Korean Journal of Microbiology (미생물학회지)

The Microbiological Society of Korea (한국미생물학회)
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A review of factors that regulate extracellular enzyme activity in wetland soils

습지 토양 내 체외효소 활성도를 조절하는 인자에 대한 고찰

  • Kim, Haryun (School of Environmental Science and Engineering, Pohang University of Science and Technology)
  • 김하련 (포항공과대학교 환경공학부)
  • Received : 2014.12.24
  • Accepted : 2015.05.21
  • Published : 2015.06.30
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Abstract

Wetlands constitute a transitional zone between terrestrial and aquatic ecosystems and have unique characteristics such as frequent inundation, inflow of nutrients from terrestrial ecosystems, presence of plants adapted to grow in water, and soil that is occasionally oxygen deficient due to saturation. These characteristics and the presence of vegetation determine physical and chemical properties that affect decomposition rates of organic matter (OM). Decomposition of OM is associated with activities of various extracellular enzymes (EE) produced by bacteria and fungi. Extracellular enzymes convert macromolecules to simple compounds such as labile organic carbon (C), nitrogen (N), phosphorus (P), and sulfur (S) that can be easily taken up by microbes and plants. Therefore, the enzymatic approach is helpful to understand the decomposition rates of OM and nutrient cycling in wetland soils. This paper reviews the physical and biogeochemical factors that regulate extracellular enzyme activities (EEa) in wetland soils, including those of ${\beta}$-glucosidase, ${\beta}$-N-acetylglucosaminidase, phosphatase, arylsulfatase, and phenol oxidase that decompose organic matter and release C, N, P, and S nutrients for microbial and plant growths. Effects of pH, water table, and particle size of OM on EEa were not significantly different among sites, whereas the influence of temperature on EEa varied depending on microbial acclimation to extreme temperatures. Addition of C, N, or P affected EEa differently depending on the nutrient state, C:N ratio, limiting factors, and types of enzymes of wetland soils. Substrate quality influenced EEa more significantly than did other factors. Also, drainage of wetland and increased temperature due to global climate change can stimulate phenol oxidase activity, and anthropogenic N deposition can enhance the hydrolytic EEa; these effects increase OM decomposition rates and emissions of $CO_2$ and $CH_4$ from wetland systems. The researches on the relationship between microbial structures and EE functions, and environmental factors controlling EEa can be helpful to manipulate wetland ecosystems for treating pollutants and to monitor wetland ecosystem services.

육상과 수계의 전이지대에 위치한 습지는 빈번한 침수, 육상생태계로부터의 영양염류의 유입, 수계와 토양에 적절하게 적응된 식생의 존재 및 토양 내 산소 결핍과 같은 독특한 특징을 가지고 있다. 이러한 생지화학적 특성과 독특한 식생의 존재는 유기물의 분해과정에 물리적 화학적 영향을 미치고 있는데, 특히 미생물에서 생산되는 체외효소 활성도는 유기물의 분해 과정과 관련을 맺고 있다. 체외효소는 고분자 유기물을 간단한 형태의 유기탄소, 무기 질소, 인, 황으로 분해하여 미생물과 식물이 용이하게 이들 영양물질을 흡수할 수 있도록 도움을 주기 때문에, 체외효소에 대한 연구는 습지 토양 내에서의 유기물 분해와 물질순환의 기작을 이해하는 데 필수적인 요소이다. 본 연구는 습지 토양 내 ${\beta}$-glucosidase, ${\beta}$-N-acetylglucosaminidase, phosphatase, arylsulfatase, phenol oxidase와 같은 체외 효소활성도에 영향을 미치는 물리적 생지화학적 요소가 무엇인지 문헌연구를 통하여 고찰하였다. 물리적 요소로써, pH와 유기물의 입자 크기는 체외효소 활성도에 크게 영향을 미치지 않았으나, 온도에 대한 영향은 미생물의 극한 온도에서의 적응성 정도에 따라 다양하게 나타났다. 화학적 요소로써, 탄소, 질소, 인의 첨가는 습지 토양의 영양상태, C:N 비율과 제한 요소, 및 체외효소의 종류에 따라 그 영향이 다양하게 발현되었다. 특히, 유기물의 기질 특성(Substrate quality)은 다른 어떤 요소보다도 체외효소 활성도에 큰 영향을 미치는 것으로 나타났다. 향후 연구 과제로써는 기후 변화와 질소 침적의 증가에 따른 효소 활성도의 변화 및 분자생물학적 접근을 통한 미생물 군집과 체외효소 기능간의 관계를 규명하는 연구가 필요하다. 또한, 습지 토양내 체외효소 활성도를 극대화 할 수 있는 환경을 조성함으로써, 앞으로 습지 토양이 오염물질을 제거하고 습지의 생태학적 기능을 최대화 할 수 있는 연구가 요구된다.

