, Volume 15, Issue 4, pp 624–636 | Cite as

Relationships Between Soil Microorganisms, Plant Communities, and Soil Characteristics in Chinese Subtropical Forests

  • Yu Ting WuEmail author
  • Jessica Gutknecht
  • Karin Nadrowski
  • Christian Geißler
  • Peter Kühn
  • Thomas Scholten
  • Sabine Both
  • Alexandra Erfmeier
  • Martin Böhnke
  • Helge Bruelheide
  • Tesfaye Wubet
  • François Buscot


We analyzed the influence of above- and belowground factors on the soil microbial community in a Chinese subtropical forest, one of the most diverse biomes in the northern hemisphere. Soil samples were taken at different depths from four replicate comparative study plots in each of three forest age classes (young 10–40 years, medium 40–80 years, old ≥80 years). Microbial biomass and community structure were then determined using phospholipid fatty acid (PLFA) analysis, and basal respiration and microbial biomass carbon (Cmic) were determined by substrate-induced respiration. These data were then related to plant community and soil variables using non-metric multidimensional scaling analysis and post-hoc permutational correlations. We found that microbial lipid composition and abundance were not related to forest age class. Instead, microbial lipid composition and abundance were related to factors reflecting primary production, i.e., percent litter cover, percent dead wood cover, and percent tree layer cover. Specifically, the relative abundance (mol fraction) of indicators for arbuscular mycorrhizal fungi, Gram-positive and Gram-negative bacteria were positively significantly correlated with percent litter cover. We also found that the biomass of all microbial groups and total PLFA were negatively significantly related to percent deadwood cover. In addition, \( {\text{pH}}_{{{\text{H}}_{ 2} {\text{O}}}} \) was the only soil parameter that was correlated significantly to microbial biomass. Our results indicate that overarching ecological factors such as plant productivity and soil pH are important factors influencing the soil microbial community, both in terms of biomass and of community composition in this subtropical ecosystem.


BEF-China PLFA SIR NMDS analysis subtropical forests microbial biomass 



We are grateful to the staff of the Gutianshan NNR and the students Bo Tong and Bo Yang for their field assistance. We also thank Annette Gurenowitz for the help with lipid analysis and Wenzel Kröber for providing leaf trait data. Funding for the project was mainly received from the German Research Foundation (DFG) (Grant BU 941/12-1 in the Research Unit FOR 891/1) and additionally from the Helmholtz Impulse and Networking Fund through the Helmholtz Interdisciplinary Graduate School for Environmental Research (HIGRADE).

Supplementary material

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Supplementary material 1 (DOC 329 kb)


  1. Boden Ad-hoc-AG. 2005. Bodenkundliche kartieranleitung. 5th edn. Hannover: Bundesanstalt für Geowissenschaft-en und Rohstoffe. p 438.Google Scholar
  2. Alexander I, Lee SS. 2005. Mycorrhizas and ecosystem processes in tropical rain forest: implications for diversity. In: Burslem DFRP, Pinard MA, Hartley SE, Eds. Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge: Cambridge University Press. p 165–203.CrossRefGoogle Scholar
  3. Anderson JPE, Domsch KH. 1973. Quantification of bacterial and fungal contributions to soil respiration. Arch Microbiol 93:113–27.CrossRefGoogle Scholar
