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Warming-induced enhancement of soil N2O efflux linked to distinct response times of genes driving N2O production and consumption

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Abstract

Temperature responses of denitrifying microbes likely play a governing role in the production and consumption of N2O. We investigated temperature effects on denitrifier communities and their potential to produce N2O and N2 by incubating grassland soils collected in multiple seasons at four temperatures with 15N-enriched NO3 for ~24 h. We quantified [N2O] concentration across time, estimated its production and reduction to N2, and quantified relative abundance of genes responsible for N2O production (cnorB) and reduction (nosZ). In all seasons, net N2O production was positively linked to incubation temperature, with highest estimates of net and gross N2O production in late spring soils. N2O dynamics were tightly coupled to changes in denitrifier community structure, which occurred on both seasonal and incubation time scales. We observed increases in nosZ abundance with increasing incubation temperature after 24 h, and relatively larger increases in cnorB abundance from winter to late June. The difference between incubation and in situ temperature was a robust predictor of cnorB:nosZ. These data provide convincing evidence that short-term increases in temperature can induce remarkably rapid changes in community structure that increase the potential for reduction of N2O to N2, and that seasonal adaptation of denitrifying communities is linked to seasonal changes in potential N2O production, with warmer seasons linked to large increases in N2O production potential. This work helps explain observations of high spatial and temporal variation in N2O effluxes, and highlights the importance of temperature as an influence on denitrification enzyme kinetics, denitrifier physiology and community adaptations, and associated N2O efflux and reduction.

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References

  • Abdalla M, Jones M, Smith P, Williams M (2009) Nitrous oxide fluxes and denitrification sensitivity to temperature in Irish pasture soils. Soil Use Manage 25:376–388

    Article  Google Scholar 

  • Ambus P (1993) Control of denitrification enzyme activity in a streamside soil. FEMS Microbiol Ecol 102:225–234

    Article  Google Scholar 

  • Barnard R, Leadley PW (2005) Global change, nitrification, denitrification: A review. Gl Biogeochem Cycles 19:GB1007. doi:10.1029/2004GB002282

  • Bergaust L, Shapleigh J, Frostegard A, Bakken L (2008) Transcription and activities of NOx reductases in Agrobacterium tumefaciens: the influence of nitrate, nitrite and oxygen availability. Environ Microbiol 10:3070–3081

    Article  Google Scholar 

  • Berks BC, Baratta D, Richardson DJ, Ferguson SJ (1993) Purification and characterization of a nitrous oxide reductase from Thiosphaera pantotropha. Eur J Biochem 212:467–476

    Article  Google Scholar 

  • Billings SA (2008) Nitrous oxide in flux. Nature 456:888–889

    Article  Google Scholar 

  • Billings SA, Ballantyne F (2013) How interactions between microbial resource demands, soil organic matter stoichiometry, and substrate reactivity determine the direction and magnitude of soil respiratory responses to warming. Glob Change Biol 19:90–102

    Article  Google Scholar 

  • Bouletreau S, Salvo E, Lyautey E, Mastrorillo S, Garabetian F (2012) Temperature dependence of denitrification in phototrophic river biofilms. Sci Total Environ 416:323–328

    Article  Google Scholar 

  • Bradford MA (2013) Thermal adaptation of decomposer communities in warming soils. Front Microbiol. doi:10.3389/fmicb.2013.00333

    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  Google Scholar 

  • Braker G, Schwarz J, Conrad R (2010) Influence of temperature on the composition and activity of denitrifying soil communities. FEMS Microbiol Ecol 73:134–148

    Google Scholar 

  • Castaldi S (2000) Responses of nitrous oxide, dinitrogen and carbon dioxide production and oxygen consumption to temperature in forest and agriculture light-textured soils determined by model experiment. Biol Fertil Soils 32:67–72

    Article  Google Scholar 

  • Cavigelli MA, Robertson GP (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–1414

    Article  Google Scholar 

  • Chapuis-Lardy L, Wrage N, Metay A, Chotte JL, Bernoux M (2007) Soils, a sink for N2O? A review. Glob Change Biol 13:1–17

    Article  Google Scholar 

  • Del Grosso SJ, Perton WJ, Mosier AR, Ojima DS, Kulmala AE, Phongpan S (2000) General model for N2O and N2 gas emissions from soils due to denitrification. Glob Biogeochem Cycles 14:1045–1060

