condition

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
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Abstract

Purpose

Roles of bulk and rhizosphere denitrifying bacteria in paddy soil denitrification under straw return conditions are rarely discriminated, limiting our understanding on nitrogen biogeochemistry in soils amended with straw. The objective of this study was to explore the microbial mechanisms accounting for the altered rhizosphere and bulk soil denitrification with straw amendment.

Methods

In this study, straw was added into two representative paddy soils (0.5% w/w) from Yixing (YX) and Taizhou (TZ) in Jiangsu city, China, for rice growth over a 37-day period. Denitrification potentials (net N2O emission, total denitrification, and N2O reduction rates) of rhizosphere and bulk soils at the end of rice growth were measured using an acetylene inhibition technique. In addition, denitrifying bacterial community compositions and functional gene abundances were analyzed using Illumina sequencing and quantitative real-time PCR.

Results and discussion

For control treatment without straw addition, total denitrification and N2O reduction rates were significantly higher in the rhizosphere than that in bulk soils; however, net N2O emission potentials were similar between rhizosphere and bulk for TZ (22.6–53.3 vs. 9.44–46.6 mg N kg−1) and YX (946 ± 126 vs. 699 ± 350 mg N kg−1). Under straw return condition, N2O emission potentials from the bulk of both soils were significantly elevated, corresponding to the increase in the relative abundance of some taxa of denitrifying bacteria (unnamed environmental samples and unclassified proteobacteria) and increase in nirK, nirS, and nosZ genes. This indicates a positive response of bulk soil denitrifying bacteria to straw addition. In contrast, straw addition produced inhibitive effects on the growth of denitrifying bacteria with decreased nirK, nirS, and nosZ gene abundances in the rhizosphere. This led to decreased N2O emission potentials at the end of incubation for rhizosphere soils, which were 98.2% and 25.2% lower for TZ and YX compared to those of bulk soils.

Conclusions

These results suggested that the roles of bulk and rhizosphere denitrifying bacteria in paddy soil denitrification shifted with straw addition, which might inspire further studies to target the denitrification hotspots to effectively mitigate greenhouse emissions at the early period of rice growth.

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References

  • Armstrong W (1971) Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiol Plant 25(2):192–197

    Article  Google Scholar 

  • Arth I, Frenzel P, Conrad R (1998) Denitrification coupled to nitrification in the rhizosphere of rice. Soil Biol Biochem 30(4):509–515

    Article  CAS  Google Scholar 

  • Bateman EJ, Baggs EM (2005) Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41(41):379–388

    Article  CAS  Google Scholar 

  • Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35(9):1183–1192

    Article  CAS  Google Scholar 

  • Becker M, Asch F, Maskey SL, Pande KR, Shah SC, Shrestha S (2007) Effects of transition season management on soil N dynamics and system N balances in rice-wheat rotations of Nepal. Field Crop Res 103(2):98–108

    Article  Google Scholar 

  • Bouchard V, Frey SD, Gilbert JM, Reed SE (2007) Effects of macrophyte functional group richness on emergent freshwater wetland functions. Ecology 88:2903–2914

    Article  Google Scholar 

  • Braker G, Tiedje JM (2003) Nitric oxide reductase (norB) genes from pure cultures and environmental samples. Appl Environ Microbiol 69:3476–3483

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Carneiro FSL, Santiago LH, de Antônio OMT, Sartoratto A, De PSM, Suhett DSR et al (2019) Heterotrophic nitrifying/aerobic denitrifying bacteria: ammonium removal under different physical-chemical conditions and molecular characterization. J Environ Manag 248:109294

    Article  Google Scholar 

  • Chen Z, Luo XQ, Hu RG, Wu MN, Wu JS, Wei WX (2010) Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb Ecol 60:850–861

    Article  CAS  Google Scholar 

  • Chen S, Di HJ, Cameron KC, Podolyan A, Shen J, He J (2019) Effect of treated farm dairy effluents, with or without animal urine, on nitrous oxide emissions, ammonia oxidisers and denitrifiers in the soil. J Soils Sediments 19(5):2330–2345

    Article  CAS  Google Scholar 

  • FAO (2013). The state of food and agriculture. Food systems for better nutrition. Rome Italy Fao 79(5): 503. FAO database. https://www.fao.org/publications/sofa. Accessed January 2013

  • Freschet GT, Masse D, Hien E, Sall S, Chotte JL (2008) Long-term changes in organic matter and microbial properties resulting from manuring practices in an arid cultivated soil in Burkina Faso. Agric Ecosys Environ 123:175–184

    Article  Google Scholar 

  • Hallin S, Lindgren PE (1999) PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol 65:1652–1657

    Article  CAS  Google Scholar 

  • Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers allow hundreds of samples to be pyrosequenced in multiplex. Nat Methods 5:235

