Abstract
Rising temperatures and nitrogen (N) deposition, both aspects of global environmental change, are proposed to alter soil organic matter (SOM) biogeochemistry. For example, increased plant productivity and enhanced microbial decomposition of litter and SOM may reduce soil carbon stocks and fertility. To better understand SOM biogeochemical shifts at the molecular-level, we employed an array of biomarker and nuclear magnetic resonance (NMR) techniques to investigate the composition and degradation of SOM components in the forest floor and mineral soil horizons of warmed (5 °C above average soil temperature) and N fertilized (5 g m−2 year−1 N applied in the growing season) plots from the soil warming × nitrogen addition study at the Harvard Forest, MA, USA. Biomarker analyses indicated increased plant-derived inputs into the forest floor under N fertilization. Soil warming promoted the decomposition of plant-derived aliphatic and cyclic compounds in the forest floor. Cutin degradation was observed in the heated forest floor which also exhibited relatively higher microbial activity. Lignin oxidation was also observed but was most pronounced in the mineral horizon of the heated plots. These results suggest that continued soil warming may promote the degradation of lignin- and cuticle-derived SOM. N fertilization also enhanced lignin oxidation but to a lesser extent likely due to a decline in microbial activity. 1H NMR spectra of the mineral soils revealed enrichment of plant-derived alkyl structures and microbial-derived organic matter with both soil warming and N fertilization. Overall, this study shows that the decomposition and accumulation of molecularly distinct SOM components occurs with soil warming and N amendment and may subsequently alter soil biogeochemical cycling.





References
Baldock JA, Skjemstad JO (2000) Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org Geochem 31:697–710
Baldock JA, Oades JM, Waters AG, Peng X, Vassallo AM, Wilson MA (1992) Aspects of the chemical structure of soil organic materials as revealed by solid-state 13C NMR spectroscopy. Biogeochemistry 16:1–42
Batjes NH (1996) Total carbon and nitrogen in the soils of the world. Eur J Soil Sci 47:151–163
Berg B, Berg MP, Bottner P, Box E, Breymeyer A, de Anta RC, Coûteaux MM, Gallardo A, Escudero A, Kratz W, Madeira M, Mälkönen E, Meentemeyer V, Munoz F, Piussi P, Remacle J, de Santo AV (1993) Litter mass loss rates in pine forests of Europe and Eastern United States: some relationships with climate and litter quality. Biogeochemistry 20:127–159
Clemente JS, Gregorich EG, Simpson AJ, Kumar R, Courtier-Murias D, Simpson MJ (2012) Comparison of nuclear magnetic resonance methods for the analysis of organic matter composition from soil density and particle fractions. Environ Chem 9:97–107
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
Contosta AR, Frey SD, Cooper AB (2011) Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils. Ecosphere 2(3):1–21 (article 36)
Cramer W, Bondeau A, Woodward FI, Prentice IC, Betts RA, Brovkin V, Cox PM, Fisher V, Foley JA, Friend AD, Kucharik C, Lomas MR, Ramankutty N, Sitch S, Smith B, White A, Young-Molling C (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate changes: results from six dynamic global vegetation models. Glob Change Biol 7:357–373
Crow SE, Lajtha K, Bowden RD, Yano Y, Brant JB, Caldwell BA, Sulzman EW (2009) Increased coniferous needle inputs accelerate decomposition of soil carbon in an old-growth forest. For Ecol Manag 258:2224–2232
Currie WS, Aber JD, McDowell WH, Boone RD, Magill AH (1996) Vertical transport of dissolved organic C and N under long-term N amendments in pine and hardwood forests. Biogeochemistry 35:471–505
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173
Deshmukh AP, Simpson AJ, Hatcher PG (2003) Evidence for cross-linking in tomato cutin using HR-MAS NMR spectroscopy. Phytochemistry 64:1163–1170
Deshmukh AP, Pacheco C, Hay MB, Myneni SCB (2007) Structural environments of carboxyl groups in natural organic molecules from terrestrial systems. Part 2: 2D NMR spectroscopy. Geochim Cosmochim Acta 71:3533–3544
