Advertisement

Flooding and prolonged drought have differential legacy impacts on soil nitrogen cycling, microbial communities and plant productivity

  • Linh T. T. Nguyen
  • Yui Osanai
  • Ian C. Anderson
  • Michael P. Bange
  • David T. Tissue
  • Brajesh K. Singh
Regular Article

Abstract

Background and aims

Extreme climate events, including flooding and prolonged drought, may establish long-lasting (legacy) effects on soil abiotic and biotic properties, potentially influencing soil N-cycling, microbial communities, and plant productivity. Nitrogen (N) fertilizer often stimulates plant growth, but it remains unknown whether N addition can alleviate the impact of legacy drought or waterlogging events on crops. Our aim was to assess the interactive effects of legacy extreme climate events and N-addition on these processes.

Methods

Using cotton as a model system, soils previously exposed to waterlogging and prolonged drought were used to examine potential legacy impacts of extreme climate on soil N process rates, abundance and structure of associated microbial communities, and cotton growth and productivity under different levels of N fertilizer application (0, 100, 200 and 300 kg N/ha).

Results

The deleterious legacy effects of prolonged drought on plant productivity were due to negative impacts on microbial abundance and community structure, and soil nutrient availability, thereby negatively influencing the rate of nitrification, and consequently plant available N. The legacy impacts of prolonged drought persisted throughout the experiment despite fertiliser applications of up to 300 kg of N/ha. The only observed legacy impacts of waterlogging were low NO3 levels in soils without N-addition and shifts in the abundance and structure of the N2O-reducing community.

Conclusions

There were strong legacy impacts of prolonged drought, but minor legacy impacts of waterlogging, on soils and crop yields which could not be fully counteracted by the high rates of N fertilizer application. This study provides critical knowledge contributing to the development of adaptation and soil N management strategies to minimize the loss of farm productivity, within the context of increased frequencies and intensities of extreme weather events.

Keywords

Legacy effects Extreme weather events Cotton (Gossypium hirsutum L.) N fertilizer supply N cycling 

Notes

Acknowledgments

The authors gratefully acknowledge Dr. Michael Braunack at CSIRO Agriculture for his help in soil collection from Narrabri, NSW. We also thank Renee Smith at WSU for her technical support for the glasshouse experiment. Thanks to Dr. Hangwei Hu at the University of Melbourne, for providing supportive materials for TRFLP analysis and to Dr. Jasmine Grinyer (WSU) for extensive editing. This work was financially supported by Hawkesbury Institute for the Environment and Western Sydney University as a part funding to Cotton Research and Development Corporation project (UWS1301). BKS work is also supported by Australian Research Council (DP170104634).

Supplementary material

11104_2018_3774_MOESM1_ESM.docx (1.1 mb)
ESM 1 (DOCX 1099 kb)

