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Eco-enzymatic stoichiometry and enzymatic vectors reveal differential C, N, P dynamics in decaying litter along a land-use gradient

Biogeochemistry volume 129, pages 21–36 (2016)Cite this article

Abstract

To evaluate carbon (C), nitrogen (N), and phosphorus (P) dynamics during the decomposition process, we investigated the temporal variability of extracellular enzymatic activities (EEA) associated with C, N, and P acquisition in microbial communities from different land uses. We hypothesized that EEA ratios would reveal different primary resource requirements with respect to microbial demand, depending on soil properties, litter type and the relative proportion of bacteria:fungi in the microbial community. To test this hypothesis, we implemented an experiment using four litters (Triticum aestivum, Fagus sylvatica, Festuca arundinacea and Robinia pseudoacacia) in four soils (cropland, plantation, prairie and forest) located in close proximity to one another on the same parent material. Analyses of EEA showed that overall N requirement increased relative to P during litter decay, but C requirement increased more rapidly than either N or P in most of these ecosystems. Soil type was the main factor controlling N versus P requirement whereas litter type was the primary driver of C versus nutrient requirement. Shifts in EEA were related to changes in metabolic quotient (C respired per unit biomass) but there was no evidence that the relative proportion of fungi:bacteria drove changes in EEA. We concluded that the use of EEA as a proxy of microbial resource demand improved our understanding of temporal shifts in resource requirements to microbial communities, their associated respiration efficiency and dynamics of C and nutrients among different ecosystems.

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References

  • Allison SD (2012) A trait-based approach for modelling microbial litter decomposition. Ecol Lett 15:1058–1070

    Article  Google Scholar 

  • 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 

  • Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp. doi:10.3791/50961

    Google Scholar 

  • Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD (2014) Rhizosphere stoichiometry: are C:N:P ratios of plants, soils, and enzymes conserved at the plant species-level? New Phytol 201:505–517

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson D (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 

  • Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Article  Google Scholar 

  • Cleveland CC, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante M, Chuyong G, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:939–947

    Article  Google Scholar 

  • Elser J, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J (2003) Growth rate–stoichiometry couplings in diverse biota. Ecol Lett 6:936–943

    Article  Google Scholar 

  • Fanin N, Bertrand I (2016) Aboveground litter quality is a better predictor than belowground microbial communities when estimating carbon mineralization along a land-use gradient. Soil Biol Biochem 94:48–60

    Article  Google Scholar 

  • Fanin N, Barantal S, Fromin N, Schimann H, Schevin P, Hättenschwiler S (2012) Distinct microbial limitations in litter and underlying soil revealed by carbon and nutrient fertilization in a tropical rainforest. PLoS One 7:e49990

    Article  Google Scholar 

  • Fanin N, Fromin N, Buatois B, Hättenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter–microbe system. Ecol Lett 16:764–772

    Article  Google Scholar 

  • Fanin N, Hättenschwiler S, Fromin N (2014) Litter fingerprint on microbial biomass, activity, and community structure in the underlying soil. Plant Soil 379:79–91

    Article  Google Scholar 

  • Fanin N, Hättenschwiler S, Schimann H, Fromin N (2015) Interactive effects of C, N and P fertilization on soil microbial community structure and function in an Amazonian rain forest. Funct Ecol 29:140–150

    Article  Google Scholar 

  • Goering HK, Van Soest PJ (1970) Forage fiber analyses (apparatus, reagents, procedures, and some applications). USDA Agr Handb

  • Güsewell S, Gessner MO (2009) N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219

    Article  Google Scholar 

  • Jangid K, Williams MA, Franzluebbers AJ, Sanderlin JS, Reeves JH, Jenkins MB, Endale DM, Coleman DC, Whitman WB (2008) Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem 40:2843–2853

    Article  Google Scholar 

  • Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7

    Article  Google Scholar 

  • Kaiser C, Franklin O, Dieckmann U, Richter A (2014) Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol Lett 17:680–690

