Modelling in situ activities of enzymes as a tool to explain seasonal variation of soil respiration from agro-ecosystems

Soil Biology and Biochemistry

Volumn 81, Issue , 2015, Pages 291-303

  Ali, Rana S ^a   Ingwersen, Joachim ^a   Demyan, Michael S ^a   Funkuin, Yvonne N ^a   Wizemann, Hans Dieter ^a   Kandeler, Ellen ^a   Poll, Christian ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

In situ activity; Moisture sensitivity; Q10; Seasonal variation; Temperature sensitivity; glucosidase

Indexed keywords

ENZYMES; ORGANIC CARBON; SOIL MOISTURE; TEMPERATURE;

GLUCOSIDASE; MOISTURE SENSITIVITY; Q10; SEASONAL VARIATION; TEMPERATURE SENSITIVITY;

SENSITIVITY ANALYSIS;

AGRICULTURAL ECOSYSTEM; AGRICULTURAL SOIL; DECOMPOSITION; ENVIRONMENTAL MODELING; ENZYME; ENZYME ACTIVITY; SEASONAL VARIATION; SOIL CARBON; SOIL RESPIRATION; TEMPERATURE EFFECT; WATER CONTENT;

GERMANY;

EID: 84919914924     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2014.12.001     Document Type: Article

References (85)