Keywords

References

  1. Aber, J.D., McDowell, W., Nadelhoffer, K., Magil, A., Berntson, G., Kamakea, M., McNulty, S., Currie, W., Rustad L., and Fernandez, I. 1998. Nitrogen saturation in temperate forest ecosystems: Hypotheses revisited. Bioscience 48, 921-934. https://doi.org/10.2307/1313296
  2. Aciego Pietri, J.C. and Brookes, P.C. 2008. Relationship between soil pH and microbial properties in a UK arable soil. Soil Biol. Biochem. 40, 1856-1861. https://doi.org/10.1016/j.soilbio.2008.03.020
  3. Acosta-Martinez, V. and Tabatabai, M.A. 2000. Enzyme activities in a limed agricultural soil. Biol. Fertil. Soils 31, 85-91. https://doi.org/10.1007/s003740050628
  4. Adu, J.K. and Oades, J.M. 1978. Utilization of organic materials in soil aggregates by bacterial and fungi. Soil Biol. Biochem. 10, 117-122. https://doi.org/10.1016/0038-0717(78)90081-0
  5. Aerts, R. 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: A triangular relationship. Oikos. 439, 449.
  6. Amador, J.A., Glucksman, A.M., Lyons, J.B., and Gorres, J.H. 1997. Spatial distribution of soil phosphatase activity within a riparian forest. Soil Sci. 162, 808-825. https://doi.org/10.1097/00010694-199711000-00005
  7. Arnone, J.A. and Hirschel, G. 1997. Does fertilizer application alter the effects of elevated ${CO_2}$ on Carex leaf litter quality and in situ decomposition in an alpine grassland? Acta Oecol. 18, 201-206. https://doi.org/10.1016/S1146-609X(97)80006-9
  8. Benner, R., Newell, S.Y., Maccubbin, A.E., and Hodson, R.E. 1984. Relative contributions of bacteria and fungi to rates of degradation of lignocellulosic detritus in salt-marsh sediments. Appl. Environ. Microbiol. 48, 36-40.
