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Nitrogen alters microbial enzyme dynamics but not lignin chemistry during maize decomposition

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Abstract

Increases in nitrogen (N) availability reduce decay rates of highly lignified plant litter. Although microbial responses to N addition are well documented, the chemical mechanisms that may give rise to this inhibitory effect remain unclear. Here, we ask: Why does increased N availability inhibit lignin decomposition? We hypothesized that either (1) decomposers degrade lignin to obtain N and stop producing lignin-degrading enzymes if mineral N is available, or (2) chemical reactions between lignin and mineral N decrease the quality of lignin and limit the ability of decomposers to break it down. In order to test these hypotheses, we tracked changes in carbon (C) mineralization, microbial biomass and enzyme activities, litter chemistry, and lignin monomer concentrations over a 478-day laboratory incubation of three maize genotypes differing in lignin quality and quantity (F292bm3 (high lignin) < F2 (medium lignin) < F2bm1 (low lignin)). Maize stem internodes of each genotype were mixed with either an acidic or neutral pH sandy soil, both with and without added N. Nitrogen addition reduced C mineralization, microbial biomass, and lignin-degrading enzyme activities across most treatments. These dynamics may be due to suppressed fungal growth and reduced microbial acquisition of lignin-shielded proteins in soils receiving N. However, N addition alone did not significantly alter the quantity or quality of lignin monomers in any treatment. Our results suggest that abiotic interactions between N and phenolic compounds did not influence lignin chemistry, but mineral N does alter microbial enzyme and biomass dynamics, with potential longer-term effects on soil C dynamics.

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References

  • Amin BAZ, Chabbert B, Moorhead D, Bertrand I (2014) Impact of fine litter chemistry on lignocellulolytic enzyme efficiency during decomposition of maize leaf and root in soil. Biogeochemistry 117:169–183

    Article  Google Scholar 

  • Bahri H, Dignac MF, Rumpel C, Rasse DP, Chenu C, Mariotti A (2006) Liginin turnover kinetics in an agricultural soil is monomer specific. Soil Biol Biochem 38:1977–1988

    Article  Google Scholar 

  • Barriere Y, Ralph J, Mechin V, Guillaumie S, Grabber JH, Argillier O, Chabbert B, Lapierre C (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability: II. Lessons from brown-rib mutants. Compte R Biol 327:847–860

    Article  Google Scholar 

  • Berg B (2000) Litter decomposition and organic matter turnover in northern forest soils. For Ecol Manag 133:13–22

    Article  Google Scholar 

  • Bertrand I, Chabbert B, Kurek B (2006) Can the biochemical features and histology of wheat residues explain their decomposition in soil? Plant Soil 281:291–307

    Article  Google Scholar 

  • Blakeney AP, Harris PJ, Henry RJ, Stone BA (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr Res 113:291–299

    Article  Google Scholar 

  • Bowden RD, Davidson E, Savage K, Arabia C, Steudler P (2004) Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. For Ecol Manag 196:43–56

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  Google Scholar 

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chen C (1992) Nitrobenzene and cupric oxide oxidations. In: Lin SY, Dence CW (eds) Methods in lignin chemistry. Springer, New York, pp 301–321

    Chapter  Google Scholar 

  • Chen R, Senbayram M, Blagodatsky S, Myachina O, Dittert K, Xiangui L, Blagodatskaya E, Kuzyakov Y (2013) Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Change Biol 20:2356–2367

    Article  Google Scholar 

  • Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial-efficiency matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable organic matter? Glob Change Biol 19:988–995

    Article  Google Scholar 

  • Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113

    Article  Google Scholar 

  • Dashtban N, Schraft H, Syed TA, Qin W (2010) Fungal biodegradation and enzymatic modification of lignin. Int J Biochem Mol Biol 1:36–50

    Google Scholar 

  • Entry JA (2000) Influence of nitrogen on cellulose and lignin mineralization in blackwater and redwater forested wetland soils. Biol Fertil Soil 31:436–440

    Article  Google Scholar 

  • Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017

    Article  Google Scholar 

  • Floch C, Alarcon-Gutierrez E, Criquet S (2007) ABTS assay of phenol oxidase activity in soil. J Microbiol Methods 71:319–324