References

  1. Abid M, Tian Z, Ata-Ul-Karim ST, Cui Y, Liu Y, Zahoor R, Jiang D, Dai T (2016) Nitrogen nutrition improves the potential of wheat (Triticum aestivum L.) to alleviate the effects of drought stress during vegetative growth periods. Front Plant Sci 7:981PubMedPubMedCentralCrossRefGoogle Scholar
  2. Aggangan R, O’Connel A, Mcgrath J, Dell B (1998) Fertilizer and previous land use effects on C and N mineralization in soils from Eucalyptus globulus plantations. Soil Biol Biochem 30:1791–1798CrossRefGoogle Scholar
  3. Banerjee S, Helgason B, Wang L, Winsley T, Ferrari BC, Siciliano SD (2016) Legacy effects of soil moisture on microbial community structure and N2O emissions. Soil Biol Biochem 95:40–50CrossRefGoogle Scholar
  4. Bange M, Milroy S, Thongbai P (2004) Growth and yield of cotton in response to waterlogging. Field Crop Res 88:129–142CrossRefGoogle Scholar
  5. Bange MP, Baker J, Bauer P, Broughton KJ, Constable G, Luo Q, Osanai Y, Payton P, Tissue DT, Reddy K, Singh BK (2016) Climate change and cotton production in modern farming system. CAB International, Oxfordshire, 61 pagesCrossRefGoogle Scholar
  6. Bastida F, Moreno JL, Hernández T, García C (2006) Microbiological activity in a soil 15 years after its devegetation. Soil Biol Biochem 38:2503–2507CrossRefGoogle Scholar
  7. Bi J, Zhang N, Liang Y, Yang H, Ma K (2011) Interactive effects of water and nitrogen addition on soil microbial communities in a semiarid steppe. J Plant Ecol 5:320–329CrossRefGoogle Scholar
  8. Boquet DJ, Tubaña BS, Mascagni HJ, Holman M, Hague S (2009) Cotton yield responses to fertilizer nitrogen rates in a cotton-corn rotation. Agron J 101:400–407CrossRefGoogle Scholar
  9. Braunack M (2013) Cotton farming systems in Australia: factors contributing to changed yield and fibre quality. Crop Pasture Sci 64:834–844Google Scholar
  10. Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bruulsema T, Fixen P, Snyder C (2004) Fertilizer nutrient recovery in sustainable cropping systems. Better Crops 88:15–17Google Scholar
  12. Carey CJ, Dove NC, Beman JM, Hart SC, Aronson EL (2016) Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea. Soil Biol Biochem 99:158–166CrossRefGoogle Scholar
  13. Carney KM, Matson PA, Bohannan BJ (2004) Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land-use types. Ecol Lett 7:684–694CrossRefGoogle Scholar
  14. Cavagnaro TR (2016) Soil moisture legacy effects: impacts on soil nutrients, plants and mycorrhizal responsiveness. Soil Biol Biochem 95:173–179CrossRefGoogle Scholar
  15. Chen XP, Cui ZL, Vitousek PM, Cassman KG, Matson PA, Bai JS, Meng QF, Hou P, Yue SC, Römheld V (2011) Integrated soil–crop system management for food security. Proc Natl Acad Sci U S A 108:6399–6404PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chen Z, Hou H, Zheng Y, Qin H, Zhu Y, Wu J, Wei W (2012) Influence of fertilisation regimes on a nosZ-containing denitrifying community in a rice paddy soil. J Sci Food Agric 92:1064–1072PubMedCrossRefGoogle Scholar
  17. Chen Y, Xu Z, Hu H, Hu Y, Hao Z, Jiang Y, Chen B (2013) Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Appl Soil Ecol 68:36–45CrossRefGoogle Scholar
  18. Culman SW, Bukowski R, Gauch HG, Cadillo-quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinf 10:1CrossRefGoogle Scholar
  19. de Vries FT, Liiri ME, Børnlund L, Setälä HM, Christensen S, Bardgett RD (2012) Legacy effects of drought on plant growth and the soil food web. Oecologia 170(3):821–833PubMedCrossRefGoogle Scholar
  20. Delin S, Lindén B (2002) Relations between net nitrogen mineralization and soil characteristics within an arable field. Acta Agric Scand Sect B Soil Plant Sci 52:78–85Google Scholar
  21. Di H, Cameron K, Shen JP, Winefield C, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624CrossRefGoogle Scholar
  22. 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 72:386–394PubMedCrossRefGoogle Scholar
