Skip to main content
SpringerLink
Log in

Dynamics of N2O in vicinity of plant residues: a microsensor approach

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Plant residues decomposing within the soil matrix are known to serve as hotspots of N2O production. However, the lack of technical tools for microscale in-situ N2O measurements limits understanding of hotspot functioning. Our aim was to assess performance of microsensor technology for evaluating the temporal patterns of N2O production in immediate vicinity to decomposing plant residues.

Methods

We incorporated intact switchgrass leaves and roots into soil matrix and monitored O2 depletion and N2O production using electrochemical microsensors along with N2O emission from the soil. We also measured residue’s water absorption and b-glucosidase activity on the surface of the residue - the characteristics related to microenvironmental conditions and biological activity near the residue.

Results

N2O production in the vicinity of switchgrass residues began within 0–12 h after the wetting, reached peak at ~0.6 day and decreased by day 2. N2O was higher near leaf than near root residues due to greater leaf N contents and water absorption by the leaves. However, N2O production near the roots started sooner than near the leaves, in part due to high initial enzyme levels on root surfaces.

Conclusion

Electrochemical microsensor is a useful tool for in-situ micro-scale N2O monitoring in immediate vicinity of soil incorporated plant residues. Monitoring provided valuable information on N2O production near leaves and roots, its temporal dynamic, and the factors affecting it. The N2O production from residues measured by microsensors was consistent with the N2O emission from the whole soil, demonstrating the validity of the microsensors for N2O hotspot studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

Abbreviations

MUF:

4-Methylumbelliferone

PAS:

Photoacoustic Spectroscopy

Substrate:

4-Methylumbelliferyl-β-D-Glucoside

UV:

Ultraviolet

References

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

    Article  CAS  Google Scholar 

  • Azam F, Müller C, Weiske A, Benckiser G, Ottow J (2002) Nitrification and denitrification as sources of atmospheric nitrous oxide–role of oxidizable carbon and applied nitrogen. Biol Fertil Soils 35:54–61

    Article  CAS  Google Scholar 

  • Baggs E, Rees R, Smith K, Vinten A (2000) Nitrous oxide emission from soils after incorporating crop residues. Soil Use Manag 16:82–87

    Article  Google Scholar 

  • Beauchamp E (1997) Nitrous oxide emission from agricultural soils. Can J Soil Sci 77:113–123

    Article  CAS  Google Scholar 

  • Birouste M, Kazakou E, Blanchard A, Roumet C (2012) Plant traits and decomposition: are the relationships for roots comparable to those for leaves? Ann Bot 109:463–472

    Article  PubMed  Google Scholar 

  • Blackmer A, Bremner J (1978) Inhibitory effect of nitrate on reduction of N2O to N2 by soil microorganisms. Soil Biol Biochem 10:187–191

    Article  CAS  Google Scholar 

  • Bragg J, Tomasi P, Zhang L, Williams T, Wood D, Lovell JT, Healey A, Schmutz J, Bonnette JE, Cheng P (2020) Environmentally responsive QTL controlling surface wax load in switchgrass. Theor Appl Genet 133:3119–3137

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cayuela M, Sinicco T, Mondini C (2009) Mineralization dynamics and biochemical properties during initial decomposition of plant and animal residues in soil. Appl Soil Ecol 41:118–127

    Article  Google Scholar 

  • Chen H, Li X, Hu F, Shi W (2013) Soil nitrous oxide emissions following crop residue addition: a meta-analysis. Glob Chang Biol 19:2956–2964

    Article  PubMed  Google Scholar 

  • Dalsgaard T, Revsbech NP (1992) Regulating factors of denitrification in trickling filter biofilms as measured with the oxygen/nitrous oxide microsensor. FEMS Microbiol Lett 101:151–164

    Article  CAS  Google Scholar 

  • De Catanzaro J, Beauchamp E (1985) The effect of some carbon substrates on denitrification rates and carbon utilization in soil. Biol Fertil Soils 1:183–187

    Article  Google Scholar 

  • Edmonds RL (1980) Litter decomposition and nutrient release in Douglas-fir, red alder, western hemlock, and Pacific silver fir ecosystems in western Washington. Can J For Res 10:327–337