    Article  Google Scholar 

  • Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev Camb Philos Soc 63:433–462

    Article  Google Scholar 

  • Freedman Z, Zak DR (2014) Atmospheric N deposition increases bacterial laccase-like multicopper oxidases: implications for organic matter decay. Appl Environ Microbiol 80:4460–4468

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Frey SD, Ollinger S, Nadelhoffer K, Bowden R, Brzostek E, Burton A, Caldwell A, 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. Biogeochem Lett 121:305–316

    Article  Google Scholar 

  • Gallo M, Amonette R, Lauber C, Sinsabaugh RL, Zak DR (2004) Microbial community structure and oxidative enzyme activity in nitrogen-amended north temperate forest soils. Microb Ecol 48:218–229

    Article  Google Scholar 

  • Gallo M, Lauber C, Cabaniss SE, Waldrop MP, Sinsabaugh RL, Zak DR (2005) Soil organic matter and litter chemistry response to experimental nitrogen addition in northern temperate forest deciduous ecosystems. Glob Change Biol 11:1514–1521

    Article  Google Scholar 

  • German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    Article  Google Scholar 

  • Glanville H, Rousk J, Golyshin P, Jones DL (2012) Mineralization of low molecular weight carbon substrates in soil solution under laboratory and field conditions. Soil Biol Biochem 48:88–95

    Article  Google Scholar 

  • Goering HK, Van Soest PG (1970) Forage fiber analysis (apparatus, reagents, procedures and some applications). USDA Agricultural Handbook No. 379, Washington, DC

    Google Scholar 

  • Grandy AS, Neff JC (2008) Molecular soil C dynamics downstream: the biochemical decomposition sequence and its effects on soil organic matter structure and function. Sci Total Environ 404:297–303

    Article  Google Scholar 

  • Grandy AS, Sinsabaugh RL, Neff JC, Stursova M, Zak DR (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 

  • Hedges JI, Ertel JR (1982) Characterization of lignin by gas capillary chromatography of cupric oxide oxidation products. Anal Chem 54:174–178

    Article  Google Scholar 

  • Hobbie SE, Eddie WC, Buyarski CR, Adair EC, Ogdahl ML, Weisenhorn P (2012) Response of decomposing litter and its microbial community to multiple forms of nitrogen enrichment. Ecol Monogr 82:389–405

    Article  Google Scholar 

  • Hodge JE (1953) Chemistry of browning reactions in model systems. J Agric Food Chem 1:928–943

    Article  Google Scholar 

  • Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991

    Article  Google Scholar 

  • Keyser P, Kirk TK, Zeikus JG (1976) Lignolytic enzyme system of Phanerochaete chrysosporium: synthesized in the absence of lignin in response to nitrogen starvation. J Bacteriol 135:790–797

    Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    Article  Google Scholar 

  • Kirk TK, Connors WJ, Zeikus JG (1976) Requirement for a growth substrate during lignin decomposition by two wood-rotting fungi. Appl Environ Microbiol 32:192–194

    Google Scholar 

  • Klotzbücher T, Filley TR, Kaiser K, Kalbitz K (2011) A study of lignin degradation in leaf and needle litter using 13C-labelled tetramethylammonium hydroxide (TMAH) thermochemolysis: comparison with CuO oxidation and van Soest methods. Org Geochem 42:1271–1278

    Article  Google Scholar 

  • Kogel I (1986) Estimation and decomposition pattern of the lignin component in forest humus layers. Microb Ecol 18:589–594

    Google Scholar 

  • Machinet GE, Bertrand I, Chabbert B, Recous S (2009) Decomposition in soil and chemical changes of maize roots with genetic variations affecting cell wall quality. Eur J Soil Sci 60:176–185

    Article  Google Scholar 

  • Machinet GE, Bertrand I, Chabbert B (2011) Assessment of lignin-related compounds in soils and maize roots by alkaline oxidations and thioacidolysis. Soil Sci Soc Am J 75:542–552