1. A'Bear A.D., Jones T.H., Kandeler E., Boddy L. Interactive effects of temperature and soil moisture on fungal-mediated wood decomposition and extracellular enzyme activity. Soil Biology and Biochemistry 2014, 70:151-158.
2. Ågren G.I., Bosatta E., Magill A.H. Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 2001, 128:94-98.
3. Allison S.D., Treseder K.K. Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology 2008, 14:2898-2909.
4. Allison S.D., Vitousek P.M. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology and Biochemistry 2005, 37:937-944.
5. Allison S.D., Wallenstein M.D., Bradford M.A. Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience 2010, 3:336-340.
6. Baldrian P., Šnajdr J., Merhautová V., Dobiášová P., Cajthaml T., Valášková V. Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biology and Biochemistry 2013, 56:60-68.
7. Bárta J., Šlajsová P., Tahovská K., Picek T., Šantrůčková H. Different temperature sensitivity and kinetics of soil enzymes indicate seasonal shifts in C, N and P nutrient stoichiometry in acid forest soil. Biogeochemistry 2014, 117:525-537.
8. Bell T.H., Klironomos J.N., Henry H.A.L. Seasonal responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Science Society of America Journal 2010, 74:820-828.
9. 2 production at elevated temperatures. Ecology Letters 2007, 10:783-790.
10. Bergfur J., Friberg N. Trade-offs between fungal and bacterial respiration along gradients in temperature, nutrients and substrata: experiments with stream derived microbial communities. Fungal Ecology 2012, 5:46-52.
11. Billings S.A., Ballantyne F. How interactions between microbial resource demands, soil organic matter stoichiometry, and substrate reactivity determine the direction and magnitude of soil respiratory responses to warming. Global Change Biology 2013, 19:90-102.
12. Blankinship J.C., Becerra C.A., Schaeffer S.M., Schimel J.P. Separating cellular metabolism from exoenzyme activity in soil organic matter decomposition. Soil Biology and Biochemistry 2014, 71:68-75.
13. Bradford M.A., Davies C.A., Frey S.D., Maddox T.R., Melillo J.M., Mohan J.E., Reynolds J.F., Treseder K.K., Wallenstein M.D. Thermal adaptation of soil microbial respiration to elevated temperature. Ecology Letters 2008, 11:1316-1327.
14. Bremner J.M., Zantua M.I. Enzyme activity in soils at subzero temperatures. Soil Biology and Biochemistry 1975, 7:383-387.
15. Brzostek E.R., Finzi A.C. Seasonal variation in the temperature sensitivity of proteolytic enzyme activity in temperate forest soils. Journal of Geophysical Research: Biogeosciences 2012, 117:G01018. 10.1029/2011JG001688.
16. Brzostek E.R., Finzi A.C. Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils. Ecology 2011, 92:892-902.
17. Buchmann N. Biotic and abiotic factors controlling soil respiration rates in picea abies stands. Soil Biology and Biochemistry 2000, 32:1625-1635.
18. Burns R.G., DeForest J.L., Marxsen J., Sinsabaugh R.L., Stromberger M.E., Wallenstein M.D., Weintraub M.N., Zoppini A. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology and Biochemistry 2013, 58:216-234.
19. Cañizares R., Benitez E., Ogunseitan O.A. Molecular analyses of β-glucosidase diversity and function in soil. European Journal of Soil Biology 2011, 47:1-8.
20. Chen G., Yang Y., Xie J., Li L., Gao R. Soil biological changes for a natural forest and two plantations in subtropical china. Pedosphere 2004, 14:297-304.
21. Conant R.T., Ryan M.G., Ågren G.I., Birge H.E., Davidson E.A., Eliasson P.E., Evans S.E., Frey S.D., Giardina C.P., Hopkins F.M., Hyvönen R., Kirschbaum M.U.F., Lavallee J.M., Leifeld J., Parton W.J., Megan Steinweg J., Wallenstein M.D., Martin Wetterstedt J.Å., Bradford M.A. Temperature and soil organic matter decomposition rates-synthesis of current knowledge and a way forward. Global Change Biology 2011, 17:3392-3404.
22. Cook F.J., Orchard V.A. Relationships between soil respiration and soil moisture. Soil Biology and Biochemistry 2008, 40:1013-1018.
23. Craine J.M., Gelderman T.M. Soil moisture controls on temperature sensitivity of soil organic carbon decomposition for a mesic grassland. Soil Biology and Biochemistry 2011, 43:455-457.
24. Davidson E.A., Janssens I.A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 2006, 440:165-173.
25. Davidson E.A., Samanta S., Caramori S.S., Savage K. The dual Arrhenius and Michaelis-menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales. Global Change Biology 2012, 18:371-384.
26. Davidson E.A., Belk E., Boone R.D. Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global Change Biology 1998, 4:217-227.
27. Feng X., Nielsen L.L., Simpson M.J. Responses of soil organic matter and microorganisms to freeze-thaw cycles. Soil Biology and Biochemistry 2007, 39:2027-2037.
28. Fenner N., Freeman C., Reynolds B. Observations of a seasonally shifting thermal optimum in peatland carbon-cycling processes; implications for the global carbon cycle and soil enzyme methodologies. Soil Biology and Biochemistry 2005, 37:1814-1821.