    Article  Google Scholar 

  • Gaillard V, Chenu C, Recous S (2003) Carbon mineralisation in soil adjacent to plant residues of contrasting biochemical quality. Soil Biol Biochem 35:93–99

    Article  CAS  Google Scholar 

  • Gaillard V, Chenu C, Recous S, Richard G (1999) Carbon, nitrogen and microbial gradients induced by plant residues decomposing in soil. Eur J Soil Sci 50:567–578

    Article  Google Scholar 

  • Garcia-Ruiz R, Baggs E (2007) N 2 O emission from soil following combined application of fertiliser-N and ground weed residues. Plant Soil 299:263–274

    Article  CAS  Google Scholar 

  • Goodroad L, Keeney D, Peterson L (1984) Nitrous oxide emissions from agricultural soils in Wisconsin. J Environ Qual 13:557–561

    Article  CAS  Google Scholar 

  • Guber AK, Kravchenko AN, Razavi BS, Blagodatskaya E, Kuzyakov Y (2019) Calibration of 2-D soil zymography for correct analysis of enzyme distribution. Eur J Soil Sci 70:715–726

    Article  CAS  Google Scholar 

  • Hansen M, Clough TJ, Elberling B (2014) Flooding-induced N2O emission bursts controlled by pH and nitrate in agricultural soils. Soil Biol Biochem 69:17–24

    Article  CAS  Google Scholar 

  • Hayashi K, Tokida T, Kajiura M, Yanai Y, Yano M (2015) Cropland soil–plant systems control production and consumption of methane and nitrous oxide and their emissions to the atmosphere. Soil science and plant nutrition 61:2–33

    Article  CAS  Google Scholar 

  • Højberg O, Revsbech NP, Tiedje JM (1994) Denitrification in soil aggregates analyzed with microsensors for nitrous oxide and oxygen. Soil Sci Soc Am J 58:1691–1698

    Article  Google Scholar 

  • Hwang S, Hanaki K (2000) Effects of oxygen concentration and moisture content of refuse on nitrification, denitrification and nitrous oxide production. Bioresour Technol 71:159–165

    Article  CAS  Google Scholar 

  • Jørgensen CJ, Elberling B (2012) Effects of flooding-induced N2O production, consumption and emission dynamics on the annual N2O emission budget in wetland soil. Soil Biol Biochem 53:9–17

    Article  Google Scholar 

  • Kang H, Freeman C, Lock M (1998) Trace gas emissions from a North Wales fen-role of hydrochemistry and soil enzyme activity. Water Air Soil Pollut 105:107–116

    Article  CAS  Google Scholar 

  • Khalil K, Mary B, Renault P (2004) Nitrous oxide production by nitrification and denitrification in soil aggregates as affected by O2 concentration. Soil Biol Biochem 36:687–699

    Article  CAS  Google Scholar 

  • Kim K, Guber A, Rivers M, Kravchenko A (2020) Contribution of decomposing plant roots to N2O emissions by water absorption. Geoderma 375:114506

    Article  CAS  Google Scholar 

  • Kravchenko A, Toosi E, Guber A, Ostrom N, Yu J, Azeem K, Rivers M, Robertson G (2017) Hotspots of soil N 2 O emission enhanced through water absorption by plant residue. Nat Geosci 10:496–500

    Article  CAS  Google Scholar 

  • Kravchenko A, Fry J, Guber A (2018) Water absorption capacity of soil-incorporated plant leaves can affect N2O emissions and soil inorganic N concentrations. Soil Biol Biochem 121:113–119

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199

    Article  CAS  Google Scholar 

  • Li X, Sørensen P, Olesen JE, Petersen SO (2016) Evidence for denitrification as main source of N2O emission from residue-amended soil. Soil Biol Biochem 92:153–160

    Article  CAS  Google Scholar 

  • Liengaard L, Figueiredo V, Markfoged R, Revsbech NP, Nielsen LP, Prast AE, Kühl M (2014) Hot moments of N2O transformation and emission in tropical soils from the Pantanal and the Amazon (Brazil). Soil Biol Biochem 75:26–36

    Article  CAS  Google Scholar 

  • Loecke TD, Robertson GP (2009) Soil resource heterogeneity in terms of litter aggregation promotes nitrous oxide fluxes and slows decomposition. Soil Biol Biochem 41:228–235