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
Feng X, Simpson MJ (2011) Molecular-level methods for monitoring soil organic matter responses to global climate change. J Environ Monit 13:1246–1254
Feng X, Simpson AJ, Wilson KP, Williams DD, Simpson MJ (2008) Increased cuticular carbon sequestration and lignin oxidation in response to soil warming. Nat Geosci 1:836–839
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 Change Biol 16:2104–2116
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171
Frey SD, Drijber R, Smith H, Melillo J (2008) Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol Biochem 40:2904–2907
Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Change 3:395–398
Frey SD, Ollinger S, Nadelhoffer K, Bowden R, Brzostek E, Burton A, Caldwell BA, Crow S, Goodale CL, Grandy AS, Finzi A, Kramer MG, Lajtha K, LeMoine J, Martin M, McDowell WH, Minocha R, Sadowsky JJ, Templer PH, Wickings K (2014) Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry 121(2):305–316
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
Galloway JN, Dentener FJ, Boyer EW, Capone DG, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vörösmarty CJ (2004) Nitrogen cycles: past, present and future. Biogeochemistry 70:153–226
Garcia-Pausas J, Paterson E (2011) Microbial community abundance and structure are determinants of soil organic matter mineralisation in the presence of labile carbon. Soil Biol Biochem 43:1705–1713
Goñi MA, Hedges JI (1990a) Cutin-derived CuO reaction products from purified cuticles and tree leaves. Geochim Cosmochim Acta 54:3065–3072
Goñi MA, Hedges JI (1990b) The diagenetic behavior of cutin acids in buried conifer needles and sediments from a coastal marine environment. Geochim Cosmochim Acta 54:3083–3093
Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307
Guckert JB, Antworth CP, Nichols PD, White DC (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Lett 31:147–159
Hedges JI, Mann DC (1979) The characterization of plant tissues by their lignin oxidation products. Geochim Cosmochim Acta 43:1803–1807
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
IPCC (2007) Climate change 2007: synthesis report. An assessment of the intergovernmental panel on climate change. Intergovernmental Panel on Climate Change (IPCC), Valencia, Spain
Kelleher BP, Simpson AJ (2006) Humic substances in soils: are they really chemically distinct? Environ Sci Technol 40:4605–4611
Kiem R, Kögel-Knabner I (2003) Contribution of lignin and polysaccharides to the refractory carbon pool in C-depleted arable soils. Soil Biol Biochem 35:101–118
Kindler R, Miltner A, Thullner M, Richnow HH, Kästner M (2009) Fate of bacterial biomass derived fatty acids in soil and their contribution to soil organic matter. Org Geochem 40:29–37
Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257
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
Kögel-Knabner I, Ekschmitt K, Flessa H, Guggenberger G, Matzner E, Marschner B, von Lützow M (2008) An integrative approach of organic matter stabilization in temperate soils: linking chemistry, physics and biology. J Plant Nutr Soil Sci 171:5–13
Koide RT, Shumway DL, Stevens CM (2000) Soluble carbohydrates of red pine (Pinus resinosa) mycorrhizas and mycorrhizal fungi. Mycol Res 104:834–840
Kolattukudy PE (1980) Biopolyester membranes of plants: cutin and suberin. Science 208:990–1000
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498
Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627
Lam TBT, Kadoya K, Iiyama K (2001) Bonding of hydroxycinnamic acids to lignin: ferulic and p-coumaric acids are predominantly linked at the benzyl position of lignin, not the β-position, in grass cell walls. Phytochemistry 57:987–992
Liang C, Cheng G, Wixon DL, Balser TC (2011) An absorbing Markov chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry 106:303–309
Lichtfouse E, Berthier G, Houot S, Barriuso E, Bergheaud V, Vallaeys T (1995) Stable carbon isotope evidence for the microbial origin of C14–C18 n-alkanoic acids in soils. Org Geochem 23:849–852
