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Changes to soil organic N dynamics with leguminous woody plant encroachment into grasslands

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Abstract

Encroachment of nitrogen-fixing trees and shrubs into grasslands and savannas is a well-documented land cover change that occurs worldwide. In the Rio Grande Plains region of southern Texas, previous studies have shown woody encroachment by leguminous Prosopis glandulosa (mesquite) trees increases soil C and N, decreases microbial biomass N relative to soil N, and accelerates N mineralization and nitrification. We examined responses of the dominant organic N components in soil (amino acids and amino sugars) and two soil-bound protein-N acquiring enzymes (arylamidase and β-N-acetylglucosaminidase) along a grassland-to-woodland successional chronosequence to determine changes to soil N chemistry and extractability. The proportion of total N held within amino compounds was significantly lower in the woodlands (47 %) relative to the grassland soils (62 %). This increase in non-hydrolysable N was accompanied by increases in plant cell wall derived amino acids (e.g. hydroxyproline, serine) and losses of microbial amino sugars, indicating the woodland organic N pool was altered in composition and potentially in quality, either because it was more structurally protected or difficult to degrade due to polymerization/condensation reactions. Soil carbon-normalized activities of both soil-bound N-acquiring enzymes were significantly higher in woodland soils, consistent with changes in the biochemical composition of organic N. Although soil total N increases following woody encroachment, this additional organic N appears to be less extractable by chemical hydrolysis and thus potentially in more refractory forms, which may limit microbial N accessibility, slow the cycling of soil organic carbon, and contribute to observed soil C and N accrual in these systems.

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References

  • Acosta-Martínez V, Tabatabai MA (2000) Arylamidase activity of soils. Soil Sci Soc Am J 64:215–221

    Article  Google Scholar 

  • Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Amelung W (2003) Nitrogen biomarkers and their fate in soil. J Plant Nutr Soil Sci 166:677–686

    Article  Google Scholar 

  • Amelung W, Zhang X, Zech W, Flach KW (1999) Amino sugars in native grassland soils along a climosequence in North America. Soil Sci Soc Am J 63:86–92

    Article  Google Scholar 

  • Amelung W, Miltner A, Zhang X (2001) Fate of microbial residues during litter decomposition as affected by minerals. Soil Sci 166:598–606

    Article  Google Scholar 

  • Amelung W, Zhang X, Flach KW (2006) Amino acids in grassland soils: climatic effects on concentrations and chirality. Geoderma 130:207–217

    Article  Google Scholar 

  • Archer SR (1990) Development and stability of grass/woody mosaics in a subtropical savanna parkland, Texas, U.S.A. J Biogeogr 17:453–462

    Article  Google Scholar 

  • Archer SR (1995) Tree-grass dynamics in a Prosopis-thornscrub savanna parkland: reconstructing the past and predicting the future. Ecoscience 2:83–99

    Google Scholar 

  • Archer SR, Scifres CJ, Bassham CR, Maggio R (1988) Autogenic succession in a subtropical savanna: conversion of grassland to thorn woodland. Ecol Monogr 58:111–127

    Article  Google Scholar 

  • Archer SR, Schimel DS, Holland EA (1995) Mechanisms of shrubland expansion: land use, climate or CO2? Climatic Change 29:91–99

    Article  Google Scholar 

  • Archer SR, Boutton TW, Hibbard KA (2001) Trees in grasslands: biogeochemical consequences of woody plant expansion. In: Schulze E-D, Harrison SP, Heimann M et al (eds) Global biogeochemical cycles in the climate system. Academic Press, San Diego, pp 1–46

    Google Scholar 

  • Boutton TW, Liao JD (2010) Changes in soil nitrogen storage and δ15N with woody plant encroachment in a subtropical savanna parkland landscape. J Geophys Res 115. doi:10.1029/2009JG001184

  • Boutton TW, Archer SR, Midwood AJ, Zitzer SF, Bol R (1998) δ13C values of soil organic carbon and their use in documenting vegetation change in a subtropical savanna ecosystem. Geoderma 82:5–41

    Article  Google Scholar 

  • Boutton TW, Rowe HI, Ariza MC, et al (2008) Mycorrhizal productivity following woody plant invasion of grassland. EOS Trans AGU 89:Abstract B23B-0415

  • Boutton TW, Liao JD, Filley TR, Archer SR (2009) Belowground carbon storage and dynamics accompanying woody plant encroachment in a subtropical savanna. In: Lal R, Follett RF (eds) Soil carbon sequestration and the greenhouse effect. Soil Science Society of America, Madison, pp 181–205