  9. Bertrand, I., Chabbert, B., Kurek, B., and Recous, S. 2006. Can the biochemical features and histology of wheat residues explain their decomposition in soil? Plant Soil 281, 291-307. https://doi.org/10.1007/s11104-005-4628-7
  10. Bowen, G.D. 1969. Nutrient status effects on loss of amides and amino acids from pine roots. Plant Soil 30, 139-142. https://doi.org/10.1007/BF01885274
  11. Bragazza, L., Freeman, C., Jones, T., Rydin, H., Limpens, J., Fenner, N., Ellis, T., Gerdol, R., Hajek, M., Hajek, T., et al. 2006. Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proc. Natl. Acad. Sci. USA 103, 19386-19389. https://doi.org/10.1073/pnas.0606629104
  12. Burns, R.G., DeForest, J.L., Marxsen, J., Sinsabaugh, R.L., Stromberger, M.E., Wallenstein, M.D., Weintraub, M.N., and Zoppini, A. 2013. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biol. Biochem. 58, 216-234. https://doi.org/10.1016/j.soilbio.2012.11.009
  13. Caravaca, F., Alguacil, M.M., Torres, P., and Rdldan, A. 2005. Plant type mediates rhizospheric microbial activities and soil aggregation in a semiarid Mediterranean slat marsh. Geoderma. 124, 375-382. https://doi.org/10.1016/j.geoderma.2004.05.010
  14. Carreiro, M., Sinsabaugh, R., Repert, D., and Parkhurst, D. 2000. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81, 2359-2365. https://doi.org/10.1890/0012-9658(2000)081[2359:MESELD]2.0.CO;2
  15. Chen, C.R., Condron, L.M., Davis, M.R., and Sherlock, R.R. 2003. Seasonal changes in soil phosphorus and associated microbial properties under adjacent grassland and forest in New Zealand. Forest Ecol. Manag. 177, 539-557. https://doi.org/10.1016/S0378-1127(02)00450-4
  16. Cotrufo, M.F., Ineson, P., and Rowland, A.P. 1994. Decomposition of tree leaf litters grown under elevated ${CO_2}$: Effect of litter quality. Plant Soil 163, 121-130. https://doi.org/10.1007/BF00033948
  17. Cotrufo, M.F. and Ineson, P. 1995. Effects of enhanced atmospheric ${CO_2}$ decomposition of the fin roots of Betula pendula Roth decomposition of the fin roots of Betula pendula Roth. and Picea sitchensis (Bong.) Carr. Plant Soil 165, 1-6.
  18. Cregger, M.A., Sanders, N., Dunn, R.R., and Classen, A.T. 2014. Microbial communities respond to experimental warming, but site matters. Peer J. 2, e358. https://doi.org/10.7717/peerj.358
  19. Cui, L.H., Ouyang, Y., Gu, W.J., Yang, W.Z., and Xu, Q.L. 2013. Evaluation of nutrient removal efficiency and microbial enzyme activity in a baffled subsurface-flow constructed wetland system. Bioresour. Technol. 146, 656-662. https://doi.org/10.1016/j.biortech.2013.07.105
  20. Curtis, P.S., Zak, D.R., Pregitzer, K.S., and Teeri, J.A. 1994. Above and below ground response of Pooulus grandidentata to elevated atmospheric ${CO_2}$ and soil N availability. Plant Soil 165, 45-51. https://doi.org/10.1007/BF00009961
  21. Curtis, P.S. and Wang, X. 1998. A meta-analysis of elevated ${CO_2}$ effects on woody plant mass, form and physiology. Oecologia 113, 299-313. https://doi.org/10.1007/s004420050381
  22. Davidson, E.A. and Janssens, I.A. 2006. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165-173. https://doi.org/10.1038/nature04514
  23. Edwards, I.P., Zak, D.R., Kellner, H., Eisenlord, S.D., and Pregitzer, K.S. 2011. Simulated atmospheric N deposition alters fungal community composition and suppresses ligninolytic gene expression in a northern hardwood forest. PLoS One 6, e20421. https://doi.org/10.1371/journal.pone.0020421
  24. Ekenler, M. and Tabatabai, M.A. 2003. Effects of liming and tillage systems on microbial biomass and glycosidases in soils. Biol. Fertil. Soils 39, 51-61. https://doi.org/10.1007/s00374-003-0664-8