Liu C, Westman CJ, Berg B, Kutsch W, Wang GZ, Man R, Ilvesniemi H (2004) Variation in litterfall–climate relationships between coniferous and broadleaf forests in Eurasia. Global Ecol Biogeogr 13:105–114
Lorenz K, Lal R, Preston CM, Nierop KGJ (2007) Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules. Geoderma 142:1–10
Mackenzie AS, Brassell SC, Eglinton G, Maxwell JR (1982) Chemical fossils: the geological fate of steroids. Science 217:491–504
Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morrisseau S (2002) Soil warming and carbon-cycle feedbacks to the climate system. Science 298:2173–2176
Melillo JM, Butler S, Johnson J, Mohan J, Steudler P, Lux H, Burrows E, Bowles F, Smith R, Scott L, Vario C, Hill T, Burton A, Zhou YM, Tang J (2011) Soil warming, carbon-nitrogen interactions, and forest carbon budgets. Proc Natl Acad Sci 108:9508–9512
Miltner A, Kindler R, Knicker H, Richnow HH, Kästner M (2009) Fate of microbial biomass-derived amino acids in soil and their contribution to soil organic matter. Org Geochem 40:978–985
Munger JW, Fan SM, Bakum PS, Goulden ML, Goldstein AH, Coleman AS, Wofsy SC (1998) Regional budgets for nitrogen oxides from continental sources: variations of rates for oxidation and deposition with season and distance from source regions. J Geophys Res 103:8355–8368
Nierop KGJ (1998) Origin of aliphatic compounds in a forest soil. Org Geochem 29:1009–1016
Otto A, Simpson MJ (2005) Degradation and preservation of vascular plant-derived biomarkers in grassland and forest soils from Western Canada. Biogeochemistry 74:377–409
Otto A, Simpson MJ (2006a) Sources and composition of hydrolysable aliphatic lipids and phenols in soils from western Canada. Org Geochem 37:385–407
Otto A, Simpson MJ (2006b) Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochemistry 80:121–142
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
Pautler BG, Simpson AJ, McNally DJ, Lamoureux SF, Simpson MJ (2010) Arctic permafrost active layer detachments stimulate microbial activity and degradation of soil organic matter. Environ Sci Technol 44:4076–4082
Pautler BG, Dubnick A, Sharp MJ, Simpson AJ, Simpson MJ (2013) Comparison of cryoconite organic matter composition from Arctic and Antarctic glaciers at the molecular-level. Geochim Cosmochim Acta 104:1–18
Peterjohn WT, Mellor JM, Steudler PA, Newkirk KM, Bowles FP, Aber JD (1994) Responses of traces gas fluxes and N availability to experimentally elevated soil temperatures. Ecol Appl 4:617–625
Pinder RW, Bettez ND, Bonan GB, Greaver TL, Wieder WR, Schlesinger WH, Davidson EA (2012) Impacts of human alteration of the nitrogen cycle in the US on radiative forcing. Biogeochemistry 114:25–40
Pisani O, Hills KM, Courtier-Murias D, Simpson AJ, Mellor NJ, Paul EA, Morris SJ, Simpson MJ (2013) Molecular level analysis of longterm vegetative shifts and relationships to soil organic matter composition. Org Geochem 62:7–16
Pisani O, Hills KM, Courtier-Murias D, Haddix ML, Paul EA, Conant RT, Simpson AJ, Arhonditsis GB, Simpson MJ (2014) Accumulation of aliphatic compounds in soil with increasing mean annual temperature. Org Geochem 76:118–127
Reinsch S, Ambus P, Paterson E, Thornton B (2013) Impact of future climatic conditions on the potential for soil organic matter priming. Soil Biol Biochem 65:133–140
Riederer M, Matzke Z, Ziegler F, Kögel-Knabner I (1993) Occurrence, distribution and fate of the lipid plant biopolymers cutin and suberin in temperate forest soils. Org Geochem 20:1063–1076
Rumpel C, Rabia N, Derenne S, Quenea K, Eusterhues K, Kögel-Knabner I, Mariotti A (2006) Alteration of soil organic matter following treatment with hydrofluoric acid (HF). Org Geochem 37:1437–1451
Savage KE, Parton WJ, Davidson EA, Trumbore SE, Frey SD (2013) Long-term changes in forest carbon under temperature and nitrogen amendments in a temperate northern hardwood forest. Glob Change Biol 19:2389–2400
Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol. doi:10.3389/fmicb.2012.00348
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