  4. Anderson JPE, Domsch KH. 1978. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–21.CrossRefGoogle Scholar
  5. Anderson TH. 1985. Determination of ecophysiological maintenance carbon requirements of soil microorganisms in a dormant state. Biol Fertil Soils 1:81–9.CrossRefGoogle Scholar
  6. Anderson TH, Domsch KH. 1990. Application of eco-physiological quotients (qCO2 and qD) on microbial biomasses from soils of different cropping histories. Soil Biol Biochem 22:251–5.CrossRefGoogle Scholar
  7. Anderson TH. 2003. Microbial eco-physiological indicators to assess soil quality. Agric Ecosyst Environ 98:285–93.CrossRefGoogle Scholar
  8. Bååth E, Anderson TH. 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–63.CrossRefGoogle Scholar
  9. Bååth E. 2003. The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Microb Ecol 45:373–83.PubMedCrossRefGoogle Scholar
  10. Balser TC, Treseder KK, Eklener M. 2005. Using lipid analysis and hyphal length to quantify AM and saprotrophic fungal abundance along a soil chronosequence. Soil Biol Biochem 37:601–4.CrossRefGoogle Scholar
  11. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B. 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–56.PubMedCrossRefGoogle Scholar
  12. Bardgett RD, Freeman C, Ostle NJ. 2008. Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–14.PubMedCrossRefGoogle Scholar
  13. Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T. 2005. Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect Plant Ecol Evol Syst 7:27–49.CrossRefGoogle Scholar
  14. Bausenwein U, Gattinger A, Langer U, Embacher A, Hartmann HP, Sommer M, Munch JC, Schloter M. 2008. Exploring soil microbial communities and soil organic matter: variability and interactions in arable soils under minimum tillage practice. Appl Soil Ecol 40:67–77.CrossRefGoogle Scholar
  15. Bezemer TM, Fountain MT, Barea JM, Christensen S, Dekker SC, Duyts H, van Hal R, Harvey JA, Hedlund K, Maraun M, Mikola J, Mladenov AG, Robin C, de Ruiter PC, Scheu S, Setälä H, Šmilauer P, van der Putten WH. 2010. Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects. Ecology 91:3027–36.PubMedCrossRefGoogle Scholar
  16. Binkley D, Giardina C. 1998. Why do tree species affect soils? The warp and woof of tree-soil interactions. Biogeochemistry 42:89–106.CrossRefGoogle Scholar
  17. Bligh E, Dyer W. 1959. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–17.PubMedCrossRefGoogle Scholar
  18. Both S, Fang T, Böhnke M, Bruelheide H, Geißler C, Kühn P, Scholten T, Trogisch S, Erfmeier A. 2011. Lack of tree layer control on herb layer characteristics in a subtropical forest, China. J Veg Sci. doi: 10.1111/j.1654-1103.2011.01324.x.
  19. Bossio DA, Scow KM, Gunapala N, Graham KJ. 1998. Determinants of soil microbial communities: effects of agricultural management, Season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12.PubMedCrossRefGoogle Scholar
  20. Boyle SA, Yarwood RR, Bottomley PJ, Myrold DD. 2008. Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon. Soil Biol Biochem 40:443–51.CrossRefGoogle Scholar
  21. Bruelheide H, Böhnke M, Both S, Fang T, Assmann T, Baruffol M, Bauhus J, Buscot F, Chen XY, Ding BY, Durka W, Erfmeier A, Fischer M, Geißler C, Guo DL, Härdtle W, He JS, Hector A, Kröber W, Kühn P, Lang AC, Nadrowski K, Pei KQ, Scherer-Lorenzen M, Shi XZ, Scholten T, Schuldt A, Trogisch S, von Oheimb G, Welk E, Wirth C, Wu YT, Yang XF, Zeng XQ, Zhang SR, Zhou HZ, Ma KP, Schmid B. 2011. Community assembly during secondary forest succession in a Chinese subtropical forest. Ecol Monogr 81:25–41.CrossRefGoogle Scholar