    Article  CAS  Google Scholar 

  • Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45

    Article  CAS  Google Scholar 

  • Henderson SL, Dandie CE, Patten CL, Zebarth BJ, Burton DL, Trevors JT, Goyer C (2010) Changes in denitrifier abundance, denitrification gene mRNA Levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. Appl Environ Microbiol 76(7):2155–2164

    Article  CAS  Google Scholar 

  • Henry S, Ezékiel B, López-Gutiérrez 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

    Article  CAS  Google Scholar 

  • Hou S, Ai C, Zhou W, Liang G, He P (2018) Structure and assembly cues for rhizospheric nirK- and nirS-type denitrifier communities in long-term fertilized soils. Soil Biol Biochem 119:32–40

    Article  CAS  Google Scholar 

  • Huang Y, Li Y, Yao H (2014) Nitrate enhances N2O emission more than ammonium in a highly acidic soil. J Soils Sediments 14(1):146–154

    Article  CAS  Google Scholar 

  • Ishii S, Ohno H, Tsuboi M, Otsuka S, Senoo K (2011) Identification and isolation of active N2O reducers in rice paddy soil. ISME J 5:1936–1945

    Article  CAS  Google Scholar 

  • Jones CM, Graf DR, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426

    Article  CAS  Google Scholar 

  • Khalil M, Richards K (2011) Denitrification enzyme activity and potential of subsoils under grazed grasslands assayed by membrane inlet mass spectrometer. Soil Biol Biochem 43:1787–1797

    Article  CAS  Google Scholar 

  • Li F, Wang Z, Dai J, Li Q, Wang X, Xue C, Liu H, He G (2015) Fate of nitrogen from green manure, straw, and fertilizer applied to wheat under different summer fallow management strategies in dryland. Biol Fertil Soils 51(7):1–12

    Article  Google Scholar 

  • Li H, Yang XR, Weng BS, Su JQ, Nie SA, Gilbert JA, Zhu YG (2016) The phenological stage of rice growth determines anaerobic ammonium oxidation activity in rhizosphere soil. Soil Biol Biochem 100:59–65

    Article  CAS  Google Scholar 

  • Lin W, Ding JJ, Li YZ, Zhang W, Ahmad R, Xu CY, Mao LL, Qiang XJ, Zheng Q, Li QZ (2019) Partitioning of sources of N2O from soil treated with different types of fertilizers by the acetylene inhibition method and stable isotope analysis. Eur J Soil Sci. https://doi.org/10.1111/ejss.12782

  • Lozupone C, Hamady M, Knight R (2006) UniFrac–An online tool for comparing microbial community diversity in a phylogenetic context. Bmc Bioinformatics 7:371

    Article  Google Scholar 

  • Lu R (1999) Analysis Methods of Soil Agricultural Chemistry. China: Agricultural Science and Technology Publishing House (In Chinese)

  • Maarastawi SA, Frindte K, Bodelier PLE, Knief C (2019) Rice straw serves as additional carbon source for rhizosphere microorganisms and reduces root exudate consumption. Soil Biol Biochem 135:235–238

    Article  CAS  Google Scholar 

  • Malghani S, Yoo GY, Giesemann A, Well R, Kang H (2020) Combined application of organic manure with urea does not alter the dominant biochemical pathway producing N2O from urea treated soil. Biol Fertil Soils 56:331–343

    Article  CAS  Google Scholar 

  • Martin K, Parsons LL, Murray RE, Smith MS (1988) Dynamics of soil denitrifier populations: relationships between enzyme activity, most-probable-number counts, and actual n gas loss. Appl Environ Microbiol 54(11):2711–2716

    Article  CAS  Google Scholar 

  • Menendez S, Lopez-Bellido RJ, Benitez-Vega J, Gonzalez-Murua C, Lopez-Bellido L, Estavillo JM (2008) Long-term effect of tillage, crop rotation and N fertilization to wheat on gaseous emissions under rainfed Mediterranean conditions. Eur J Agron 28:559–569

    Article  CAS  Google Scholar 

  • Moreau D, Bardgett RD, Finlay RD, Jones DL, Philippot L (2019) A plant perspective on nitrogen cycling in the rhizosphere. Funct Ecol 33:540–552

    Article  Google Scholar 

  • Nie SA, Xu HJ, Li S, Li H, Su JQ (2014) Relationships between abundance of microbial functional genes and the status and fluxes of carbon and nitrogen in rice rhizosphere and bulk soils. Pedosphere 24:645–651

    Article  Google Scholar 

  • Nie SA, Li H, Yang XR, Zhang ZJ, Weng BS, Huang FY, Zhu GB, Zhu YG (2015) Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. ISME J 9(9):2059–2067

    Article  CAS  Google Scholar 

  • Oksanen J (2011) Multivariate Analysis of Ecological Communities in R: Vegan Tutorial. American. Community Ecology Package. R package version 1(7)

  • Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. Adv Agron 96:249–305

    Article  CAS  Google Scholar 

  • Savant N, De Datta S (1982) Nitrogen transformations in wetland rice soils. Adv Agron 35:241–302

    Article  CAS  Google Scholar 

  • Schmid MW, Hahl T, Van Moorsel SJ, Wagg C, De Deyn GB, Schmid B (2019) Feedbacks of plant identity and diversity on the diversity and community composition of rhizosphere microbiomes from a long-term biodiversity experiment. Mol Ecol 28(4):863–878

    Article  Google Scholar 

  • Singh SN (2000) Climate Change with Increasing N2O Fluxes. Trace Gas Emissions and Plants. Springer Netherlands.

