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Soil Enzymology pp 229–243Cite as

Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function

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Part of the book series: Soil Biology ((SOILBIOL,volume 22))

Abstract

Extracellular enzymes allow microbes and plant roots to acquire resources from complex molecules, and thereby catalyze the rate-limiting step in soil carbon and nutrient cycling. We examine the hypothesis that extracellular enzyme producers are under evolutionary pressure to minimize the cost:benefit ratio of enzyme production. Consistent with this prediction, enzyme producers generally allocate more resources to enzymes that target limiting nutrients. Additionally, regulatory systems have evolved to increase enzyme production when substrates are abundant and available resources are scarce. Finally, theoretical models predict that producers should control enzyme diffusion rates and adopt strategies to reduce competition for enzymatic reaction products. Because extracellular enzymes regulate ecosystem processes, enzyme allocation could affect ecosystem responses to environmental change. In particular, shifts in enzyme allocation may result in negative feedbacks to changes in resource availability. Enzyme allocation patterns therefore link ecological and evolutionary constraints at the organismal level with ecosystem-level processes.

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References

  • Ajwa HA, Dell CJ, Rice CW (1999) Changes in enzyme activities and microbial biomass of tallgrass prairie soil as related to burning and nitrogen fertilization. Soil Biol Biochem 31:769–777

    Article  CAS  Google Scholar 

  • Allison SD (2005) Cheaters, diffusion, and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol Lett 8:626–635

    Article  Google Scholar 

  • Allison SD (2006) Brown ground: a soil carbon analogue for the green world hypothesis? Am Nat 167:619–627

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Allison SD, Nielsen CB, Hughes RF (2006) Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana. Soil Biol Biochem 38:1537–1544

    Article  CAS  Google Scholar 

  • Allison SD, Gartner TB, Holland K, Weintraub M, Sinsabaugh RL (2007a) Soil enzymes: linking proteomics and ecological processes. In: Hurst CJ, Crawford RL, Garland JL, Lipson DA, Mills AL, Stetzenbach LD (eds) Manual of environmental microbiology, 3rd edn. ASM, Washington, DC, pp 704–711

    Google Scholar 

  • Allison VJ, Condron LM, Peltzer DA, Richardson SJ, Turner BL (2007b) Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol Biochem 39:1770–1781

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Antibus RK, Sinsabaugh RL, Linkins AE (1992) Phosphatase activities and phosphorus uptake from inositol phosphate by ectomycorrhizal fungi. Can J Bot 70:794–801

    Article  CAS  Google Scholar 

  • Bartnicki-Garcia S (1968) Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu Rev Microbiol 22:87–108

    Article  PubMed  CAS  Google Scholar 

  • Burns RG (1978) Soil enzymes. Academic, New York

    Google Scholar 

  • Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427

    Article  CAS  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 

  • Chróst RJ (1991) Environmental control of the synthesis and activity of aquatic microbial ectoenzymes. In: Chróst RJ (ed) Microbial enzymes in aquatic environments. Springer, New York, pp 29–59

    Chapter  Google Scholar 

  • Chung H, Zak DR, Reich PB, Ellsworth DS (2007) Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Global Change Biol 13:908–989

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867

    Article  PubMed  CAS  Google Scholar 

  • Drissner D, Blum H, Tscherko D, Kandeler E (2007) Nine years of enriched CO2 changes the function and structural diversity of soil microorganisms in a grassland. Eur J Soil Sci 58:260–269

    Article  Google Scholar 

  • Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

    Article  CAS  Google Scholar 

  • Ekschmitt K, Liu MQ, Vetter S, Fox O, Wolters V (2005) Strategies used by soil biota to overcome soil organic matter stability – why is dead organic matter left over in the soil? Geoderma 128:167–176

    Article  Google Scholar 

  • Elser J (2006) Biological stoichiometry: a chemical bridge between ecosystem ecology and evolutionary biology. Am Nat 168:S25–S35

    Article  PubMed  Google Scholar 

  • Eriksson KE, Pettersson B, Westmark U (1974) Oxidation: an important enzyme reaction in fungal degradation of cellulose. FEBS Lett 49:282–285