29. Fierer N., Craine J.M., McLauchlan K., Schimel J.P. Litter quality and the temperature sensitivity of decomposition. Ecology 2005, 86:320-326.
30. Frey S.D., Lee J., Melillo J.M., Six J. The temperature response of soil microbial efficiency and its feedback to climate. Nature Climate Change 2013, 3:395-398.
31. Georlette D., Blaise V., Collins T., D'Amico S., Gratia E., Hoyoux A., Marx J.-, Sonan G., Feller G., Gerday C. Some like it cold: biocatalysis at low temperatures. FEMS Microbiology Reviews 2004, 28:25-42.
32. German D.P., Chacon S.S., Allison S.D. Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology 2011, 92:1471-1480.
33. German D.P., Marcelo K.R.B., Stone M.M., Allison S.D. The Michaelis-menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Global Change Biology 2012, 18:1468-1479.
34. Gougoulias C., Clark J.M., Shaw L.J. The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems. Journal of the Science of Food and Agriculture 2014, 10.1002/jsfa.6577.
35. Hamamoto S., Moldrup P., Kawamoto K., Komatsu T. Excluded-volume expansion of Archie's law for gas and solute diffusivities and electrical and thermal conductivities in variably saturated porous media. Water Resources Research 2010, 46:W06514.
36. Han G., Zhou G., Xu Z., Yang Y., Liu J., Shi K. Biotic and abiotic factors controlling the spatial and temporal variation of soil respiration in an agricultural ecosystem. Soil Biology and Biochemistry 2007, 39:418-425.
37. Hargreaves S., Hofmockel K. Physiological shifts in the microbial community drive changes in enzyme activity in a perennial agroecosystem. Biogeochemistry 2014, 117:67-79.
38. He Y., Zhuang Q., Harden J.W., McGuire A.D., Fan Z., Liu Y., Wickland K.P. The implications of microbial and substrate limitation for the fates of carbon in different organic soil horizon types: a mechanistically based model analysis. Biogeosciences 2014, 2227-2266. Discussion 11.
39. Henry H.A.L. Soil extracellular enzyme dynamics in a changing climate. Soil Biology and Biochemistry 2012, 47:53-59.
40. Hinojosa M.B., Carreira J.A., García-Ruíz R., Dick R.P. Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils. Soil Biology and Biochemistry 2004, 36:1559-1568.
41. Hueso S., Hernández T., García C. Resistance and resilience of the soil microbial biomass to severe drought in semiarid soils: the importance of organic amendments. Applied Soil Ecology 2011, 50:27-36.
42. IPCC Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, Cambridge University Press, Cambridge and New York.
43. IUSS Working Group WRB World Reference Base for Soil Resources 2006, First Update 2007 2007, FAO, Rome, World Soil Resources Reports.
44. Jing X., Wang Y., Chung H., Mi Z., Wang S., Zeng H., He J. No temperature acclimation of soil extracellular enzymes to experimental warming in an alpine grassland ecosystem on the Tibetan plateau. Biogeochemistry 2014, 117:39-54.
45. Johnsen A.R., Jacobsen O.S. Aquick and sensitive method for the quantification of peroxidase activity of organic surface soil from forests. Soil Biology and Biochemistry 2008, 40:814-821.
46. Kandeler E. Characterization of free and adsorbed phosphatases in soils. Biology and Fertility of Soils 1990, 9:199-202.
47. Kandeler E., Stemmer M., Gerzabek M.H. Role of microorganisms in carbon cycling in soils. Microorganisms in Soils: Roles in Genesis and Functions 2005, 139-157. Springer, Berlin Heidelberg. A. Varma, F. Buscot (Eds.).
48. Kirschbaum M.U.F. Will changes in soil organic carbon act as a positive or negative feedback on global warming?. Biogeochemistry 2000, 48:21-51.
49. Kirschbaum M.U.F. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biology and Biochemistry 1995, 27:753-760.
50. Koch O., Tscherko D., Kandeler E. Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Global Biogeochemical Cycles 2007, 21:GB4017. 10.1029/2007GB002983.
51. Kramer S., Marhan S., Haslwimmer H., Ruess L., Kandeler E. Temporal variation in surface and subsoil abundance and function of the soil microbial community in an arable soil. Soil Biology and Biochemistry 2013, 61:76-85.
52. Kramer S., Marhan S., Ruess L., Armbruster W., Butenschoen O., Haslwimmer H., Kuzyakov Y., Pausch J., Scheunemann N., Schoene J., Schmalwasser A., Totsche K.U., Walker F., Scheu S., Kandeler E. Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems. Pedobiologia 2012, 55:111-119.
53. Lal R. Soil carbon sequestration impacts on global climate change and food security. Science 2004, 304:1623-1627.
54. Li J., Wang G., Allison S., Mayes M., Luo Y. Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity. Biogeochemistry 2014, 119:67-84.
55. Loague K., Green R.E. Statistical and graphical methods for evaluating solute transport models: overview and application. Journal of Contaminant Hydrology 1991, 7:51-73.