  23. Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71:8335–8343PubMedPubMedCentralCrossRefGoogle Scholar
  24. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:153–188CrossRefGoogle Scholar
  25. Fiala K, Tůma I, Holub P (2011) Effect of nitrogen addition and drought on above-ground biomass of expanding tall grasses Calamagrostis epigejos and Arrhenatherum elatiu. Biologia 66:275–281CrossRefGoogle Scholar
  26. Fierer N, Schimel JP (2003) A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci Soc Am J 67:798–805CrossRefGoogle Scholar
  27. Geisseler D, Scow KM (2014) Long-term effects of mineral fertilizers on soil microorganisms–a review. Soil Biol Biochem 75:54–63CrossRefGoogle Scholar
  28. Geng S, Yan D, Zhang T, Weng B, Zhang Z, Gang W (2014) Effects of extreme drought on agriculture soil and sustainability of different drought soil. Hydrol Earth Syst Sci 11:1–29CrossRefGoogle Scholar
  29. 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 74:575–591PubMedCrossRefGoogle Scholar
  30. Göransson H, Godbold DL, Jones DL, Rousk J (2013) Bacterial growth and respiration responses upon rewetting dry forest soils: impact of drought-legacy. Soil Biol Biochem 57:477–486CrossRefGoogle Scholar
  31. Grime J, Curtis A (1976) The interaction of drought and mineral nutrient stress in calcareous grassland. J Ecol 64:975–988CrossRefGoogle Scholar
  32. Haddad NM, Tilman D, Knops JM (2002) Long-term oscillations in grassland productivity induced by drought. Ecol Lett 5:110–120CrossRefGoogle Scholar
  33. Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605PubMedCrossRefGoogle Scholar
  34. Hamonts K, Clough TJ, Stewart A, Clinton PW, Richardson AE, Wakelin SA, O’Callaghan M, Condron LM (2013) Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat. FEMS Microbiol Ecol 83:568–584PubMedCrossRefGoogle Scholar
  35. Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In: Weaver RW, Angle JS, Bottomley PD (eds) Methods of soil analysis: part 2—microbiological and biochemical properties. Soil Science Society of America, Madison, pp 985–1018Google Scholar
  36. Hartmann AA, Barnard RL, Marhan S, Niklaus PA (2013) Effects of drought and N-fertilization on N cycling in two grassland soils. Oecologia 171:705–717PubMedCrossRefGoogle Scholar
  37. He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, 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 9:2364–2374PubMedCrossRefGoogle Scholar
  38. He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146–154CrossRefGoogle Scholar
  39. Head L, Adams M, McGregor HV, Toole S (2014) Climate change and Australia. WIREs Climate Change 5:175–197CrossRefGoogle Scholar
  40. Hearn AB, Fitt GP (1992) Cotton cropping systems. In: Pearson CJ (ed) Field crop ecosystems. Elsevier, Amsterdam, pp 85–142Google 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 72:5181–5189PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hu HW, Macdonald CA, Trivedi P, Holmes B, Bodrossy L, He JZ, Singh BK (2015) Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry subhumid ecosystems. Environ Microbiol 17:444–461PubMedCrossRefGoogle Scholar
  43. Hu HW, Macdonald CA, Trivedi P, Anderson IC, Zheng Y, Holmes B, Bodrossy L, Wand JT, He JZ, Singh BK (2016) Effects of climate warming and elevated CO2 on autotrophic nitrification and nitrifiers in dryland ecosystems. Soil Biol Biochem 92:1–15CrossRefGoogle Scholar
  44. Hueso S, García C, Hernández T (2012) Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biol Biochem 50:167–173CrossRefGoogle Scholar
  45. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  46. Jin ZJ, Li LQ, Liu XY, Pan GX, Qaiser H, Liu YZ (2014) Impact of long-term fertilization on community structure of Ammonia oxidizing and denitrifying Bacteria based on amoA and nirK genes in a Rice Paddy from Tai Lake region, China. J Integr Agric 13:2286–2298CrossRefGoogle Scholar
  47. Jung J, Yeom J, Kim J, Han J, Lim HS, Park H, Hyun S, Park W (2011) Change in gene abundance in the nitrogen biogeochemical cycle with temperature and nitrogen addition in Antarctic soils. Res Microbiol 162:1018–1026PubMedCrossRefGoogle Scholar