  22. Cannell MGR. 1984. Woody biomass of forest stands. For Ecol Manage 8:299–312.CrossRefGoogle Scholar
  23. Carney KM, Matson PA. 2005. Plant communities, soil microorganisms, and soil carbon cycling: does altering the world belowground matter to ecosystem functioning? Ecosystems 8:928–40.CrossRefGoogle Scholar
  24. Carney KM, Matson PA. 2006. The influence of tropical plant diversity and composition on soil microbial communities. Microb Ecol 52:226–38.PubMedCrossRefGoogle Scholar
  25. Clausen CA. 1996. Bacterial associations with decaying wood: a review. Int Biodeterior Biodegradation 37:101–7.CrossRefGoogle Scholar
  26. Cornwell WK, Cornelissen JHC, Allison SD, Bauhus J, Eggleton P, Preston CM, Scarff F, Weedon JT, Wirth C, Zanne AE. 2009. Plant traits and wood fates across the globe: rotted, burned, or consumed? Glob Change Biol 15:2431–49.CrossRefGoogle Scholar
  27. FAO. 2006. Guidelines for soil description. 4th edn. Rome: FAO.Google Scholar
  28. Fierer N, Schime JP, Holden PA. 2003. Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–76.CrossRefGoogle Scholar
  29. Fraterrigo JM, Balser TC, Turner MG. 2006. Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87:570–9.PubMedCrossRefGoogle Scholar
  30. Fritze H, Smolander A, Levula T, Kitunen V, Mälkönen E. 1994. Wood-ash fertilization and fire treatment in a Scots pine forest stand: effects on the organic layer, microbial biomass, and microbial activity. Biol Fertil Soils 17:57–63.CrossRefGoogle Scholar
  31. Frostegård Å, Tunlid A, Bååth E. 1991. Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods 14:151–63.CrossRefGoogle Scholar
  32. Frostegård Å, Bååth E, Tunlid A. 1993. Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–30.CrossRefGoogle Scholar
  33. Frostegård A, Bååth E. 1996. The use of fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65.CrossRefGoogle Scholar
  34. Geißler C, Kühn P, Böhnke M, Bruelheide H, Shi X, Scholten T. 2011. Splash erosion potential under tree canopies in subtropical SE China. Catena 174:596–601.Google Scholar
  35. Gershenson A, Bader NE, Cheng WX. 2009. Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Glob Change Biol 15:176–83.CrossRefGoogle Scholar
  36. Groffman PM, Eagan P, Sullivan WM, Lemunyon JL. 1996. Grass species and soil type effects on microbial biomass and activity. Plant Soil 183:61–7.CrossRefGoogle Scholar
  37. Gutknecht JLM, Field CB, Balser TC. 2012. Microbial response to simulated global change: temporal patterns as an important context. Glob Change Biol (In press).Google Scholar
  38. Heinemeyer O, Insam H, Kaiser EA, Walenzik G. 1989. Soil microbial biomass and respiration measurements: an automated technique based on infra-red analysis. Plant Soil 116:191–5.CrossRefGoogle Scholar
  39. Hernesmaa A, Björklöf K, Kiikkila O, Fritze H, Haahtela K, Romantschuk M. 2005. Structure and function of microbial communities in the rhizosphere of Scots pine after tree-felling. Soil Biol Biochem 37:777–85.CrossRefGoogle Scholar
  40. Hill TCJ, McPherson EF, Harris JA, Birch P. 1993. Microbial biomass estimated by phospholipid phosphate in soils with diverse microbial communities. Soil Biol Biochem 25:1779–86.CrossRefGoogle Scholar
  41. Hodge A, Campbell CD, Fitter AH. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–9.PubMedCrossRefGoogle Scholar
