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Long-term nitrogen addition suppresses microbial degradation, enhances soil carbon storage, and alters the molecular composition of soil organic matter

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Abstract

Forest soil organic carbon (SOC) is one of the largest reservoirs of terrestrial carbon (C) and is a major component of the global C cycle. Yet there is still uncertainty regarding how ecosystems, and the SOC they store, will respond to changes due to anthropogenic processes. Current and future reactive nitrogen (N) deposition to forest soils may alter biogeochemical processes and shift both the quantity and quality of stored SOC. We studied SOC storage and molecular-level composition after 22 years of N additions (100 kg N ha−1 y−1) in a temperate deciduous forest. SOC storage in surface soils increased by 0.93 kg m−2 due to a decline in microbial biomass (phospholipid fatty acids) and litter decomposition. N additions resulted in the selective preservation of a range of plant-derived compounds including steroids, lignin-derived, cutin-derived, and suberin-derived compounds that have anti-microbial properties or are non-preferred microbial substrates. This overall shift in SOC composition suggests limited sustainability and a decline in soil health. The reduction in microbial biomass and increase in specific SOC components demonstrate that long-term N fertilization negatively alters fundamental C cycling in forest soils. This study also demonstrates unequivocally that anthropogenic impacts on C and N cycling in forests at the molecular-level must be considered more holistically.

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References

  • Aber J, McDowell W, Nadelhoffer K et al (1998) Nitrogen saturation in temperate forest ecosystems. Bioscience 48:921–934

    Article  Google Scholar 

  • Adamczyk S, Adamczyk B, Kitunen V, Smolander A (2015) Monoterpenes and higher terpenes may inhibit enzyme activities in boreal forest soil. Soil Biol Biochem 87:59–66

    Article  Google Scholar 

  • Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1156–1168

    Article  Google Scholar 

  • Angst G, Heinrich L, Kögel-Knabner I, Mueller CW (2016) The fate of cutin and suberin of decaying leaves, needles and roots—inferences from the initial decomposition of bound fatty acids. Org Geochem 95:81–92

    Article  Google Scholar 

  • Baldock JA, Oades JM, Waters AG et al (1992) Aspects of the chemical structure of soil organic materials as revealed by solid-state 13C NMR spectroscopy. Biogeochemistry 16:1–42

    Article  Google Scholar 

  • Bhatnagar JM, Peay KG, Treseder KK (2018) Litter chemistry influences decomposition through activity of specific microbial functional guilds. Ecol Monogr 88:429–444

    Article  Google Scholar 

  • Bianchi TS (2011) The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. Proc Natl Acad Sci 108:19473–19481

    Article  Google Scholar 

  • Billings SA, Ziegler SE (2008) Altered patterns of soil carbon substrate usage and heterotrophic respiration in a pine forest with elevated CO2 and N fertilization. Glob Chang Biol 14:1025–1036

    Article  Google Scholar 

  • Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278

    Article  Google Scholar 

  • Bowden RD, Steudler PA, Melillo JM, Aber JD (1990) Annual nitrous oxide fluxes from temperate forest soils in the northeastern United States. J Geophys Res 95:13997–14005

    Article  Google Scholar 

  • Bowden RD, Rullo G, Stevens GR, Steudler PA (2000) Soil fluxes of carbon dioxide, nitrous oxide, and methane at a productive temperate deciduous forest. J Environ Qual 29:268–276

    Article  Google Scholar 

  • Bowden RD, Deem L, Plante AF et al (2014) Litter input controls on soil carbon in a temperate deciduous forest. Soil Sci Soc Am J 78:S66–S75

    Article  Google Scholar 

  • Chan ASK, Steudler PA, Bowden RD et al (2005) Consequences of nitrogen fertilization on soil methane consumption in a productive temperate deciduous forest. Biol Fertil Soils 41:182–189

    Article  Google Scholar 

  • Conte P, Spaccini R, Piccolo A (2004) State of the art of CPMAS 13C-NMR spectroscopy applied to natural organic matter. Prog Nucl Magn Reson Spectrosc 44:215–223