    Article  CAS  Google Scholar 

  • Markfoged R, Nielsen LP, Nyord T, Ottosen LDM, Revsbech NP (2011) Transient N2O accumulation and emission caused by O2 depletion in soil after liquid manure injection. Eur J Soil Sci 62:541–550

    Article  CAS  Google Scholar 

  • McKenney D, Drury C, Wang S (2001) Effects of oxygen on denitrification inhibition, repression, and derepression in soil columns. Soil Sci Soc Am J 65:126–132

    Article  CAS  Google Scholar 

  • Meyer RL, Allen DE, Schmidt S (2008) Nitrification and denitrification as sources of sediment nitrous oxide production: a microsensor approach. Mar Chem 110:68–76

    Article  CAS  Google Scholar 

  • Millar N, Baggs E (2004) Chemical composition, or quality, of agroforestry residues influences N2O emissions after their addition to soil. Soil Biol Biochem 36:935–943

    Article  CAS  Google Scholar 

  • Milliken GA, Johnson DE (2009) Analysis of messy data volume 1: designed experiments. CRC Press

  • Morley N, Baggs E (2010) Carbon and oxygen controls on N2O and N2 production during nitrate reduction. Soil Biol Biochem 42:1864–1871

    Article  CAS  Google Scholar 

  • Myrold DD, Tiedje JM (1985) Establishment of denitrification capacity in soil: effects of carbon, nitrate and moisture. Soil Biol Biochem 17:819–822

    Article  CAS  Google Scholar 

  • Nagahashi G, Baker AF (1984) β-Glucosidase activity in corn roots: problems in subcellular fractionation. Plant Physiol 76:861–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negassa WC, Guber AK, Kravchenko AN, Marsh TL, Hildebrandt B, Rivers ML (2015) Properties of soil pore space regulate pathways of plant residue decomposition and community structure of associated bacteria PLoS one:10

  • Nielsen LP, Christensen PB, Revsbech NP, Sørensen J (1990) Denitrification and oxygen respiration in biofilms studied with a microsensor for nitrous oxide and oxygen. Microb Ecol 19:63–72

    Article  CAS  PubMed  Google Scholar 

  • Oates LG, Duncan DS, Gelfand I, Millar N, Robertson GP, Jackson RD (2016) Nitrous oxide emissions during establishment of eight alternative cellulosic bioenergy cropping systems in the north Central United States. GCB Bioenergy 8:539–549

    Article  CAS  Google Scholar 

  • Parkin TB (1987) Soil microsites as a source of denitrification variability 1. Soil Sci Soc Am J 51:1194–1199

    Article  CAS  Google Scholar 

  • Parsons LL, Smith MS, Murray RE (1991) Soil denitrification dynamics: spatial and temporal variations of enzyme activity, populations, and nitrogen gas loss. Soil Sci Soc Am J 55:90–95

    Article  CAS  Google Scholar 

  • Partey S, Preziosi R, Robson G (2014) Improving maize residue use in soil fertility restoration by mixing with residues of low C-to-N ratio: effects on C and N mineralization and soil microbial biomass. J Soil Sci Plant Nutr 14:518–531

    Google Scholar 

  • Razavi BS, Zarebanadkouki M, Blagodatskaya E, Kuzyakov Y (2016) Rhizosphere shape of lentil and maize: spatial distribution of enzyme activities. Soil Biol Biochem 96:229–237

    Article  CAS  Google Scholar 

  • Revsbech N, 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 

  • Revsbech NP, Nielsen LP, Christensen PB, Sørensen J (1988) Combined oxygen and nitrous oxide microsensor for denitrification studies. Appl Environ Microbiol 54:2245–2249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riederer M, Schreiber L (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot 52:2023–2032

    Article  CAS  PubMed  Google Scholar 

  • Rohe L, Apelt B, Vogel H-J, Well R, Wu G-M, Schlüter S (2020) Denitrification in soil as a function of oxygen supply and demand at the microscale. Biogeosci Discuss:1–32

  • Schimel J, Becerra CA, Blankinship J (2017) Estimating decay dynamics for enzyme activities in soils from different ecosystems. Soil Biol Biochem 114:5–11