  42. Högberg MN, Högberg P, Myrold DD. 2007. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590–601.Google Scholar
  43. Hooper DU, Vitousek PM. 1997. The effects of plant composition and diversity on ecosystem processes. Science 277:1302–5.CrossRefGoogle Scholar
  44. Hooper DU, Bignell DE, Brown VK, Brussaard L, Dangerfield JM, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, Van der Putten WH, De Ruiter PC, Rusek J, Silver WL, Tiedje JM, Wolters V. 2000. Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience 50:1049–61.CrossRefGoogle Scholar
  45. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35.CrossRefGoogle Scholar
  46. Hu ZH, Yu MJ. 2008. Study on successions sequence of evergreen broad-leaved forest in Gutian Mountain of Zhejiang, Eastern China: species diversity. Front Biol China 3:45–9.CrossRefGoogle Scholar
  47. Ingham RE, Trofymow JA, Ingham ER, Coleman DC. 1985. Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol Monogr 55:119–40.CrossRefGoogle Scholar
  48. IUSS Working Group WRB. 2007. World reference base for soil resources 2006. First update 2007. World Soil Resources Reports No. 103. FAO, Rome.Google Scholar
  49. Johnson D, Booth RE, Whiteley AS, Bailey MJ, Read DJ, Grime JP, Leake JR. 2003. Plant community composition affects the biomass, activity, and diversity of microorganisms in limestone grassland soil. Eur J Soil Sci 54:671–7.CrossRefGoogle Scholar
  50. Kao-Kniffin J, Balser TC. 2008. Soil fertility and the impact of exotic invasion on microbial communities in Hawaiian forests. Microb Ecol 56:55–63.PubMedCrossRefGoogle Scholar
  51. Kier G, Mutke J, Dinerstein E, Ricketts TH, Küper W, Kreft H, Barthlott W. 2005. Global patterns of plant diversity and floristic knowledge. J Biogeogr 32:1107–16.CrossRefGoogle Scholar
  52. Langer U, Klimanek EM. 2006. Soil microbial diversity of four German long-term field experiments. Arch Agron Soil Sci 52:507–23.CrossRefGoogle Scholar
  53. Langer U, Rinklebe J. 2009. Lipid biomarkers for assessment of microbial communities in floodplain soils of the Elbe River (Germany). Wetlands 29:353–62.CrossRefGoogle Scholar
  54. Legendre P, Mi XC, Ren HB, Ma KP, Yu MJ, Sun IF, He FL. 2009. Partitioning beta diversity in a subtropical broad-leaved forest of China. Ecology 90:663–74.PubMedCrossRefGoogle Scholar
  55. Mao DM, Min YW, Yu LL, Martens R, Insam H. 1992. Effect of afforestation on microbial biomass and activity in soils of tropical China. Soil Biol Biochem 24:865–72.CrossRefGoogle Scholar
  56. McSpadden Gardener B, Lilley A. 1997. Application of common statistical tools. In: Elsas J, van Trevors J, Wellington E, Eds. Modern soil microbiology. New York: Marcel Dekker Inc. p 501–24.Google Scholar
  57. McTiernan KB, Ineson P, Coward PA. 1997. Respiration and nutrient release from tree leaf litter mixtures. Oikos 78:527–38.CrossRefGoogle Scholar
  58. Melero S, Porras JCR, Herencia JF, Madejon E. 2006. Chemical and biochemical properties in a silty loam soil under conventional and organic management. Soil Tillage Res 90:162–70.CrossRefGoogle Scholar
  59. Moore-Kucera J, Dick RP. 2008. PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb Ecol 55:500–11.PubMedCrossRefGoogle Scholar
  60. McCune B, Grace JB. 2002. Analysis of ecological communities. Gleneden Beach (OR): MjM Software Design.Google Scholar
  61. Nottingham AT, Griffiths H, Chamberlain PM, Stott AW, Tanner EVJ. 2009. Soil priming by sugar and leaf-litter substrates: a link to microbial groups. Appl Soil Ecol 42:183–90.CrossRefGoogle Scholar