  25. Eversberger, D., Niklaus, P.A., and Kandeler, E. 2001.c. Soil Biol. Biochem. 35, 965-972.
  26. Fenner, N., Dowrick, D.J., Lock, M.A., Rafarel, C.R., and Freeman, C. 2006. A novel approach to studying the effects of temperature on soil biogeochemistry using a thermal gradient bar. Soil Use Manage. 22, 267-273. https://doi.org/10.1111/j.1475-2743.2006.00037.x
  27. Fenner, N., Freeman, C., and Reynolds, B. 2005a. Observation of a seasonally shifting thermal optimum in peatland carbon-cycling processes: Implications for the global carbon cycle and soil enzyme methodologies. Soil Biol. Biochem. 37, 1814-1821. https://doi.org/10.1016/j.soilbio.2005.02.032
  28. Fenner, N., Freeman, C., and Reynolds, B. 2005b. Hydrological effects on the diversity of phenolic degrading bacteria in a peatland: implications for carbon cycling. Soil Biol. Biochem. 37, 1277-1287. https://doi.org/10.1016/j.soilbio.2004.11.024
  29. Fenner, N. and Freeman, C. 2011. Drought-induced carbon loss in peatlands. Nat. Geosci. 4, 895-900. https://doi.org/10.1038/ngeo1323
  30. Freeman, C., Fenner, N., Ostle, N.J., Kang, H., Dowrick, D.J., Reynolds, B., Lock, M.A., Sleep, D., Hughes, S., and Hudson, J. 2004. Export of dissolved organic carbon from peatlands under elevated carbon dioxide levels. Nature 430, 195-198. https://doi.org/10.1038/nature02707
  31. Freeman, C., Liska, G., Ostle, N.J., Locj, M.A., Reynolds, B., and Hudson, J. 1996. Microbial activity and enzymatic decomposition processes following peatland water table drawdown. Plant Soil 180, 121-127. https://doi.org/10.1007/BF00015418
  32. Freeman, C., Lock, M.A., Marxsen, J., and Jones, S.E. 1990. Inhibitory effects of high molecular weight dissolved organic matter upon metabolic processes in biofilms from contrasting rivers and streams. Freshwater Biol. 24, 159-166. https://doi.org/10.1111/j.1365-2427.1990.tb00315.x
  33. Freeman, C., Nevison, G.B., Hughes, S., Reynolds, B., and Hudson, J. 1998. Enzymic involvement in the biogeochemical responses of a Welsh peatland to a rainfall enhancement manipulation. Biol. Fert. Soils 27, 173-178. https://doi.org/10.1007/s003740050417
  34. Freeman, C., Ostle, N., and Kang, H. 2001. An enzymic 'latch' on a global carbon store. Nature 409, 149.
  35. Freitas, J., Duarte, B., and Cacador, I. 2014. Biogeochemical drivers of phosphatase activity in salt marsh sediments. J. Sea Res. doi:10.1016/j.seares.2014.04.002.
  36. Frey, S.D., Knorr, M., Parrent, J.L., and Simpson, R.T. 2004. Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperature hardwood and pine forest. Forest Ecol. Manag. 196, 159-171. https://doi.org/10.1016/j.foreco.2004.03.018
  37. Gorissen, A., van Ginkel, J.H., Keurentjes, J.J.B., and van Veen, J.A. 1995. Grass root decomposition in retarded when grass has been grown under elevated ${CO_2}$. Soil Biol. Biochem. 17, 117-120.
  38. Grayston, S.J., Vaughan, D., and Jones, D. 1996. Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impacts on microbial activity and nutrient availability. Appl. Soil Ecol. 5, 29-56.
  39. Harrington, E.D., Singh, A.H., Doerks, T., Letunic, I., Mering, C., von Jensen, L.J., Raes, J., and Bork, P. 2007. Quantitative assessment of protein function prediction from metagenomics shotgun sequences. Proc. Natl. Acad. Sci. USA 104, 13913-1318. https://doi.org/10.1073/pnas.0702636104
  40. Henriksen, T.M. and Breland, T.A. 1999. Nitrogen availability effects on carbon mineralization, fungal and bacterial growth, and enzyme activities during decomposition of wheat straw in soil. Soil Biol. Biochem. 31, 1121-1134. https://doi.org/10.1016/S0038-0717(99)00030-9
  41. Henry, H.A.L. 2013. Reprint of "Soil extracellular enzyme dynamics in a changing climate". Soil Biol. Biochem. 56, 53-59. https://doi.org/10.1016/j.soilbio.2012.10.022
  42. Holland, E.A. and Coleman, D.C. 1987. Litter placement effects in microbial and organic matter dynamics in an agroecosystem. Ecology 68, 425-433. https://doi.org/10.2307/1939274
  43. Huang, L., Gao, X., Liu, M., Du, G., Guo, J., and Ntakirutimana, T. 2012. Correlation among soil microorganisms, soil enzyme activities, and removal rates of pollutants in three constructed wetlands purifying micro-polluted river water. Ecol. Eng. 46, 9-106.