    Article  CAS  Google Scholar 

  • Senbayram M, Chen R, Budai A, Bakken L, Dittert K (2012) N2O emission and the N2O/(N2O+ N2) product ratio of denitrification as controlled by available carbon substrates and nitrate concentrations. Agric Ecosyst Environ 147:4–12

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Article  PubMed  Google Scholar 

  • Smith MS, Tiedje JM (1979) Phases of denitrification following oxygen depletion in soil. Soil Biol Biochem 11:261–267

    Article  CAS  Google Scholar 

  • Spohn M, Carminati A, Kuzyakov Y (2013) Soil zymography–a novel in situ method for mapping distribution of enzyme activity in soil. Soil Biol Biochem 58:275–280

    Article  CAS  Google Scholar 

  • Steffens C, Helfrich M, Joergensen RG, Eissfeller V, Flessa H (2015) Translocation of 13C-labeled leaf or root litter carbon of beech (Fagus sylvatica L.) and ash (Fraxinus excelsior L.) during decomposition–a laboratory incubation experiment. Soil Biol Biochem 83:125–137

    Article  CAS  Google Scholar 

  • Toosi E, Kravchenko A, Guber A, Rivers M (2017) Pore characteristics regulate priming and fate of carbon from plant residue. Soil Biol Biochem 113:219–230

    Article  CAS  Google Scholar 

  • Uselman SM, Qualls RG, Lilienfein J (2012) Quality of soluble organic C, N, and P produced by different types and species of litter: root litter versus leaf litter. Soil Biol Biochem 54:57–67

    Article  CAS  Google Scholar 

  • Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106

    Article  CAS  Google Scholar 

  • Wang JJ, Tharayil N, Chow AT, Suseela V, Zeng H (2015) Phenolic profile within the fine-root branching orders of an evergreen species highlights a disconnect in root tissue quality predicted by elemental-and molecular-level carbon composition. New Phytol 206:1261–1273

    Article  CAS  PubMed  Google Scholar 

  • Wu D, Wei Z, Well R, Shan J, Yan X, Bol R, Senbayram M (2018) Straw amendment with nitrate-N decreased N2O/(N2O+ N2) ratio but increased soil N2O emission: a case study of direct soil-born N2 measurements. Soil Biol Biochem 127:301–304

    Article  CAS  Google Scholar 

  • Yeats TH, Rose JK (2013) The formation and function of plant cuticles. Plant Physiol 163:5–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Hui D, Luo Y, Zhou G (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85–93

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Chelsea Mamott and GLBRC communication team for help with figure preparations. We also thank Dr. Dirk Colbry for help with data processing and Maxwell Oerther for assisting in laboratory work.

Availability of data and material

Not applicable.

Code availability

Not applicable.

Funding

This work was funded in part by the National Science Foundation’s Geobiology and Low Temperature Geochemistry Program (Award 1630399). This material is based upon work supported in part by the Great Lakes Bioenergy Research Center, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC0018409. Support for this research was provided by the National Science Foundation Long-term Ecological Research Program (DEB 1832042) at the Kellogg Biological Station, and by Michigan State University AgBioResearch.

Author information

Authors and Affiliations

  1. Department of Plant Soil and Microbial Sciences, Michigan State University, East Lansing, MI, 48823, USA

    Kyungmin Kim, Turgut Kutlu, Alexandra Kravchenko & Andrey Guber

  2. DOE Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, 48823, USA

    Kyungmin Kim, Alexandra Kravchenko & Andrey Guber

Authors
  1. Kyungmin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Turgut Kutlu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexandra Kravchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrey Guber
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.K and A.G. designed and directed the project. T.K. and A.G. worked out technical details and performed calibrations for the microsensor experiment. All the authors performed the experiments. K.K., A.K., and A.G processed analyzed the data. All authors discussed the results and K.K. and A.K. wrote the manuscript.

Corresponding author

Correspondence to Kyungmin Kim.

Ethics declarations

Conflict of interest

Not applicable.

Additional information

Responsible Editor: Feike A. Dijkstra

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 258 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, K., Kutlu, T., Kravchenko, A. et al. Dynamics of N2O in vicinity of plant residues: a microsensor approach. Plant Soil 462, 331–347 (2021). https://doi.org/10.1007/s11104-021-04871-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-04871-7

Keywords

Search

Navigation