    Article  Google Scholar 

  • Doyle A, Weintraub MN, Schimel JP (2004) Persulfate digestion and simultaneous colorimetric analysis of carbon and nitrogen in soil extracts. Soil Sci Soc Am J 68:669–676

    Article  Google Scholar 

  • Firestone MK, Davidson EA (1989) Microbiological basis of NO and N2O production and consumption in soil. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the atmosphere. Wiley, Chichester, pp 7–21

    Google Scholar 

  • Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nature Clim Change 3:395–398

    Article  Google Scholar 

  • Gamble TN, Betiach MR, Tiedje JM (1977) Numerically dominant denitrifying bacteria from world soils. Appl Environ Microbiol 33:926–939

    Google Scholar 

  • Goldberg SD, Gebauer G (2009) Drought turns a Central European Norway spruce forest soil from an N2O source to a transient N2O sink. Glob Change Biol 15:850–860

    Article  Google Scholar 

  • Grant RF, Pattey E (2008) Temperature sensitivity of N2O emissions from fertilized agricultural soils: Mathematical modeling in ecosystems. Glob Biogeochem Cycles 22:GB4019. doi:10.1029/2008GB003273

  • Groffman PM, Brumme R, Butterbach-Bahl K, Dobbie KE, Mosier AR, Ojima D, Papen H, Parton WJ, Smith KA, Wagner-Riddle C (2000) Evaluating annual nitrous oxide fluxes at the ecosystem scale. Glob Biogeochem Cycles 14:1061–1070

    Article  Google Scholar 

  • Holtan-Hartwig L, Dörsch P, Bakken LR (2000) Comparison of denitrifying communities in organic soils: kinetics of NO3 and N2O reduction. Soil Biol Biochem 32:833–843

    Article  Google Scholar 

  • Holtan-Hartwig L, Dörsch P, Bakken LR (2002) Low temperature control of soil denitrifying communities: kinetics of N2O production and reduction. Soil Biol Biochem 34:1797–1806

    Article  Google Scholar 

  • Inselsbacher E, Hinko-Najera Umana N, Stange FC et al (2010) Short-term competition between crop plants and soil microbes for inorganic N fertilizer. Soil Biol Biochem 42:360–372

    Article  Google Scholar 

  • 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, Cambridge

  • Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7

    Article  Google Scholar 

  • Jung J, Yeom J, Han J, Kim J, Park W (2012) Seasonal changes in nitrogen-cycle gene abundances and in bacterial communities in acidic forest soils. J Microbiol 3:365–373

    Article  Google Scholar 

  • Körner H, Zumft WG (1989) Expression of denitrification enzymes in response to the dissolved oxygen level and respiratory substrate in continuous culture of Pseudomonas stutzeri. Appl Environ Microbiol 55:1670–1676

    Google Scholar 

  • Kraigher B, Stres B, Hacin J, Ausec L, Mahne I, van Elsa JD, Mandic-Mulec I (2006) Microbial activity and community structure in two drained fen soils in the Ljubljana Marsh. Soil Biol Biochem 36:757–766

    Google Scholar 

  • Kulkarni MV, Groffman PM, Yavitt JB (2008) Solving the global nitrogen problem: it’s a gas! Front Ecol Environ 6:199–206

    Article  Google Scholar 

  • Lehmeier CA, Min K, Niehues ND, Ballantyne F IV, Billings SA (2013) Temperature-mediated changes of exoenzyme-substrate reaction rates and their consequences for the carbon to nitrogen flow ratio of liberated resources. Soil Biol Biochem 57:374–382

    Article  Google Scholar 

  • Linn DM, Doran JW (1984) Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci Soc Am J 48:1267–1272

    Article  Google Scholar 

  • Maag M, Vinther FP (1996) Nitrous oxide emission by nitrification and denitrification in different soil types and at different soil moisture contents and temperatures. Appl Soil Ecol 4:5–14

    Article  Google Scholar 

  • Maag M, Vinther FP (1999) Effect of temperature and water on gaseous emissions from soils treated with animal slurry. Soil Sci Soc Am J 63:858–865

    Article  Google Scholar 

  • McClain ME, Boyer EW, Dent CL et al (2003) Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–312

    Article  Google Scholar 

  • Mergel A, Schmitz O, Mallmann T, Bothe H (2001) Relative abundance of denitrifying and dinitrogen-fixing bacteria in layers of a forest soil. FEMS Microbiol Ecol 36:33–42

    Article  Google Scholar 

  • Morse JL, Bernhardt ES (2013) Using 15N tracers to estimate N2O and N2 emissions from nitrification and denitrification in coastal plain wetlands under contrasting land-uses. Soil Biol Biochem 57:635–643