    Article  Google Scholar 

  • Monties B (1984) Dosage de la lignine insoluble en milieu acide: influence du pretraitement par hydrolyse acide sur la lignine klason de bois et pialle. Agronomie 4:387–392

    Article  Google Scholar 

  • Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174

    Article  Google Scholar 

  • Moorhead DL, Lashermes G, Sinsabaugh RL, Weintraub MN (2013a) Calculating co-metabolic costs of lignin decay and their impacts on carbon use efficiency. Soil Biol Biochem 66:17–19

    Article  Google Scholar 

  • Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013b) Dynamic relationships between microbial biomass, respiration, inorganic nutrients, and enzyme activities: informing enzyme-based decomposition models. Front Microbiol 4:233. doi:10.3389/fmicb.2013.00223

    Article  Google Scholar 

  • Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, Bowman WD (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–917

    Article  Google Scholar 

  • Ochoa-Hueso R, Maestre FT, de Los RA, Valea S, Theobald MR, Vivanco MG, Manrique E, Bowker MA (2013) Nitrogen deposition alters nitrogen cycling and reduces soil carbon content in low-productivity semiarid Mediterranean systems. Envrion Pollut 179:185–193

    Article  Google Scholar 

  • Otto A, Simpson MJ (2006) Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochemistry 80:121–142

    Article  Google Scholar 

  • Ramirez KS, Craine JM, Fierer N (2010) Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied. Soil Biol Biochem 42:2336–2338

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Recous S, Robin D, Darwis D, Mary B (1995) Soil inorganic N availability: effect on maize residue decomposition. Soil Biol Biochem 12:1529–1538

    Article  Google Scholar 

  • Rinkes ZL, Weintraub MN, DeForest JL, Moorhead DL (2011) Microbial substrate preference and community dynamics during the decomposition of Acer saccharum. Fungal Ecol 4:396–407

    Article  Google Scholar 

  • Rinkes ZL, Sinsabaugh RL, Moorhead DL, Grandy AS, Weintraub MN (2013) Field and lab conditions alter microbial enzyme and biomass dynamics driving decomposition of the same leaf litter. Front Microbiol 4:260. doi:10.3389/fmicb.2013.00260

    Article  Google Scholar 

  • Rinkes ZL, DeForest JL, Grandy AS, Moorhead DL, Weintraub MN (2014) Interactions between leaf litter quality, particle size, and microbial community during the earliest stage of decay. Biogeochemistry 117:153–168

    Article  Google Scholar 

  • Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggests functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596

    Article  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    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 

  • Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563

    Article  Google Scholar 

  • Schulze W (2004) Environmental proteomics—what proteins from soil and surface water can tell us: a perspective. Biogeosci Discuss 1:195–218

    Article  Google Scholar 

  • Scott-Denton LE, Rosensteil TN, Monson RK (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Change Biol 12:205–216

    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 

  • Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569

    Article  Google Scholar 

  • Snyder JD, Trofymow JA (1984) A rapid accurate wet oxidation diffusion procedure for determining organic and inorganic carbon in plants and soil. Commun Soil Sci Plant Anal 15:587–597

    Article  Google Scholar 

  • Soderstrom B, Baath E, Lundgren B (1983) Decrease in soil microbial activity and biomasses owing to nitrogen amendments. Can J Microbiol 29:1500–1506

    Article  Google Scholar 

  • Stevenson FJ (1982) Humus chemistry. Genesis, composition, reactions. Wiley, New York

    Google Scholar 

  • Stewart CE, Moturi P, Follett RF, Halvorson AD (2015) Lignin biochemistry and soil N determine crop residue decomposition and soil priming. Biogeochemistry 124:335–351

    Article  Google Scholar 

  • Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395

    Article  Google Scholar 

  • Sugai SF, Schimel JP (2003) Decomposition and biomass incorporation of 14C-labeled glucose and phenolics in a taiga forest floor: effect of substrate quality, successional state, and season. Soil Biol Biochem 25:1379–1385

    Article  Google Scholar 

  • Talbot JM, Yelle DJ, Nowick J, Treseder KK (2012) Litter decay rates are determined by lignin chemistry. Biogeochemistry 108:279–295