  • Surey R, Schimpf CM, Sauheitl L, Mueller CW, Mikutta R (2020) Potential denitrification stimulated by water-soluble organic carbon from plant residues during initial decomposition. Soil Biol Biochem 147:107841

    Article  CAS  Google Scholar 

  • Tayefeh M, Sadeghi SM, Noorhosseini SA, Bacenetti J, Damalas CA (2018) Environmental impact of rice production based on nitrogen fertilizer use. Environ Sci Pollut Res Int 25(16):15885–15895

    Article  CAS  Google Scholar 

  • Throbäck IN, Enwall K, Jarvis Å, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417

    Article  Google Scholar 

  • Tiedje JM (1994) Denitrifiers. Methods of Soil Analysis: Part 2—Microbiological and Biochemical Properties, pp. 245–267.

  • Tiirola MA, Rissanen AJ, Sarpakunnas M, Arvola L, Nykanen H (2011) Stable isotope profiles of nitrogen gas indicate denitrification in oxygenstratified humic lakes. Rapid Commun Mass Sp 25:1497–1502

    Article  CAS  Google Scholar 

  • Wan X, Gao Q, Zhao J, Feng J, van Nostrand JD, Yang Y, Zhou J (2020) Biogeographic patterns of microbial association networks in paddy soil within Eastern China. Soil Biol Biochem 142:107696

    Article  CAS  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  Google Scholar 

  • Wang W, Lai DYF, Wang C, Pan T, Zeng C (2015) Effects of rice straw incorporation on active soil organic carbon pools in a subtropical paddy field. Soil Tillage Res 152:8–16

    Article  Google Scholar 

  • Wang YY, Lu SE, Xiang QJ, Yu XM, Zhao K, Zhang XP, Tu SH, Gu YF (2017a) Responses of N2O reductase gene (nosZ)-denitrifier communities to long-term fertilization follow a depth pattern in calcareous purplish paddy soil. J Integr Agric 016(011):2597–2611

    Article  CAS  Google Scholar 

  • Wang N, Luo JL, Juhasz AL, Li HB, Yu JG (2020) Straw decreased N2O emissions from flooded paddy soils via altering denitrifying bacterial community compositions and soil organic carbon fractions. FEMS Microbiol Ecol 96:fiaa046

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Wu H, Wang X, He X, Zhang S, Liang R, Shen J (2017) Effects of root exudates on denitrifier gene abundance, community structure and activity in a micro-polluted constructed wetland. Sci Total Environ 598:697–703

    Article  CAS  Google Scholar 

  • Xing GX, Zhu ZL (2000) An assessment of N loss from agricultural fields to the environment in China. Nutr Cycl Agroecosyst 57:67–73

    Article  Google Scholar 

  • Xu Y, Xu Z, Cai Z, Reverchon F (2013) Review of denitrification in tropical and subtropical soils of terrestrial ecosystems. J Soils Sediments 13(4):699–710

    Article  CAS  Google Scholar 

  • Xu HJ, Yang XR, Li S, Xue XM, Chang S, Li H, Singh BK, Su JQ, Zhu YG (2019) Nitrogen inputs are more important than denitrifier abundances in controlling denitrification-derived N2O emission from both urban and agricultural soils. Sci Total Environ 650:2807–2817

    Article  CAS  Google Scholar 

  • Yoshida M, Ishii S, Otsuka S, Senoo K (2009) Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biol Biochem 41(10):2044–2051

    Article  CAS  Google Scholar 

  • Zhu ZL (2008) Research on soil nitrogen in China. Acta Pedol Sin 45:778–783

    Google Scholar 

  • Zhu G, Wang S, Wang Y, Wang C, Risgaard-Petersen N, Jetten MSM, Yin C (2011) Anaerobic ammonia oxidation in a fertilized paddy soil. ISME J 5:1905–1912

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (41601261) and the Natural Science Foundation of Jiangsu Province (SBK2020022180).

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Correspondence to Jian-Guang Yu or Li-Hong Xue.

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Wang, N., Zhao, YH., Yu, JG. et al. Roles of bulk and rhizosphere denitrifying bacteria in denitrification from paddy soils under straw return condition. J Soils Sediments 21, 2179–2191 (2021). https://doi.org/10.1007/s11368-021-02942-x

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