Schmidt MWI, Knicker H, Hatcher PG, Kögel-Knabner I (1997) Improvement of C-13 and N-15 CPMAS NMR spectra of bulk soils, particle size fractions and organic material by treatment with 10% hydrofluoric acid. Europ J Soil Sci 48:319–325
Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56
Schulten HR, Schnitzer M (1990) Aliphatics in soil organic matter in fine-clay fractions. Soil Sci Soc Am J 54:98–105
Shaver GR, Canadell J, Chapin FS, Gurevitch J, Harte J, Henry G, Ineson P, Jonasson S, Melillo J, Pitelka L, Rustad L (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. BioScience 50:871–882
Simoneit BRT (2005) A review of current applications of mass spectrometry for biomarker/molecular tracer elucidations. Mass Spectrom Rev 24:719–765
Simoneit BRT, Elias VO, Kobayashi M, Kawamura K, Rushdi AI, Medeiros PM, Rogge WF, Didyk BM (2004) Sugars–dominant water-soluble organic compounds in soils and characterization as tracers in atmospheric particulate matter. Environ Sci Technol 38:5939–5949
Simpson MJ, Simpson AJ (2012) The chemical ecology of soil organic matter molecular constituents. J Chem Ecol 38:768–784
Simpson AJ, Burdon J, Graham CL, Hayes MHB, Spencer N, Kingery WL (2001) Interpretation of heteronuclear and multidimensional NMR spectroscopy of humic substances. Eur J Soil Sci 52:495–509
Simpson AJ, Lefebvre B, Moser A, Williams A, Larin N, Kvasha M, Kingery WL, Kelleher B (2004) Identifying residues in natural organic matter through spectral prediction and pattern matching of 2D NMR datasets. Magn Reson Chem 42:14–22
Simpson AJ, Song G, Smith E, Lam B, Novotny EH, Hayes MHB (2007) Unraveling the structural components of soil humin by use of solution-state nuclear magnetic resonance spectroscopy. Environ Sci Technol 41:876–883
Simpson MJ, Otto A, Feng X (2008) Comparison of solid-state carbon-13 nuclear magnetic resonance and organic matter biomarkers for assessing soil organic matter degradation. Soil Sci Soc Am J 72:268–276
Simpson AJ, McNally DJ, Simpson MJ (2011) NMR spectroscopy in environmental research: from molecular interactions to global processes. Prog Nucl Magn Reson Spectrosc 58:97–175
Simpson AJ, Simpson MJ, Soong R (2012) Nuclear magnetic resonance spectroscopy and its key role in environmental research. Environ Sci Technol 46:11488–11496
Thenot JP, Horning EC, Stafford M, Horning MG (1972) Fatty acid esterification with N, N-Dimethylformamide dialkyl acetals for GC analysis. Anal Lett 5:217–223
Treonis AM, Ostle NJ, Stott AW, Primrose R, Grayston SJ, Ineson P (2004) Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs. Soil Biol Biochem 36:533–537
Trumbore SE, Czimczik CI (2008) An uncertain future for soil carbon. Science 321:1455–1456
Vitousek PM, Hättenschwiler S, Olander L, Allison S (2002) Nitrogen and nature. Ambio 31:97–101
von Lützow M, Kögel-Knabner I, Ekschitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur J Soil Sci 57:426–445
Woods GC, Simpson MJ, Koerner PJ, Napoli A, Simpson AJ (2011) HILIC-NMR: toward the identification of individual molecular components in dissolved organic matter. Environ Sci Technol 45:3880–3886
Zhang D, Hui D, Luo Y, Zhou G (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:1–9
Acknowledgments
We thank two anonymous reviewers and the Associate Editor (Prof. Sharon Billings) for their helpful feedback on earlier versions of this manuscript. We also thank Melissa Knorr for sample collection and Jonathan Chio for assistance with the PLFA analysis. The Natural Sciences and Engineering Research Council (NSERC) of Canada is thanked for support via a Discovery Grant and a Discovery Accelerator Grant to M.J.S. Installation and maintenance of the Soil Warming × Nitrogen Addition Study at Harvard Forest was supported by a NSF Faculty Early Career Development Award to S.D.F. and the NSF Long-term Ecological Research (LTER) Program.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Sharon A. Billings.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pisani, O., Frey, S.D., Simpson, A.J. et al. Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level. Biogeochemistry 123, 391–409 (2015). https://doi.org/10.1007/s10533-015-0073-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-015-0073-8