    Article  Google Scholar 

  • Keiblinger KM, Hall EK, Wanek W, Szukics U, Hämmerle I, Ellersdorfer G, Böck S, Strauss J, Sterflinger K, Richter A (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiol Ecol 73:430–440

    Google Scholar 

  • Kuzyakov Y, Friedel J, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498

    Article  Google Scholar 

  • Machinet GE, Bertrand I, Barrière Y, Chabbert B, Recous S (2011) Impact of plant cell wall network on biodegradation in soil: role of lignin composition and phenolic acids in roots from 16 maize genotypes. Soil Biol Biochem 43:1544–1552

    Article  Google Scholar 

  • Manzoni S, Taylor P, Richter A, Porporato A, Ågren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91

    Article  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • McGuire KL, Bent E, Borneman J, Majumder A, Allison SD, Treseder KK (2010) Functional diversity in resource use by fungi. Ecology 91:2324–2332

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Moorhead D, Lashermes G, Recous S, Bertrand I (2014) Interacting microbe and litter quality controls on litter decomposition: a modeling analysis. PLoS One. doi:10.1371/journal.pone.0108769

    Google Scholar 

  • Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016) Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem 93:1–7

    Article  Google Scholar 

  • Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014a) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol. doi:10.3389/fmicb.2014.00022

    Google Scholar 

  • Mooshammer M, Wanek W, Hämmerle I, Fuchslueger L, Hofhansl F, Knoltsch A, Schnecker J, Takriti M, Watzka M, Wild B, Keiblinger KM, Zechmeister-Boltenstern S, Richter A (2014b) Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling. Nat Commun. doi:10.1038/ncomms4694

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006

    Article  Google Scholar 

  • Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343

    Article  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

    Google Scholar 

  • Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    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 

  • Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JW (2011) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ 9:9–17

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15

    Article  Google Scholar 

  • Walker T, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  Google Scholar 

  • Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113

    Article  Google Scholar 

  • Watanabe F, Olsen S (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Sci Soc Am J 29:677–678

    Article  Google Scholar 

Download references

Acknowledgments

We thank Sylvie Millon, Antoine Portelette, Manon Gaddi, Olivier Delfosse, Marie Sauvadet, Bruno Buatois and Jorge Lebrato Mejijas for their laboratory assistance and help harvesting microcosms. The microcosm experiment, chemical analyses and enzymatic assays were performed at the Fractionnement AgroRessource et Environnement laboratory in Reims, and the PLFA analyses were performed at the Plate-Forme d’Analyses Chimiques en Ecologie (PACE) technical facility of the Laboratoire d’Excellence, Centre Méditerranéen de l’Environnement et de la Biodiversité, in Montpellier. Financial support for this study was provided by Champagne Ardennes Region and the CARINNA Agency through the EPRC project.

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Authors and Affiliations

  1. INRA, UMR 614 FARE, 2 Esplanade Roland Garros, 51100, Reims, France

    Nicolas Fanin & Isabelle Bertrand

  2. Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, 901-83, Umeå, Sweden

    Nicolas Fanin

  3. Department of Environmental Science, University of Toledo, Toledo, OH, 43606, USA

    Daryl Moorhead

  4. INRA, UMR 1222 Eco&Sols, 2 Place Viala, 34060, Montpellier, France

    Isabelle Bertrand

Authors
  1. Nicolas Fanin
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  2. Daryl Moorhead
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  3. Isabelle Bertrand
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Correspondence to Isabelle Bertrand.

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Responsible Editor: E. Matzner.

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Fanin, N., Moorhead, D. & Bertrand, I. Eco-enzymatic stoichiometry and enzymatic vectors reveal differential C, N, P dynamics in decaying litter along a land-use gradient. Biogeochemistry 129, 21–36 (2016). https://doi.org/10.1007/s10533-016-0217-5

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  • DOI: https://doi.org/10.1007/s10533-016-0217-5

Keywords

  • Decomposition
  • Extracellular enzymes
  • Microbial metabolism
  • Soil microorganisms
  • Stoichiometry