  44. Jackson, C.R. and Vallaire, S.C. 2007. Microbial activity and decomposition of fine particulate organic matter in a Louisiana cypress swamp. J. N. Am. Benthol. Soc. 26, 743-753. https://doi.org/10.1899/07-020R1.1
  45. Kang, H. and Freeman, C. 1999. Phosphatase and arylsulphatase activities in wetland soils: annual variation and controlling factors. Soil Biol. Biochem. 31, 449-454. https://doi.org/10.1016/S0038-0717(98)00150-3
  46. Kang, H. and Freeman, C. 2007. Interactions of marsh orchid (Dactylorhiza spp.) and soil microorganisms in relation to extracellular enzyme activities in a peat soil. Pedosphere 17, 681-687. https://doi.org/10.1016/S1002-0160(07)60082-4
  47. Kang, H., Freeman, C., and Ashendon, T.W. 2001. Effects of elevated ${CO_2}$ on fen peat biogeochemistry. Sci. Total Environ. 279, 45-50. https://doi.org/10.1016/S0048-9697(01)00724-0
  48. Kang, H., Freeman, C., Lee, D., and Mitch, W.J. 1998. Enzyme activities in constructed wetlands: implication for water quality amelioration. Hydrobiologia 368, 231-235. https://doi.org/10.1023/A:1003219123729
  49. Kang, H., Kim, S., Fenner, N., and Freeman, C. 2005. Shifts of soil enzyme activities in wetlands exposed to elevated ${CO_2}$. Sci. Total Environ. 337, 207-212. https://doi.org/10.1016/j.scitotenv.2004.06.015
  50. Kellner, H., Luis, P., and Buscot, F. 2007. Diversity of laccase-like multicopper oxidase genes in Morchellaceae: identification of genes potentially involved in extracellular activities related to plant litter decay. FEMS Microbiol. Ecol. 61, 153-163. https://doi.org/10.1111/j.1574-6941.2007.00322.x
  51. Kim, J.G. 2001. Decomposition of plant material in a subalpine marsh. Plant Biol. 44, 73-80. https://doi.org/10.1007/BF03030278
  52. Koch, O., Tscherko, D., and Kandeler, E. 2007. Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Global Biogeochem. Cy. 21, GB4017.
  53. Kong, L., Wang, Y.B., Zhao, L.N., and Chen, Z.H. 2009. Enzyme and root activities in surface-flow constructed wetlands. Chemosphere 76, 601-608. https://doi.org/10.1016/j.chemosphere.2009.04.056
  54. Korboulewsky, N., Wang, R.Y., and Baldy, V. 2012. Purification processes involved in sludge treatment by a vertical flow wetland system: focus on the role of the substrate and plants on N and P removal. Bioresour. Technol. 105, 9-14. https://doi.org/10.1016/j.biortech.2011.11.037
  55. Koukoura, Z., Mamolos, A.P., and Kalburtji, K.L. 2003. Decomposition of dominant plant species litter in a semi-arid grassland. Appl. Soil Ecol. 23, 13-23. https://doi.org/10.1016/S0929-1393(03)00006-4
  56. Kwon, M., Haraguchi, A., and Kang, H. 2013. Long-term water regime differentiates changes in decomposition and microbial properties in tropical peat soils exposed to the short-term drought. Soil Biol. Biochem. 60, 33-44. https://doi.org/10.1016/j.soilbio.2013.01.023
  57. Kues, U. 2015. Fungal enzymes for environmental management. Curr. Opin. Biotechnol. 33, 268-278. https://doi.org/10.1016/j.copbio.2015.03.006
  58. Martens, D.A., Johanson, J.B., and Frankenberger, W.T. 1992. Production and persistence of soil enzymes with repeated addition of organic residues. Soil Sci. 153, 53-61. https://doi.org/10.1097/00010694-199201000-00008
  59. Marx, M.C., Kandeler, E., Wood, M., Wermbter, N., and Jarvis, S.C. 2005. Exploring the enzymatic landscape: distribution and kinetics of hydrolytic enzymes in soil particle-size fractions. Soil Biol. Biochem. 37, 35-48. https://doi.org/10.1016/j.soilbio.2004.05.024