    Article  Google Scholar 

  • Crow SE, Lajtha K, Filley TR et al (2009) Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Glob Chang Biol 15:2003–2019

    Article  Google Scholar 

  • Dria KJ, Sachleben JR, Hatcher PG (2002) Solid-state carbon-13 nuclear magnetic resonance of humic acids at high magnetic field strengths. J Environ Qual 31:393–401

    Article  Google Scholar 

  • Du E, deVries W, Galloway JN et al (2014) Changes in wet nitrogen deposition in the United States between 1985 and 2012. Environ Res Lett 9:095004

    Article  Google Scholar 

  • Eswaran H, Vandenberg E, Reich P (1993) Organic-carbon in soils of the world. Soil Sci Soc Am J 57:192–194

    Article  Google Scholar 

  • Feng X, Simpson MJ (2009) Temperature and substrate controls on microbial phospholipid fatty acid composition during incubation of grassland soils contrasting in organic matter quality. Soil Biol Biochem 41:804–812

    Article  Google Scholar 

  • Feng X, Simpson AJ, Schlesinger WH, Simpson MJ (2010) Altered microbial community structure and organic matter composition under elevated CO2 and N fertilization in the duke forest. Glob Chang Biol 16:2104–2116

    Article  Google Scholar 

  • Frey SD, Ollinger S, Nadelhoffer K et al (2014) Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry 121:305–316

    Article  Google Scholar 

  • Frostegård A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  • Gallardo A, Schlesinger WH (1994) Factors limiting microbial biomass in the mineral soil and forest floor of a warm-temperate forest. Soil Biol Biochem 26:1409–1415

    Article  Google Scholar 

  • Gallo ME, Lauber CL, Cabaniss SE et al (2005) Soil organic matter and litter chemistry response to experimental N deposition in northern temperate deciduous forest ecosystems. Glob Chang Biol 11:1514–1521

    Article  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    Article  Google Scholar 

  • Greaver TL, Clark CM, Compton JE et al (2016) Key ecological responses to nitrogen are altered by climate change. Nat Clim Chang 6:836–843

    Article  Google Scholar 

  • Hatton PJ, Kleber M, Zeller B et al (2012) Transfer of litter-derived N to soil mineral-organic associations: evidence from decadal 15N tracer experiments. Org Geochem 42:1489–1501

    Article  Google Scholar 

  • Hedges JI, Blanchette RA, Weliky K, Devol AH (1988) Effects of fungal degradation on the CuO oxidation products of lignin: a controlled laboratory study. Geochim Cosmochim Acta 52:2717–2726

    Article  Google Scholar 

  • Hobbie SE, Eddy WC, Buyarski CR et al (2012) Response of decomposing litter and its microbial community to multiple forms of nitrogen enrichment. Ecol Monogr 82:389–405

    Article  Google Scholar 

  • Janssens IA, Dieleman W, Luyssaert S et al (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322

    Article  Google Scholar 

  • Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162

    Article  Google Scholar 

  • Lamarque J-F (2005) Assessing future nitrogen deposition and carbon cycle feedback using a multimodel approach: analysis of nitrogen deposition. J Geophys Res 110:D19303

    Article  Google Scholar 

  • Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68

    Article  Google Scholar 

  • Li Y, Schichtel BA, Walker JT et al (2016) Increasing importance of deposition of reduced nitrogen in the United States. Proc Natl Acad Sci 113:5874–5879

    Article  Google Scholar 

  • Li XG, Jia B, Lv J et al (2017) Nitrogen fertilization decreases the decomposition of soil organic matter and plant residues in planted soils. Soil Biol Biochem 112:47–55

    Article  Google Scholar 

  • Liu J, Wu N, Wang H et al (2016) Nitrogen addition affects chemical compositions of plant tissues, litter and soil organic matter. Ecology 97:1796–1806

    Article  Google Scholar 

  • Lu M, Zhou X, Luo Y et al (2011) Minor stimulation of soil carbon storage by nitrogen addition: a meta-analysis. Agric Ecosyst Environ 140:234–244