  48. Kadono A, Funakawa S, Kosaki T (2008) Factors controlling mineralization of soil organic matter in the Eurasian steppe. Soil Biol Biochem 40:947–955CrossRefGoogle Scholar
  49. Kandeler E, Böhm KE (1996) Temporal dynamics of microbial biomass, xylanase activity, N-mineralisation and potential nitrification in different tillage systems. Appl Soil Ecol 4:181–191CrossRefGoogle Scholar
  50. Kelly JJ, Policht K, Grancharova T, Hundal LS (2011) Distinct responses in ammonia-oxidizing archaea and bacteria after addition of biosolids to an agricultural soil. Appl Environ Microbiol 77:6551–6558PubMedPubMedCentralCrossRefGoogle Scholar
  51. Krček M, Slamka P, Olšovská K, Brestič M, Benčíková M (2008) Reduction of drought stress effect in spring barley (Hordeum vulgare L.) by nitrogen fertilization. Plant Soil Environ 54:7–13CrossRefGoogle Scholar
  52. Levičnik-Höfferle Š, Nicol GW, Ausec L, Mandić-Mulec I, Prosser JI (2012) Stimulation of thaumarchaeal ammonia oxidation by ammonia derived from organic nitrogen but not added inorganic nitrogen. FEMS Microbiol Ecol 80:114–123PubMedCrossRefGoogle Scholar
  53. Liu C, Wang K, Meng S, Zheng X, Zhou Z, Han S, Chen D, Yang Z (2011) Effects of irrigation, fertilization and crop straw management on nitrous oxide and nitric oxide emissions from a wheat–maize rotation field in northern China. Agric Ecosyst Environ 140:226–233CrossRefGoogle Scholar
  54. Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Singh BK (2016) Species identity of biocrust-forming lichens drives the response of soil nitrogen cycle to altered precipitation frequency and nitrogen amendment. Soil Biol Biochem 96:128–136CrossRefGoogle Scholar
  55. Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Wang JT, Singh BK (2017) Identity of biocrust species and microbial communities drive the response of multifunctionality to simulated global change. Soil Biol Biochem 107:208–217CrossRefGoogle Scholar
  56. Loecke TD, Cambardella CA, Liebman M (2012) Synchrony of net nitrogen mineralization and maize nitrogen uptake following applications of composted and fresh swine manure in the Midwest US. Nutr Cycl Agroecosyst 93:65–74CrossRefGoogle Scholar
  57. Lu Y, Sun Y, Liao Y, Nie J, Xie J, Yang Z, Zhou X (2015) Effects of the application of controlled release nitrogen fertilizer on rapeseed yield, agronomic characters and soil fertility. Agric Sci Technol 16:1216Google Scholar
  58. Macdonald BCT, Chang YF, Nadelko A, Tuomi S, Glover M (2017) Tracking fertiliser and soil nitrogen in irrigated cotton: uptake, losses, and the soil N stock. Soil Res 55:264–272CrossRefGoogle Scholar
  59. Malchair S, Carnol M (2013) AOB community structure and richness under European beech, sessile oak, Norway spruce and Douglas-fir at three temperate forest sites. Plant Soil 366:521–535CrossRefGoogle Scholar
  60. Malchair S, De Boeck H, Lemmens C, Ceulemans R, Merckx R, Nijs I, Carnol M (2010) Diversity–function relationship of ammonia-oxidizing bacteria in soils among functional groups of grassland species under climate warming. Appl Soil Ecol 44:15–23CrossRefGoogle Scholar
  61. Martens-Habbena W, Berube PM, Urakawa H, José R, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979PubMedCrossRefGoogle Scholar
  62. Martiny JB, Martiny AC, Weihe C, Lu Y, Berlemont R, Brodie EL, Goulden ML, Treseder KK, Allison SD (2017) Microbial legacies alter decomposition in response to simulated global change. ISME J 11:490–499PubMedCrossRefGoogle Scholar
  63. Meisner A, Bååth E, Rousk J (2013a) Microbial growth responses upon rewetting soil dried for four days or one year. Soil Biol Biochem 66:188–192CrossRefGoogle Scholar
  64. Meisner A, De Deyn GB, De Boer W, Van Der Putten WH (2013b) Soil biotic legacy effects of extreme weather events influence plant invasiveness. Proc Natl Acad Sci U S A 110:9835–9838PubMedPubMedCentralCrossRefGoogle Scholar