  60. Mentzer, J.L., Goodman, R.M., and Balser, T.C. 2006. Microbial response over time to hydrologic and fertilization treatments in a simulated wet prairie. Plant Soil 284, 85-100. https://doi.org/10.1007/s11104-006-0032-1
  61. Min, K., Kang, H., and Lee, D. 2011. Effects of ammonium and nitrate additions on carbon mineralization in wetland soils. Soil Biol. Biochem. 43, 2461-2469. https://doi.org/10.1016/j.soilbio.2011.08.019
  62. Mitsch, W.J. and Gosselink, J.G. 1993. Wetlands. Von Nostrand Reinhold, New York, N.Y., USA.
  63. Morel, M., Meux, E., Mathieu, Y., Thuillier, A., Chibani, K., Harvengt, L., Jacquot, J.P., and Gelhaye, E. 2013. Xenomic networks variability and adaptation traits in wood decay fungi. Microb. Biotechnol. 6, 248-263. https://doi.org/10.1111/1751-7915.12015
  64. Moretto, A.S., Destel, R.A., and Diton, N.G. 2001. Decomposition and nutrient dynamic of leaf litter and roots palatable and unpalatable grasses in semi-arid grassland. Appl. Soil Ecol. 18, 31-37. https://doi.org/10.1016/S0929-1393(01)00151-2
  65. Morozova, O., Hirst, M., Marra, M.A. 2009. Applications of new sequencing technologies for transcriptome analysis. Annu. Rev. Genomics Hum. Genet. 10, 135-151. https://doi.org/10.1146/annurev-genom-082908-145957
  66. Nannipieri, P., Kandeler, E., and Ruggiero, R. 2002. Enzyme activities and microbiological and biochemical processes in soil, pp. 1-33. In Burns, I.R.G. (ed.), Enzymes in the environment. Marcel Dekker, New York, N.Y., USA.
  67. Newman, S. and Reddy, K.R. 1992. Sediment resuspension effects on alkaline phosphatase activity. Hydrobiologia 245, 75-86. https://doi.org/10.1007/BF00764767
  68. Olander, L.P. and Vitousek, P.M. 2000. Regulation of soil phosphatase and chitinase activity by N and P availability. Biochemistry 49, 175-190.
  69. Penton, C.R. and Newman, S. 2007. Enzyme activity responses to nutrient loading in subtropical wetlands. Biogeochemistry 84, 83-98. https://doi.org/10.1007/s10533-007-9106-2
  70. Pietikainen, J., Pettersson, M., and Baath, E. 2005. Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol. Ecol. 52, 49-58. https://doi.org/10.1016/j.femsec.2004.10.002
  71. Pind, A., Freeman, C., and Lock, M.A. 1994. Enzymic degradation of phenolic materials in peatlands-measurement of phenol oxidase activity. Plant Soil 159, 227-231. https://doi.org/10.1007/BF00009285
  72. Press, M.C., Henderson, J., and Lee, J.A. 1985. Arylsulphatase activity in peat in relation to acid deposition. Soil Biol. Biochem. 17, 99-103. https://doi.org/10.1016/0038-0717(85)90096-3
  73. Pulford, I.D. and Tabatabai, M.A. 1988. Effect of waterlogging on enzyme activities in soils. Soil Biol. Biochem. 20, 215-219. https://doi.org/10.1016/0038-0717(88)90039-9
  74. Raes, J., Foerstner, K.U., and Bork, P. 2007. Get the most out of your metagenome: computational analysis of environmental sequence data. Curr. Opin. Microbiol. 10, 490-498. https://doi.org/10.1016/j.mib.2007.09.001
  75. Rao, M.A., Scelza, R., Acevedo, F., Diez, M.C., and Gianfreda, L. 2014. Enzymes as useful tools for environmental purposes. Chemosphere 107, 145-162. https://doi.org/10.1016/j.chemosphere.2013.12.059
  76. Reddy, K.R. and DeLaune, R.D. 2007. Biogeochemistry of wetlands: Science and applications. Crc Press, Boca Raton, Florida, USA.