    Article  Google Scholar 

  • Morrison EW, Frey SD, Sadowsky JJ et al (2016) Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest. Fungal Ecol 23:48–57

    Article  Google Scholar 

  • Müller K, Marhan S, Kandeler E, Poll C (2017) Carbon flow from litter through soil microorganisms: from incorporation rates to mean residence times in bacteria and fungi. Soil Biol Biochem 115:187–196

    Article  Google Scholar 

  • NADP (National Atmospheric Deposition Program), University of Wisconsin, Wisconsin State Laboratory of Hygiene, http://nadp.slh.wisc.edu/NADP. Accessed 11 September 2018

  • Otto A, Simpson MJ (2006) Sources and composition of hydrolysable aliphatic lipids and phenols in soils from western Canada. Org Geochem 37:385–407

    Article  Google Scholar 

  • Otto A, Simpson MJ (2007) Analysis of soil organic matter biomarkers by sequential chemical degradation and gas chromatography—mass spectrometry. J Sep Sci 30:272–282

    Article  Google Scholar 

  • Otto A, Shunthirasingham C, Simpson MJ (2005) A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada. Org Geochem 36:425–448

    Article  Google Scholar 

  • Pan Y, Birdsey RA, Fang J et al (2011) A large and persistent carbon sink in the world’s forests. Science 333:988–993

    Article  Google Scholar 

  • Pardo LH, Robin-Abbott MJ, Fenn ME et al (2015) Effects and empirical critical loads of nitrogen for ecoregions of the United States. Ecol Appl 21:129–169

    Google Scholar 

  • Peng Y, Guo D, Yang Y (2017) Global patterns of root dynamics under nitrogen enrichment. Glob Ecol Biogeogr 26:102–114

    Article  Google Scholar 

  • Pisani O, Frey SD, Simpson AJ, Simpson MJ (2015) Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level. Biogeochemistry 123:391–409

    Article  Google Scholar 

  • Preston CM, Trofymow JA, Sayer BG, Niu J (1997) 13C nuclear magnetic resonance spectroscopy with cross-polarization and magic-angle spinning investigation of the proximate-analysis fractions used to assess litter quality in decomposition studies. Can J Bot 75:1601–1613

    Article  Google Scholar 

  • Pries CEH, Castanha C, Porras RC, Torn MS (2017) The whole-soil carbon flux in response to warming. Science 355:1420–1422

    Article  Google Scholar 

  • Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927

    Article  Google Scholar 

  • Schmidt MWI, Knicker H, Hatcher PG, Kögel-Knabner I (1997) Improvement of 13C and 15N CPMAS NMR spectra of bulk soils, particle size fractions and organic material by treatment with 10% hydrofluoric acid. Eur J Soil Sci 48:319–328

    Article  Google Scholar 

  • Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

    Article  Google Scholar 

  • Simpson MJ, Simpson AJ (2012) The chemical ecology of soil organic matter molecular constituents. J Chem Ecol 38:768–784

    Article  Google Scholar 

  • Smania EFA, Delle Monache F, Smania A et al (2003) Antifungal activity of sterols and triterpenes isolated from Ganoderma annulare. Fitoterapia 74:375–377

    Article  Google Scholar 

  • Sollins P, Swanston C, Kleber M et al (2006) Organic C and N stabilization in a forest soil: evidence from sequential density fractionation. Soil Biol Biochem 38:3313–3324

    Article  Google Scholar 

  • Sollins P, Kramer MG, Swanston C et al (2009) Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96:209–231

    Article  Google Scholar 

  • Theuerl S, Dorr N, Guggenberger G et al (2010) Response of recalcitrant soil substances to reduced N deposition in a spruce forest soil: integrating laccase-encoding genes and lignin decomposition. FEMS Microbiol Ecol 73:166–177

    Google Scholar 

  • Thomas DC, Zak DR, Filley TR (2012) Chronic N deposition does not apparently alter the biochemical composition of forest floor and soil organic matter. Soil Biol Biochem 54:7–13