    Google Scholar 

  • Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445

    Article  Google Scholar 

  • Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365

    Article  Google Scholar 

  • Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 49:281–309

    Article  Google Scholar 

  • Creamer CA, Filley TR, Boutton TW, Oleynik S, Kantola IB (2011) Controls on soil carbon accumulation during woody plant encroachment: evidence from physical fractionation, soil respiration, and δ13C of respired CO2. Soil Biol Biochem 43:1678–1687

    Article  Google Scholar 

  • Dauwe B, Middelburg JJ (1998) Amino acids and hexosamines as indicators of organic matter degradation state in North Sea sediments. Limnol Oceangr 43:782–798

    Article  Google Scholar 

  • de Graaff M-A, van Groenigen K-J, Six J, Hungate B, van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Glob Change Biol 12:2077–2091

    Article  Google Scholar 

  • Filley TR, Boutton TW, Liao JD, Jastrow JD, Gamblin DE (2008) Chemical changes to nonaggregated particulate soil organic matter following grassland-to-woodland transition in a subtropical savanna. J Geophys Res. doi:10.1029/2007JG000564

    Google Scholar 

  • Gärdenäs AI, Ågren GI, Bird JA et al (2011) Knowledge gaps in soil carbon and nitrogen interactions—from molecular to global scale. Soil Biol Biochem 43:702–717

    Article  Google Scholar 

  • Glaser B, Turrión M-B, Alef K (2004) Amino sugars and muramic acid—biomarkers for soil microbial community structure analysis. Soil Biol Biochem 36:399–407

    Article  Google Scholar 

  • Grandy A, Sinsabaugh R, Neff J et al (2008) Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91:37–49

    Article  Google Scholar 

  • Grandy AS, Strickland MS, Lauber CL et al (2009) The influence of microbial communities, management, and soil texture on soil organic matter chemistry. Geoderma 150:278–286

    Article  Google Scholar 

  • Hibbard KA, Archer S, Schimel DS, Valentine DW (2001) Biogeochemical changes accompanying woody plant encroachment in a subtropical savanna. Ecology 82:1999–2011

    Article  Google Scholar 

  • Hibbard KA, Schimel DS, Archer SR et al (2003) Grassland to woodland transitions: integrating changes in landscape structure and biogeochemistry. Ecol Appl 13:911–926

    Article  Google Scholar 

  • Holecheck JL, Munshikpu AV, Saiwana L et al (1990) Influence of six shrub diets varying in phenol content on intake and nitrogen retention by goats. Trop Grasslands 24:93–98

    Google Scholar 

  • Hu S, Chapin FS, Firestone MK, Field CB, Chiariello NR (2001) Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409:118–191

    Article  Google Scholar 

  • Johnson DC, Dobberpuhl D, Roberts R, Vandeberg P (1993) Pulsed amperometric detection of carbohydrates, amines and sulfur species in ion chromatography—the current state of research. J Chromatogr 640:79–96

    Article  Google Scholar 

  • Kandeler E, Tscherko D, Bruce KD et al (2000) Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biol Fertility Soils 32:390–400

    Article  Google Scholar 

  • Keil RG, Tsamakis E, Hedges JI (2001) Early diagenesis of particulate amino acids in marine systems. In: Goodfriend GA, Collins MJ, Fogel ML, Macko SA, Wehmiller JF (eds) Perspectives in amino acid and protein geochemistry. Oxford University Press, New York, pp 69–82

    Google Scholar 

  • Kleber M, Sollins P, Sutton R (2007) A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85:9–24

    Article  Google Scholar 

  • Knicker H (2004) Stabilization of N-compounds in soil and organic-matter-rich sediments—what is the difference? Mar Chem 92:167–195

    Article  Google Scholar 

  • Knicker H (2011) Soil organic N—an under-rated player for C sequestration in soils? Soil Biol Biochem 43:1118–1129

    Article  Google Scholar 

  • Knicker H, Hatcher PG (1997) Survival of protein in an organic-rich sediment: possible protection by encapsulation in organic matter. Naturwissenschaften 84:231–234

    Article  Google Scholar 

  • Knicker H, Frund R, Ludemann H-D (1993) The chemical nature of nitrogen in native soil organic matter. Naturwissenschaften 80:219–221

    Article  Google Scholar 

  • Kögel-Knabner I (2006) Chemical structure of organic N and organic P in soil. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer, Berlin, pp 23–48