  77. Rejamankova, E. and Komarkova, J. 2000. A function of cyanobacterial mats in phosphorus-limited tropical wetlands. Hydrobiologia 431, 135-153. https://doi.org/10.1023/A:1004011318643
  78. Rejmankova, E. and Komarkova, J. 2005. Response of cyanobacterial mats to nutrient and salinity changes. Aquat. Bot. 83, 87-107. https://doi.org/10.1016/j.aquabot.2005.05.011
  79. Rojo, M.J., Carcedo, S.G., and Mateos, M.P. 1990. Distribution and characterization of phosphatase and organic phosphorus in soil fractions. Soil Biol. Biochem. 22, 169-174. https://doi.org/10.1016/0038-0717(90)90082-B
  80. Ross, D.J., Tate, K.R., Newton, P.C., and Clark, H. 2002. Decomposability of $C_3$ and $C_4$ grass litter sampled under different concentrations of atmospheric carbon dioxide at natural ${CO_2}$ spring. Plant Soil 240, 275-286. https://doi.org/10.1023/A:1015779431271
  81. Saiya-Cork, K.R., Sinsabaugh, R.L., and Zak, D.R. 2002. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34, 1309-1315. https://doi.org/10.1016/S0038-0717(02)00074-3
  82. Salvato, M., Borin, M., Doni, S., Macci, C., Ceccanti, B., Marinari, S., and Masciandaro, G. 2012. Wetland plants, microorganisms and enzymatic activities interrelations in treating N polluted water. Ecol. Eng. 47, 36-43. https://doi.org/10.1016/j.ecoleng.2012.06.033
  83. Schlesinger, W.H. 1977. Carbon balance in terrestrial detritus. Annu. Rev. Ecol. Syst. 8, 51-81. https://doi.org/10.1146/annurev.es.08.110177.000411
  84. Schothorst, C.J. 1977. Subsidence of low moor peat soils in the western Netherlands. Geoderma. 17, 265-291. https://doi.org/10.1016/0016-7061(77)90089-1
  85. Shackle, V.J., Freeman, C., and Reynolds, B. 2000. Carbon supply and the regulation of enzyme activity in constructed wetlands. Soil Biol. Biochem. 32, 1935-1940. https://doi.org/10.1016/S0038-0717(00)00169-3
  86. Sinsabaugh, R. 2010. Pehnol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol. Biochem. 42, 391-404. https://doi.org/10.1016/j.soilbio.2009.10.014
  87. Sinsabaugh, R.L. and Findlay, S. 1995. Microbial production, enzyme activity and carbon turnover in surface sediments of the Hudson River Estuary. Microb. Ecol. 30, 127-141.