    Article  Google Scholar 

  • Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120

    Article  Google Scholar 

  • Tritton LM, Hornbeck JW (1982) Biomass equations for major tree species of the Northeast. US Department of Agriculture, Forest Service, Northeastern Forest Experiment Station, Upper Darby, PA

    Google Scholar 

  • Vet R, Artz RS, Carou S, Shaw M, Ro CU, Aas W, Baker A, Bowersox VC, Dentener F, Galy-Lacaux C, Hou A, Pienaar JJ, Gillett R, Forti MC, Gromov S, Hara H, Khodzher T, Mahowald NM, Nickovic S, Rao PSP, Reid NW (2014) A global assessment of precipitation chemistry and deposition of sulfur, nitrogen, sea salt, base cations, organic acids, acidity and pH, and phosphorus. Atmos Environ 93:3–100. https://doi.org/10.1016/j.atmosenv.2013.10.060

    Article  Google Scholar 

  • Waldner P, Marchetto A, Thimonier A, Schmitt M, Rogora M, Granke O, Mues V, Hansen K, Pihl Karlsson G, Žlindra D, Clarke N, Verstraeten A, Lazdins A, Schimming C, Iacoban C, Lindroos AJ, Vanguelova E, Benham S, Meesenburg H, Nicolas M, Kowalska A, Apuhtin V, Napa U, Lachmanová Z, Kristoefel F, Bleeker A, Ingerslev M, Vesterdal L, Molina J, Fischer U, Seidling W, Jonard M, O’Dea P, Johnson J, Fischer R, Lorenz M (2014) Detection of temporal trends in atmospheric deposition of inorganic nitrogen and sulphate to forests in Europe. Atmos Environ 95:363–374. https://doi.org/10.1016/j.atmosenv.2014.06.054

    Article  Google Scholar 

  • Wang J-J, Pisani O, Lin LH et al (2017) Long-term litter manipulation alters soil organic matter turnover in a temperate deciduous forest. Sci Total Environ 607–608:865–875

    Article  Google Scholar 

  • Watzinger A (2015) Microbial phospholipid biomarkers and stable isotope methods help reveal soil functions. Soil Biol Biochem 86:98–107

    Article  Google Scholar 

  • Wu NN, Filley TR, Bai E et al (2015) Incipient changes of lignin and substituted fatty acids under N addition in a Chinese forest soil. Org Geochem 79:14–20

    Article  Google Scholar 

  • Xia M, Talhelm AF, Pregitzer KS (2017) Chronic nitrogen deposition influences the chemical dynamics of leaf litter and fine roots during decomposition. Soil Biol Biochem 112:24–34

    Article  Google Scholar 

  • Yue K, Peng Y, Peng C et al (2016) Stimulation of terrestrial ecosystem carbon storage by nitrogen addition: a meta-analysis. Sci Rep 6:19895

    Article  Google Scholar 

  • Zak DR, Freedman ZB, Upchurch RA et al (2017) Anthropogenic N deposition increases soil organic matter accumulation without altering its biochemical composition. Glob Chang Biol 23:933–944

    Article  Google Scholar 

  • Zelles L, Bai QY, Rackwitz R et al (1995) Determination of phospholipid- and lipopolysaccharide-derived fatty acids as an estimate of microbial biomass and community structures in soils. Biol Fertil Soils 19:115–123

    Article  Google Scholar 

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Acknowledgements

This research was supported by the Natural Sciences and Engineering Research Council (NSERC) of Canada via a Discovery Grant (#2015-05760) and a Discovery Accelerator Supplement (#478038-15) to M.J.S. We sincerely thank Lori vandenEnden, Zhangliu Du, Sam Reese, Ivy Ryan, and Allegheny College for field, laboratory, and financial assistance.

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Correspondence to Myrna J. Simpson.

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Wang, JJ., Bowden, R.D., Lajtha, K. et al. Long-term nitrogen addition suppresses microbial degradation, enhances soil carbon storage, and alters the molecular composition of soil organic matter. Biogeochemistry 142, 299–313 (2019). https://doi.org/10.1007/s10533-018-00535-4

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