  65. Najeeb U, Bange MP, Tan DK, Atwell BJ (2015) Consequences of waterlogging in cotton and opportunities for mitigation of yield losses. AoB Plants 7:plv080PubMedPubMedCentralCrossRefGoogle Scholar
  66. Nguyen LT, Osanai Y, Anderson IC, Bange MP, Braunack M, Tissue DT, Singh BK (2018a) Impacts of waterlogging on soil nitrification and ammonia oxidising communities in farming system. Plant Soil 426:299–311CrossRefGoogle Scholar
  67. Nguyen LT, Osanai Y, Lai K, Anderson IC, Bange MP, Tissue DT, Singh BK (2018b) Responses of the soil microbial community to nitrogen fertilizer regimes and historical exposure to extreme weather events: flooding or prolonged-drought. Soil Biol Biochem 118:227–236CrossRefGoogle Scholar
  68. Northcote KH, Hubble G, Isbell R, Thompson C, Bettenay E (1975) A description of Australian soils. CSIRO Div. Soils, AustraliaGoogle Scholar
  69. Offre P, Kerou M, Spang A, Schleper C (2014) Variability of the transporter gene complement in ammonia-oxidizing archaea. Trends Microbiol 22:665–675PubMedCrossRefGoogle Scholar
  70. Ponnamperuma F (1984) Effects of flooding on soils. In: Flooding and plant growth. Academic Press, New York, pp 9–45CrossRefGoogle Scholar
  71. Rahimi A, Sayadi F, Dashti H (2013) Effects of water and nitrogen supply on growth, water-use efficiency and mucilage yield of isabgol (Plantago ovata Forsk). J Soil Sci Plant Nutr 13:341–354Google Scholar
  72. Rochester I, Constable G (2015) Improvements in nutrient uptake and nutrient use-efficiency in cotton cultivars released between 1973 and 2006. Field Crop Res 173:14–21CrossRefGoogle Scholar
  73. Rosenstock T, Liptzin D, Six J, Tomich T (2013) Nitrogen fertilizer use in California: assessing the data, trends and a way forward. Calif Agric 67:68–79CrossRefGoogle Scholar
  74. Rousk J, Smith AR, Jones DL (2013) Investigating the long-term legacy of drought on the soil microbial community across five European shrubland ecosystems. Glob Chang Biol 19(12):3872–3884PubMedCrossRefGoogle Scholar
  75. Scala DJ, Kerkhof LJ (1998) Nitrous oxide reductase (nosZ) gene-specific PCR primers for detection of denitrifiers and three nosZ genes from marine sediments. FEMS Microbiol Lett 162:61–68PubMedCrossRefGoogle Scholar
  76. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394PubMedCrossRefGoogle Scholar
  77. Schimel JP, Wetterstedt JM, Holden PA, Trumbore SE (2011) Drying/rewetting cycles mobilize old C from deep soils from a California annual grassland. Soil Biol Biochem 43:1101–1103CrossRefGoogle Scholar
  78. Schröder J, Neeteson J, Oenema O, Struik P (2000) Does the crop or the soil indicate how to save nitrogen in maize production?: reviewing the state of the art. Field Crop Res 66:151–164CrossRefGoogle Scholar
  79. 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 10:1601–1611PubMedCrossRefGoogle Scholar
  80. Shen XY, Zhang LM, Shen JP, Li LH, Yuan CL, He JZ (2011) Nitrogen loading levels affect abundance and composition of soil ammonia oxidizing prokaryotes in semiarid temperate grassland. J Soils Sediments 11:1243–1252CrossRefGoogle Scholar
  81. Smith MS, Tiedje M (1979) Phases of denitrification following oxygen depletion in soil. Soil Biol Biochem 11:261–267CrossRefGoogle Scholar
  82. Stark JM, Firestone MK (1995) Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol 61:218–221PubMedPubMedCentralGoogle Scholar
  83. Stres B, Mahne I, Avguštin G, Tiedje JM (2004) Nitrous oxide reductase (nosZ) gene fragments differ between native and cultivated Michigan soils. Appl Environ Microbiol 70:301–309PubMedPubMedCentralCrossRefGoogle Scholar
  84. Thion C, Prosser JI (2014) Differential response of nonadapted ammonia-oxidising archaea and bacteria to drying–rewetting stress. FEMS Microbiol Ecol 90:380–389PubMedGoogle Scholar
  85. Tian XF, Hu HW, Ding Q, Song MH, Xu XL, Zheng Y, Guo LD (2014) Influence of nitrogen fertilization on soil ammonia oxidizer and denitrifier abundance, microbial biomass, and enzyme activities in an alpine meadow. Biol Fertil Soils 50:703–713CrossRefGoogle Scholar