    Article  Google Scholar 

  • Öquist MG, Nilsson M, Sorensson F, Kasimir-Klemedtsson A, Persson T, Weslien P, Klemedtsson LK (2002) Nitrous oxide production in a forest soil at low temperatures—processes and environmental controls. FEMS Microbiol Ecol 49:371–378

    Article  Google Scholar 

  • Peterjohn WT (1991) Denitrification: enzyme content and activity in desert soils. Soil Biol Biochem 23:845–855

    Article  Google Scholar 

  • Peterjohn WT, Melillo JM, Steudler PA, Newkirk KM, Bowles FP, Aber JD (1994) Responses of trace gas fluxes and N availability to experimentally elevated soil temperatures. Ecol Appl 4:617–625

    Article  Google Scholar 

  • Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14:993–1008

    Article  Google Scholar 

  • Philippot L, Mirleau P, Mazurier S, Siblot S, Hartmann A, Lemanceau P, Germon JC (2001) Characterization and transcriptional analysis of Pseudomonas fluorescens denitrifying clusters containing the nar, nir, nor and nos genes. Biochim Biophys Acta Gene Struct Express 1517:436–440

    Article  Google Scholar 

  • Philippot L, Andert J, Jones CM, Bru D, Hallin S (2011) Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Glob Change Biol 17:1497–1504

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Rösch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol 68:3818–3829

    Article  Google Scholar 

  • Saad OA, Conrad R (1993) Temperature dependence of nitrification, denitrification, and turnover of nitric oxide in different soils. Biol Fertil Soils 15:21–27

    Article  Google Scholar 

  • Saleh-Lakha S, Shannon KE, Henderson SL, Goyer C, Trevors JT, Zebarth BJ, Burton DL (2009) Effect of pH and temperature on denitrification gene expression and activity in Pseudomonas mandelii. Appl Environ Microbiol 75:3903–3911

    Article  Google Scholar 

  • Sanford RA, Wagner DD, Wu Q et al (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci 109:19709–19714

    Article  Google Scholar 

  • Silver WL, Thompson AW, Reich A, Ewel JJ, Firestone MK (2005) Nitrogen cycling in tropical plantation forests: potential controls on nitrogen retention. Ecol Appl 15:1604–1614

    Article  Google Scholar 

  • Stres B, Danevčič T, Pal L et al (2008) Influence of temperature and soil water content on bacterial, archaeal and denitrifying microbial communities in drained fen grassland soil microcosms. FEMS Microbiol Ecol 66:110–122

    Article  Google Scholar 

  • Szukics U, Abell GC, Hödl V, Mitter B, Sessitsch A, Hackl E, Zechmeister-Boltenstern S (2010) Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol Ecol 72:395–406

    Article  Google Scholar 

  • Tiemann LK, Billings SA (2012) Tracking C and N flows through microbial biomass with increased soil moisture variability. Soil Biol Biochem 49:11–22

    Article  Google Scholar 

  • Wallenstein MD, Vilgalys RJ (2005) Quantitative analyses of nitrogen cycling genes in soils. Pedobiologia 49:665–672

    Article  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  Google Scholar 

  • Xu-Ri, Prentice CI, Spahni R, Niu HS (2012) Modelling terrestrial nitrous oxide emissions and implications for climate feedback. New Phytol 196:472–488

    Article  Google Scholar 

  • Zhang L, Shoun H (2008) Purification and functional analysis of fungal nitric oxide reductase cytochrome P450nor. Meth Enzym 437:117–133

    Google Scholar 

  • Yergeau E, Kang S, He Z, Zhou J, Kowalchuk GA (2007) Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J 1:163–179

    Article  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616

    Google Scholar 

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Acknowledgments

This research was supported by NSF DEB-0910343. We thank Stefany Molina and Ryan Rastok, who assisted with field and lab work, and Dr. Jude Kastens and Dr. Bryan Young who provided insights during data analysis. Three anonymous reviewers provided valuable feedback. This study was conducted at and supported by the University of Kansas Field station, a research unit of the Kansas Biological Survey and the University of Kansas.

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Correspondence to S. A. Billings.

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Billings, S.A., Tiemann, L.K. Warming-induced enhancement of soil N2O efflux linked to distinct response times of genes driving N2O production and consumption. Biogeochemistry 119, 371–386 (2014). https://doi.org/10.1007/s10533-014-9973-2

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