  88. Sinsabaugh, R.L. and Linkins, A.E. 1993. Statistical modeling of litter decomposition from integrated cellulase activity. Ecology 74, 1594-1597. https://doi.org/10.2307/1940087
  89. Sinsabaugh, R.L. and Moorhead, D.L. 1994. Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol. Biochem. 26, 1305-1311. https://doi.org/10.1016/0038-0717(94)90211-9
  90. Snajdr, J., Cajthaml, T., Valaskova, V., Merhautova, V., Petrankova, M., Spetz, P., and Baldrian, P. 2011. Transformation of Quercus petraea litter: Successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. FEMS Microbiol. Ecol. 75, 291-303. https://doi.org/10.1111/j.1574-6941.2010.00999.x
  91. Song, Y., Song, C., Tao, B., Wang, J., Zhu, X., and Wang, X. 2014. Short-term responses of soil enzyme activities and carbon mineralization to added nitrogen and litter in a freshwater marsh of Northeast China. Eur. J. Soil Biol. 61, 72-79. https://doi.org/10.1016/j.ejsobi.2014.02.001
  92. Strakova, P., Niemi, R.M., Freeman, C., Peltoniemi, K., Toberman, H., Heiskanen, I., Fritze, H., and Laiho, R. 2011. Litter type affects the activity of aerobic decomposers in a boreal peatland more than site nutrient and water table regimes. Biogeosciences 8, 2741-2755. https://doi.org/10.5194/bg-8-2741-2011
  93. Torn, M.S., Swanston, C.W., Castanha, C., and Trumbore, S.E. 2009. Storage and turnover of organic matter in soil, pp. 219-272. In Senesi, N., Xing, B., and Huang, P.M. (ed.), Biophysicochemical processes involving natural nonliving organic matter in environmental systems. John Wiley & Sons, Hoboken, New Jersey, USA.
  94. Wallenstein, M.D. and Weintraub, M.N. 2008. Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol. Biochem. 40, 2098-2106. https://doi.org/10.1016/j.soilbio.2008.01.024
  95. Wang, L., Yin, C., Wang, W., and Shan, B. 2010. Phosphatase activity along soil C and P gradients in a reed-dominated wetland of North China. Wetland 30, 649-655. https://doi.org/10.1007/s13157-010-0055-5
  96. Weiss, M.S.U., Abele, J., Weckesser, W., Schiltz, W.E., and Schulz, G.E. 1991. Molecular architecture and electrostatic properties of a bacterial porin. Science 254, 1627-1630. https://doi.org/10.1126/science.1721242
  97. Wetzel, R.G. 1993. Humic compounds from wetlands: complexation, inactivation, and reactivation of surface-bound and extracellular enzymes. Verh Intern. Verein. Limnol. 25, 122-128.
  98. Williams, C.J., Shingara, E.A., and Yavitt, J.B. 2000. Phenol oxidase activity in peatlands in New York State: Response to summer drought and peat type. Wetlands 20, 416-421. https://doi.org/10.1672/0277-5212(2000)020[0416:POAIPI]2.0.CO;2
  99. Wilmes, P. and Bond, P.L. 2008. The dynamic genetic repertoire of microbial communities. FEMS Microbiol. Rev. 33, 109-132.
  100. Wright, A.L. and Reddy, K.R. 2001. Phosphorus loading effects on extracellular enzyme activity in Everglades wetland soils. Soil Sci. Soc. Am. J. 65, 588-595. https://doi.org/10.2136/sssaj2001.652588x
  101. Zak, D.R., Pregitzer, K.S., King, J.S., and Holmes, W.E. 2000. Elevated atmospheric ${CO_2}$, fine roots and the responses of soil microorganisms: a review and hypothesis. New Phytol. 147, 201-222. https://doi.org/10.1046/j.1469-8137.2000.00687.x
  102. Zedler, J.B. and Kercher, S. 2004. Causes and consequences of invasive plants in wetlands: opportunities, opportunists, and outcomes. Crit. Rev. Plant Sci. 23, 431-452. https://doi.org/10.1080/07352680490514673
  103. Zheng, J.Q., Han, S.J., Wang, Y., Zhang, C.G., and Li, M.H. 2010. Composition and function of microbial communities during the early decomposition stages of foliar litter exposed to elevated ${CO_2}$ concentrations. Eur. J. Soil Sci. 61, 914-925. https://doi.org/10.1111/j.1365-2389.2010.01280.x

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