    Article  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 (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:34–355

    Google Scholar 

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

    Article  Google Scholar 

  • Tu L, Hu H, Chen G, Peng Y, Xiao Y, Hu T, Zhang J, Li X, Liu L, Tang Y (2014) Nitrogen additions significantly affects forest litter decomposition under high levels of ambient nitrogen deposition. PLoS One. doi:10.1371/journal.pone.0088752

    Google Scholar 

  • Waldrop MP, Zak DR (2006) Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems 9:921–933

    Article  Google Scholar 

  • Waldrop MP, Zak DR, Sinsabaugh RL (2004) Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biol Biochem 36:1443–1451

    Article  Google Scholar 

  • Wallenstein MD, McNulty S, Fernandez IJ, Boggs J, Schlesinger WH (2006) Nitrogen fertilization decreases forest fungal and bacterial biomass in three long-term experiments. For Ecol Manag 222:459–468

    Article  Google Scholar 

  • Wang WJ, Baldock JA, Dalal RC, Moody PW (2004) Decomposition dynamics of plant materials in relation to nitrogen availability and biochemistry determined by NMR and wet-chemical analysis. Soil Biol Biochem 36:2045–2058

    Article  Google Scholar 

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Acknowledgments

This research was supported by an NSF Ecosystems Program Grant (# 0918718) to MNW and ASG and the NSF Research Coordination Network on Enzymes in the Environment Grant (# 0840869). For field and laboratory assistance, we thank Bethany Chidester, Dashanne Czegledy, Michael Elk, Mallory Ladd, Ryan Monnin, Steve Solomon, Heather Thoman, Logan Thornsberry, Eric Wellman, Travis White, and Megan Wenzel. We also thank three anonymous reviewers whose suggestions greatly improved this work.

Author contributions

MNW and IB conceived the project. Microbial analyses were conducted by ZLR. CuO analyses were performed by BZA and IB. ASG and KW provided the py-GCMS data. ZLR and BZA analyzed the data. ZLR wrote the article with input from the other authors.

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Author notes

  1. Isabelle Bertrand

    Present address: INRA UMR Eco&Sols, place P Viala, 34060, Montpellier, France

  2. Bilal Ahmad Zafar Amin

    Present address: Department of Environmental Sciences, COMSATS, CIIT, Abbottabad, Pakistan

Authors and Affiliations

  1. Department of Environmental Sciences, University of Toledo, Toledo, OH, 43606, USA

    Zachary L. Rinkes & Michael N. Weintraub

  2. INRA, UMR614 FARE, esplanade Roland Garros, 51100, Reims, France

    Isabelle Bertrand & Bilal Ahmad Zafar Amin

  3. Department of Natural Resources and the Environment, University of New Hampshire, Durham, NH, 03824, USA

    A. Stuart Grandy

  4. Department of Entomology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY, 14456, USA

    Kyle Wickings

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  1. Zachary L. Rinkes
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Correspondence to Zachary L. Rinkes.

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Responsible Editor: Susan E. Crow.

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Supplementary Fig. 1

Microbial biomass-C (MB-C) for all genotypes in both soil types (acidic and neutral pH) with and without added N after day 0. Values represent the mean ± SE for each treatment over the final 9 incubation harvests (n = 36). Units are mg-C g dry litter−1. Significant nitrogen (N− > N+) and pH (neutral > acidic) effects predominated between days 27–478. Supplementary material 1 (TIFF 328 kb)

Supplementary Fig. 2

Cn/V ratio on days 120 and 478 during a laboratory incubation of low (A), medium (B), and high (C) lignin maize genotypes. Each genotype was mixed with either an acidic or neutral pH sandy soil, both with and without added N. Nitrogen addition had no significant effect on Cn/V ratios. Supplementary material 2 (TIFF 486 kb)

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Rinkes, Z.L., Bertrand, I., Amin, B.A.Z. et al. Nitrogen alters microbial enzyme dynamics but not lignin chemistry during maize decomposition. Biogeochemistry 128, 171–186 (2016). https://doi.org/10.1007/s10533-016-0201-0

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