    Article  PubMed  CAS  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 

  • Franck VM, Hungate BA, Chapin FS III, Field CB (1997) Decomposition of litter produced under elevated CO2: dependence on plant species composition. Biogeochemistry 36:223–237

    Article  Google Scholar 

  • Frankena J, Vanverseveld HW, Stouthamer AH (1988) Substrate and energy costs of the production of exocellular enzymes by Bacillus-licheniformis. Biotechnol Bioeng 32:803–812

    Article  PubMed  CAS  Google Scholar 

  • Friedel JK, Scheller E (2002) Composition of hydrolyzable amino acids in soil organic matter and soil microbial biomass. Soil Biol Biochem 34:315–325

    Article  CAS  Google Scholar 

  • Hamilton EW III, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2404

    Article  Google Scholar 

  • Hanif A, Yasmeen A, Rajoka MI (2004) Induction, production, repression, and de-repression of exoglucanase synthesis in Aspergillus niger. Bioresour Technol 94:311–319

    Article  PubMed  CAS  Google Scholar 

  • Haynes RJ, Swift RS (1988) Effects of lime and phosphate additions on changes in enzyme activities, microbial biomass and levels of extractable nitrogen, sulfur and phosphorus in an acid soil. Biol Fertil Soils 6:153–158

    Article  CAS  Google Scholar 

  • Henry HAL, Juarez JD, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Global Change Biol 11:1808–1815

    Article  Google Scholar 

  • Hughes RF, Denslow JS (2005) Invasion by a N2-fixing tree alters function and structure in wet lowland forests of Hawai’i. Ecol Appl 15:1615–1628

    Article  Google Scholar 

  • Hungate BA, Holland EA, Jackson RB, Chapin FS III, Mooney HA, Field CB (1997) The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388:576–579

    Article  CAS  Google Scholar 

  • Jackson RB, Mooney HA, Schulze E-D (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci USA 94:7362–7366

    Article  PubMed  CAS  Google Scholar 

  • Jacob F, Monod J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3:318–356

    Article  PubMed  CAS  Google Scholar 

  • Johnson DW (2006) Progressive N limitation in forests: review and implications for long-term responses to elevated CO2. Ecology 87:64–75

    Article  PubMed  Google Scholar 

  • Johnson D, Leake JR, Lee JA, Campbell CD (1998) Changes in soil microbial biomass and microbial activities in response to 7 years simulated pollutant nitrogen deposition on a heathland and two grasslands. Environ Pollut 103:239–250

    Article  CAS  Google Scholar 

  • Koide RT, Xu B, Sharda J, Lekberg Y, Ostiguy N (2005) Evidence of species interactions within an ectomycorrhizal fungal community. New Phytol 165:305–316

    Article  PubMed  Google Scholar 

  • Koroljova-Skorobogatko OV, Stepanova EV, Gavrilova VP, Morozova OV, Lubimova NV, Dzchafarova AN, Jaropolov AI, Makower A (1998) Purification and characterization of the constitutive form of laccase from the basidiomycete Coriolus hirsutus and effect of inducers on laccase synthesis. Biotechnol Appl Biochem 28:47–54

    CAS  Google Scholar 

  • Larson JL, Zak DR, Sinsabaugh RL (2002) Extracellular enzyme activity beneath temperate trees growing under elevated carbon dioxide and ozone. Soil Sci Soc Am J 66:1848–1856

    Article  CAS  Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  • Makino W, Cotner JB, Sterner RW, Elser JJ (2003) Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C:N:P stoichiometry. Funct Ecol 17:121–130

    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 

  • Moorhead DL, Linkins AE (1997) Elevated CO2 alters belowground exoenzyme activities in tussock tundra. Plant Soil 189:321–329

    Article  CAS  Google Scholar 

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

    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  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2004) Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289

    Article  CAS  Google Scholar 

  • Priest FG (1977) Extracellular enzyme synthesis in the genus Bacillus. Bacteriol Rev 41:711–753

    PubMed  CAS  Google Scholar 

  • Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil processes. Ecology 80:2408–2419

    Article  Google Scholar 

  • Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221

    CAS  Google Scholar 

  • Redfield RJ (2002) Is quorum sensing a side effect of diffusion sensing. Trends Microbiol 10:365–372