56. Manzoni S., Schimel J.P., Porporato A. Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 2012, 93:930-938.
57. Manzoni S., Taylor P., Richter A., Porporato A., Ågren G.I. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist 2012, 196:79-91.
58. Marx M.C., Wood M., Jarvis S.C. Amicroplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biology and Biochemistry 2001, 33:1633-1640.
59. Mendiburu F.d. Agricolae: Statistical Procedures for Agricultural Research. R Package Version 1.1-8 2014, http://CRAN.R-project.org/package=agricolae.
60. Mikan C.J., Schimel J.P., Doyle A.P. Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biology and Biochemistry 2002, 34:1785-1795.
61. Mtambanengwe F., Mapfumo P., Kirchmann H. Decomposition of organic matter in soil as influenced by texture and pore size distribution. Managing Nutrient Cycles to Sustain Soil Fertility in Sub-saharan Africa 2004, 261-297. Academy Science Publishers (ASP), Nairobi. B. Andre (Ed.).
62. Pinheiro J., Bates D., DebRoy S., Sarkar, Deepayan Nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-111 2013, R Development Core Team.
63. Poll C., Ingwersen J., Stemmer M., Gerzabek M.H., Kandeler E. Mechanisms of solute transport affect small-scale abundance and function of soil microorganisms in the detritusphere. European Journal of Soil Science 2006, 57:583-595.
64. 2 flux in a temperate agricultural ecosystem. Agriculture, Ecosystems and Environment 2013, 165:88-97.
65. R Core Team R: a Language and Environment for Statistical Computing 2013, R Foundation for Statistical Computing, Vienna, Austria, URL. http://www.R-project.org/.
66. Resat H., Bailey V., McCue L., Konopka A. Modeling microbial dynamics in heterogeneous environments: growth on soil carbon sources. Microbial Ecology 2012, 63:883-897.
67. Ryan M.G., Law B.E. Interpreting, measuring, and modeling soil respiration. Biogeochemistry 2005, 73:3-27.
68. Schimel J., Balser T.C., Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 2007, 88:1386-1394.
69. Schimel J.P., Clein J.S. Microbial response to freeze-thaw cycles in tundra and taiga soils. Soil Biology and Biochemistry 1996, 28:1061-1066.
70. Schimel J.P., Weintraub M.N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology and Biochemistry 2003, 35:549-563.
71. Schinner F., von Mersi W. Xylanase-, CM-cellulase- and invertase activity in soil: an improved method. Soil Biology and Biochemistry 1990, 22:511-515.
72. Sinsabaugh R.L. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology and Biochemistry 2010, 42:391-404.
73. Sinsabaugh R.S. Enzymic analysis of microbial pattern and process. Biology and Fertility of Soils 1994, 17:69-74.
74. Sinsabaugh R., Follstad Shah J. Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse. Biogeochemistry 2011, 102:31-43.
75. Steinweg J.M., Dukes J.S., Paul E.A., Wallenstein M.D. Microbial responses to multi-factor climate change: effects on soil enzymes. Frontiers in Microbiology 2013, 4. Article 146.
76. Steinweg J.M., Dukes J.S., Wallenstein M.D. Modeling the effects of temperature and moisture on soil enzyme activity: linking laboratory assays to continuous field data. Soil Biology and Biochemistry 2012, 55:85-92.
77. Todd-Brown K., Hopkins F., Kivlin S., Talbot J., Allison S. Aframework for representing microbial decomposition in coupled climate models. Biogeochemistry 2012, 109:19-33.
78. Trasar-Cepeda C., Gil-Sotres F., Leirós M.C. Thermodynamic parameters of enzymes in grassland soils from galicia, NW spain. Soil Biology and Biochemistry 2007, 39:311-319.
79. Wallenstein M.D., McMahon S.K., Schimel J.P. Seasonal variation in enzyme activities and temperature sensitivities in arctic tundra soils. Global Change Biology 2009, 15:1631-1639.
80. Wallenstein M.D., Weintraub M.N. Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biology and Biochemistry 2008, 40:2098-2106.
81. Wan S., Luo Y. Substrate regulation of soil respiration in a tallgrass prairie: results of a clipping and shading experiment. Global Biogeochemical Cycles 2003, 17. 10.1029/2002GB001971.
82. Wang G., Post W.M., Mayes M.A., Frerichs J.T., Sindhu J. Parameter estimation for models of ligninolytic and cellulolytic enzyme kinetics. Soil Biology and Biochemistry 2012, 48:28-38.
83. Weedon J.T., Aerts R., Kowlachuk G.A., van Bodegom P.M. Enzymology under global change: organic nitrogen turnover in alpine and sub-arctic soils. Biochemical Society Transactions 2011, 39:309-314.
84. Wyman C., Decker S., Himmel M., Brady J., Skopec C., Viikari L. Hydrolysis of cellulose and hemicellulose. Polysaccharides: Structural Diversity and Functional Versatility 2004, 995-1034. CRC Press, New York. second ed. S. Dumitriu (Ed.).
85. Zimmermann M., Bird M.I. Temperature sensitivity of tropical forest soil respiration increase along an altitudinal gradient with ongoing decomposition. Geoderma 2012, 187-188:8-15.