    Chapter  Google Scholar 

  • Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil 256:41–66

    Article  Google Scholar 

  • Laird DA, Martens DA, Kingery WL (2001) Nature of clay-humic complexes in an agricultural soil. I. Chemical, biochemical, and spectroscopic analyses. Soil Sci Soc Am J 65:1413–1418

    Article  Google Scholar 

  • Laursen AK, Mayer LM, Townsend DW (1996) Lability of proteinaceous material in estuarine seston and subcellular fractions of phytoplankton. Mar Ecol Prog Ser 136:227–234

    Article  Google Scholar 

  • Leinweber P, Schulten H-R (1998) Nonhydrolyzable organic nitrogen in soil size separates from long-term agricultural experiments. Soil Sci Soc Am J 62:383–393

    Article  Google Scholar 

  • Leinweber P, Schulten H (2000) Nonhydrolyzable forms of soil organic nitrogen: extractability and composition. J Plant Nutr Soil Sci 163:433–439

    Article  Google Scholar 

  • Liang C, Zhang X, Rubert KF, Balser TC (2007) Effect of plant materials on microbial transformation of amino sugars in three soil microcosms. Biol Fertility Soils 43:631–639

    Article  Google Scholar 

  • Liao JD, Boutton TW (2008) Soil microbial biomass response to woody plant invasion of grassland. Soil Biol Biochem 40:1207–1216

    Article  Google Scholar 

  • Liao JD, Boutton TW, Jastrow JD (2006) Organic matter turnover in soil physical fractions following woody plant invasion of grassland: evidence from natural 13C and 15N. Soil Biol Biochem 38:3197–3210

    Article  Google Scholar 

  • Liu F, Wu XB, Bai E et al (2010) Spatial scaling of ecosystem C and N in a subtropical savanna landscape. Glob Change Biol 16:2213–2223

    Article  Google Scholar 

  • Luo Y, Su B, Currie WS et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Article  Google Scholar 

  • Lyon CK, Gumbmann MR, Becker R (1988) Value of mesquite leaves as forage. J Sci Food Agric 44:111–117

    Article  Google Scholar 

  • Madany MH, West NE (1983) Livestock grazing-fire regime interactions within montane forests of Zion National Park, Utah. Ecology 64:661–667

    Article  Google Scholar 

  • Martens DA, Loeffelmann KL (2003) Soil amino acid composition quantified by acid hydrolysis and anion chromatography-pulsed amperometry. J Agric Food Chem 51:6521–6529

    Article  Google Scholar 

  • Martens DA, Jaynes DB, Colvin TS et al (2006) Soil organic nitrogen enrichment following soybean in an Iowa corn-soybean rotation. Soil Sci Soc Am J 70:382–392

    Article  Google Scholar 

  • McCulley RL, Archer SR, Boutton TW et al (2004) Soil respiration and nutrient cycling in wooded communities developing in grassland. Ecology 85:2804–2817

    Article  Google Scholar 

  • McFarland J, Ruess R, Kielland K et al (2010) Glycine mineralization in situ closely correlates with soil carbon availability across six North American forest ecosystems. Biogeochemistry 99:175–191

    Article  Google Scholar 

  • McLendon T (1993) Preliminary description of the vegetation of south Texas exclusive of costal saline zones. Texas J Sci 43:13–32

    Google Scholar 

  • Minzemayer FE (1979) Soil survey of Jim Wells County. Texas US Department of Agriculture Soil Conservation Service, Washington

    Google Scholar 

  • Muruganandam S, Israel DW, Robarge WP (2009) Activities of nitrogen-mineralization enzymes associated with soil aggregate size fractions of three tillage systems. Soil Sci Soc Am J 73:751–759

    Article  Google Scholar 

  • Nannipieri P, Paul EA (2009) The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem 41:2357–2369

    Article  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitanse activity by N and P availability. Biogeochemistry 49:175–190

    Article  Google Scholar 

  • Olk DC (2008) Improved analytical techniques for carbohydrates, amino compounds, and phenols: tools for understanding soil processes. Soil Sci Soc Am J 72:1672–1682

    Article  Google Scholar 

  • Olk DC, Cassman KG, Schmidt-Rohr K et al (2006) Chemical stabilization of soil organic nitrogen by phenolic lignin residues in anaerobic agroecosystems. Soil Biol Biochem 38:3303–3312

    Article  Google Scholar 

  • Olk DC, Fortuna A, Honeycutt CW (2008) Using anion chromatography-pulsed amperometry to measure amino compounds in dairy manure-amended soils. Soil Sci Soc Am J 72:1711–1720