    Article  PubMed  CAS  Google Scholar 

  • Reiners WA (1986) Complementary models for ecosystems. Am Nat 127:59–73

    Article  Google Scholar 

  • Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental warming. Oecologia 126:543–562

    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  CAS  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  CAS  Google Scholar 

  • Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Microbiol Mol Biol Rev 36:407–477

    CAS  Google Scholar 

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

    Article  CAS  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, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    PubMed  Google Scholar 

  • Skujins JJ (1976) History of abiontic soil enzyme research. In: Burns RG (ed) Soil enzymes. Academic, London, pp 1–49

    Google Scholar 

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

    Google Scholar 

  • Sun Y-P, Unestam T, Lucas SD, Johanson KJ, Kenne L, Finlay R (1999) Exudation-reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and soil microorganisms. Mycorrhiza 9:137–144

    Article  CAS  Google Scholar 

  • Swift MJ, Andrén O, Brussaard L, Briones M, Couteaux M-M, Ekschmitt K, Kjoller A, Loiseau P, Smith P (1998) Global change, soil biodiversity, and nitrogen cycling in terrestrial ecosystems: three case studies. Global Change Biol 4:729–743

    Article  Google Scholar 

  • Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954

    Article  Google Scholar 

  • Trumbore SE (1997) Potential responses of soil organic carbon to global environmental change. Proc Natl Acad Sci USA 94:8284–8291

    Article  PubMed  CAS  Google Scholar 

  • Vetter YA, Denning JW, Jumars PA, Krieger-Brockett BB (1998) A predictive model of bacterial foraging by means of freely released extracellular enzymes. Microb Ecol 36:75–92

    Article  PubMed  CAS  Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Voigt B, Schweder T, Sibbald MJJB, Albrecht D, Ehrenreich A, Bernhardt J, Feesche J, Maurer K-H, Gottschalk G, van Dijl JM, Hecker M (2006) The extracellular proteome of Bacillis licheniformis grown in different media and under different nutrient starvation conditions. Proteomics 6:268–281

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Waldrop MP, Zak DR, Sinsabaugh RL, Gallo M, Lauber C (2004b) Nitrogen deposition modifies soil carbon storage through changes in microbial enzyme activity. Ecol Appl 14:1172–1177

    Article  Google Scholar 

  • Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106

    Article  CAS  Google Scholar 

  • Weintraub MN, Schimel JP (2005) Seasonal protein dynamics in Alaskan arctic tundra soils. Soil Biol Biochem 37:1469–1475

    Article  CAS  Google Scholar 

  • Zou X, Binkley D, Caldwell BA (1995) Effects of dinitrogen-fixing trees on phosphorus biogeochemical cycling in contrasting forests. Soil Sci Soc Am J 59:1452–1458

    Article  CAS  Google Scholar 

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Acknowledgments

We thank B. Caldwell, J. Talbot, K. Treseder, and S. Perakis for valuable comments on the manuscript. This research was supported by a NOAA Climate and Global Change Fellowship to SDA and a workshop grant from the NSF-LTER Network Office.

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Authors and Affiliations

  1. University of California, Irvine, 321 Steinhaus, Irvine, CA, 92697, USA

    Steven D. Allison

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

    Michael N. Weintraub

  3. Department of Biology and the Environmental Science Program, Carthage College, Kenosha, WI, 53140, USA

    Tracy B. Gartner

  4. US Geological Survey, 345 Middlefield Rd, MS 962, Menlo Park, CA, 94025, USA

    Mark P. Waldrop

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  1. Steven D. Allison
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  2. Michael N. Weintraub
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  3. Tracy B. Gartner
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  4. Mark P. Waldrop
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Corresponding author

Correspondence to Steven D. Allison .

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Editors and Affiliations

  1. Dept. Biological, Geological &, Environmental Sciences, Cleveland State University, Euclid Ave. 2121, Cleveland, 44115-2214, Ohio, USA

    Girish Shukla

  2. Amity Institute of Microbial Sciences, Amity University Uttar Pradesh, Noida, 201303, Uttar Pradesh, India

    Ajit Varma

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Allison, S.D., Weintraub, M.N., Gartner, T.B., Waldrop, M.P. (2010). Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function. In: Shukla, G., Varma, A. (eds) Soil Enzymology. Soil Biology, vol 22. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14225-3_12

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