  86. Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. Biol Anaerobic Microorg 717:179–244Google Scholar
  87. Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108:8420–8425PubMedPubMedCentralCrossRefGoogle Scholar
  88. Treseder KK, Balser TC, Bradford MA, Brodie DL, Dubinsky EA, Eviner VT, Hofmockel KS, Lennon JT, Levine UY, MacGregor BJ, Pett-Ridge J, Waldrop MD (2012) Integrating microbial ecology into ecosystem models: challenges and priorities. Biogeochemistry 109:7–18CrossRefGoogle Scholar
  89. Uchida Y, Wang Y, Akiyama H, Nakajma Y, Hayatsu M (2014) Expression of denitrification genes in response to a waterlogging event in a Fluvisol and its relationship with large nitrous oxide pulses. FEMS Microbiol Ecol 88:407–423PubMedCrossRefGoogle Scholar
  90. Van Meeteren M, Tietema A, Van Loon E, Verstraten J (2008) Microbial dynamics and litter decomposition under a changed climate in a Dutch heathland. Appl Soil Ecol 38:119–127CrossRefGoogle Scholar
  91. Voroney R (2007) The soil habitat. In: Paul EA (ed) Soil microbiology, ecology, and biochemistry. Academic Press, Burlington, pp 25–49CrossRefGoogle Scholar
  92. Walker C, De La Torre J, Klotz M, Urakawa H, Pinel N, Arp D, Brochier-Armanet C, Chain P, Chan P, Gollabgir A (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci U S A 107:8818–8823PubMedPubMedCentralCrossRefGoogle Scholar
  93. Wallenstein MD, Peterjohn WT, Schlesinger WH (2006) N fertilization effects on denitrification and N cycling in an aggrading forest. Ecol Appl 16:2168–2176PubMedCrossRefGoogle Scholar
  94. Wang J, Xiong Z, Yan X (2011) Fertilizer-induced emission factors and background emissions of N2O from vegetable fields in China. Atmos Environ 45:6923–6929CrossRefGoogle Scholar
  95. Webster G, Embley TM, Freitag TE, Smith Z, Prosser JI (2005) Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ Microbiol 7:676–684PubMedCrossRefGoogle Scholar
  96. Wegner LH (2010) Oxygen transport in waterlogged plants. In: Mancuso S, Shabala S (eds) Waterlogging Signalling and tolerance in plants. Springer, Berlin, pp 3–22CrossRefGoogle Scholar
  97. Wertz S, Leigh AK, Grayston SJ (2012) Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol Ecol 79:142–154PubMedCrossRefGoogle Scholar
  98. 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 48:261–271PubMedCrossRefGoogle Scholar
  99. Xu Z, Zhou G, Shimizu H (2010) Plant responses to drought and rewatering. Plant Signal Behav 5:649–654PubMedPubMedCentralCrossRefGoogle Scholar
  100. Xu N, Guo W, Liu J, Du N, Wang R (2015) Increased nitrogen deposition alleviated the adverse effects of drought stress on Quercus variabilis and Quercus mongolica seedlings. Acta Physiol Plant 37:1–11CrossRefGoogle Scholar
  101. Yang H, Sheng R, Zhang Z, Wang L, Wang Q, Wei W (2016) Responses of nitrifying and denitrifying bacteria to flooding-drying cycles in flooded rice soil. Appl Soil Ecol 103:101–109CrossRefGoogle Scholar
  102. 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 6:1032–1045PubMedCrossRefGoogle Scholar
  103. Zhang X, Wang Q, Xu J, Gilliam FS, Tremblay N, Li C (2015) In situ nitrogen mineralization, nitrification, and ammonia volatilization in maize field fertilized with urea in Huanghuaihai region of northern China. PLoS One 10:e0115649PubMedPubMedCentralCrossRefGoogle Scholar
  104. Zhou Z, Shi X, Zheng Y, Qin Z, Xie D, Li Z, Guo T (2014) Abundance and community structure of ammonia-oxidizing bacteria and archaea in purple soil under long-term fertilization. Eur J Soil Biol 60:24–33CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia
  2. 2.School of Environmental and Rural SciencesUniversity of New EnglandArmidaleAustralia
  3. 3.CSIRO Agriculture and FoodAustralian Cotton Research InstituteNarrabriAustralia
  4. 4.Global Centre for Land-Based InnovationWestern Sydney UniversityPenrithAustralia

Personalised recommendations