    Article  Google Scholar 

  • Olk DC, Anders MM, Filley TR, Isbell C (2009) Crop nitrogen uptake and soil phenols accumulation under continuous rice cropping in Arkansas. Soil Sci Soc Am J 73:952

    Article  Google Scholar 

  • Palm CA, Sanchez PA (1990) Decomposition and nutrient release patterns of the leaves of three tropical legumes. Biotropica 22:330

    Article  Google Scholar 

  • Parham JA, Deng SP (2000) Detection, quantification and characterization of β-glucosaminidase activity in soil. Soil Biol Biochem 32:1183–1190

    Article  Google Scholar 

  • Rillig MC, Caldwell BA, Wösten HAB, Sollins P (2007) Role of proteins in soil carbon and nitrogen storage: controls on persistence. Biogeochemistry 85:25–44

    Article  Google Scholar 

  • Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315

    Article  Google Scholar 

  • Schlesinger WH, Pilmanis AM (1998) Plant–soil interactions in deserts. Biogeochemistry 42:169–187

    Article  Google Scholar 

  • Schlesinger WH, Raikes JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77:364–374

    Article  Google Scholar 

  • Schmidt-Rohr K, Mao J-D, Olk DC (2004) Nitrogen-bonded aromatics in soil organic matter and their implications for a yield decline in intensive rice cropping. Proc Natl Acad Sci USA 101:6351–6354

    Article  Google Scholar 

  • Scifres CJ, Koerth BH (1987) Climate, soils, and vegetation of the La Copita Research Area. Texas Agricultural Experimental Station, MP-1626, College Station, TX

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    Google Scholar 

  • Sinsabaugh RS (1994) Enzymic analysis of microbial pattern and process. Biol Fertility Soils 17:69–74

    Article  Google Scholar 

  • Sinsabaugh RL, Moorhead DL (1994) Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311

    Article  Google Scholar 

  • Sinsabaugh RL, Antibus RK, Linkins AE, McClaugherty CA, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593

    Article  Google Scholar 

  • Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24

    Article  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    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, Swanston C, Kramer M (2007) Stabilization and destabilization of soil organic matter—a new focus. Biogeochemistry 85:1–7

    Article  Google Scholar 

  • Stoker RL (1997) Object-oriented, spatially explicit simulation model of vegetation dynamics in a south Texas savanna. Disseration, Texas A&M Unviersity, College Station, TX, UMI Dissertation Number 9729281

  • Tremblay L, Benner R (2006) Microbial contributions to N-immobilization and organic matter preservation in decaying plant detritus. Geochim Cosmochim Acta 70:133–146

    Article  Google Scholar 

  • Zang X, Brown JC, van Heemst JD et al (2001) Characterization of amino acids and proteinaceous materials using online tetramethylammonium hydroxide (TMAH) thermochemolysis and gas chromatography-mass spectrometry technique. J Anal Appl Pyrol 61:181–193

    Article  Google Scholar 

  • Zeglin LH, Stursova M, Sinsabaugh RL, Collins SL (2007) Microbial responses to nitrogen addition in three contrasting grassland ecosystems. Oecologia 154:349–359

    Article  Google Scholar 

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Acknowledgments

This project was funded by the National Science Foundation Biogeosciences Program (EAR-0525349). We would like to thank Terry Grimard for help with amino acid and amino sugar analyses and Rhonda Graef for assistance with the enzyme assays.

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Authors and Affiliations

  1. Department of Earth and Atmospheric Sciences, Purdue University, West Lafayette, IN, 47907, USA

    Courtney A. Creamer, Timothy R. Filley & Valerie Dooling

  2. Purdue Climate Change Research Center, West Lafayette, IN, 47907, USA

    Courtney A. Creamer & Timothy R. Filley

  3. USDA-ARS, National Laboratory for Agriculture and the Environment, Ames, IA, 50011, USA

    Dan C. Olk

  4. USDA-ARS, National Soil Erosion Research Laboratory, West Lafayette, IN, 47907, USA

    Diane E. Stott

  5. Department of Ecosystem Science and Management, Texas A&M University, College Station, TX, 77843, USA

    Thomas W. Boutton

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  1. Courtney A. Creamer
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  2. Timothy R. Filley
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Correspondence to Courtney A. Creamer.

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Creamer, C.A., Filley, T.R., Olk, D.C. et al. Changes to soil organic N dynamics with leguminous woody plant encroachment into grasslands. Biogeochemistry 113, 307–321 (2013). https://doi.org/10.1007/s10533-012-9757-5

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