  62. Oksanen J, Kinddt R, Legendre P, O′Hara B. 2006. Vegan: community ecology package.
  63. Olsson PA. 1999. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–10.CrossRefGoogle Scholar
  64. Pennanen T, Liski J, Bååth E, Kitunen V, Uotila J, Westman CJ, Fritze H. 1999. Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38:168–79.PubMedCrossRefGoogle Scholar
  65. Polit JI, Brown S. 1996. Mass and nutrient content of dead wood in a central Illinois floodplain forest. Wetlands 16:488–94.CrossRefGoogle Scholar
  66. Porazinska DL, Bardgett RD, Blaauw MB, Hunt HW, Parsons AN, Seastedt TR, Wall DH. 2003. Relationships at the aboveground-belowground interface: plants, soil biota and soil processes. Ecology 73:377–95.Google Scholar
  67. Prosser JI, Bohannan BJM, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, Green JL, Green LE, Killham K, Lennon JJ, Osborn AM, Solan M, van der Gast CJ, Young JPW. 2007. The role of ecological theory in microbial ecology. Nat Rev Microbiol 5:384–92.PubMedCrossRefGoogle Scholar
  68. Ramette A. 2007. Multivariate analysis in microbial ecology. FEMS Microbiol Ecol 62:142–60.PubMedCrossRefGoogle Scholar
  69. R Development Core Team. 2008. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  70. Rinklebe J, Langer U. 2006. Microbial diversity in three floodplain soils at the Elbe River (Germany). Soil Biol Biochem 38:2144–51.CrossRefGoogle Scholar
  71. Saetre P. 1999. Spatial patterns of ground vegetation, soil microbial biomass and activity in a mixed spruce-birch stand. Ecography 22:183–92.CrossRefGoogle Scholar
  72. Scherer-Lorenzen M, Bonilla JL, Potvin C. 2007. Tree species richness affects litter production and decomposition rates in a tropical biodiversity experiment. Oikos 116:2108–24.CrossRefGoogle Scholar
  73. Schimel JP, Bennett J. 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602.CrossRefGoogle Scholar
  74. Smithwick EAH, Turner MG, Metzger KL, Balser TC. 2005. Variation in NH4 + mineralization and microbial communities with stand age in lodgepole pine (Pinus contorta) forests, Yellowstone National Park (USA). Soil Biol Biochem 37:1546–59.CrossRefGoogle Scholar
  75. Steenwerth KL, Jackson LE, Calderón FJ, Stromberg MR, Scow KM. 2003. Soil microbial lipid composition and land use history in cultivated and grassland ecosystems of coastal California. Soil Biol Biochem 35:489–500.CrossRefGoogle Scholar
  76. Ushio M, Wagai R, Balser TC, Kitayama K. 2008. Variations in the soil microbial community composition of a tropical montane forest ecosystem: does tree species matter? Soil Biol Biochem 40:2699–702.CrossRefGoogle Scholar
  77. Vestal JR, White DC. 1989. Lipid analysis in microbial ecology quantitative approaches to the study of microbial communities. Bioscience 39:535–41.PubMedCrossRefGoogle Scholar
  78. Waldrop MP, Balser TC, Firestone MK. 2000. Linking microbial lipid composition to function in a tropical soil. Soil Biol Biochem 32:1837–46.CrossRefGoogle Scholar
  79. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH. 2004. Ecological linkages between aboveground and belowground biota. Science 304:1629–33.PubMedCrossRefGoogle Scholar
  80. Whelan MJ, Anderson JM. 1996. Modeling spatial patterns of throughfall and interception loss in a Norway spruce (Picea abies) plantation at the plot scale. J Hydrol 186:335–54.CrossRefGoogle Scholar
  81. White DC, Davis WM, Nickels JS, King JD, Bobbie RJ. 1979. Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62.CrossRefGoogle Scholar
  82. Wilkinson SC, Anderson JM. 2001. Spatial patterns of soil microbial communities in a Norway spruce (Picea abies) plantation. Microb Ecol 42:248–55.PubMedCrossRefGoogle Scholar
  83. Wilkinson SC, Anderson JM, Scardelis SP, Tisiafouli M, Taylor A, Wolters V. 2002. PLFA profiles of microbial communities in decomposing conifer litters subject to moisture stress. Soil Biol Biochem 34:189–200.CrossRefGoogle Scholar
  84. Wu YP, Ding N, Wang G, Xu JM, Wu JJ, Brookes PC. 2009. Effects of different soil weights, storage times and extraction methods on soil phospholipid fatty acid analyses. Geoderma 150:171–8.CrossRefGoogle Scholar
  85. Yang JC, Insam H. 1991. Microbial biomass and relative contributions of bacteria and fungi in soil beneath tropical rain forest, Hainan Island, China. J Trop Ecol 7:385–93.CrossRefGoogle Scholar
  86. Yeates GW. 1999. Effects of plants on nematode community structure. Annu Rev Phytopathol 37:127–49.PubMedCrossRefGoogle Scholar
  87. Zak DR, Tilman D, Parmenter RR, Rice CW, Fisher FM, Vose J, Milchunas D, Martin CW. 1994. Plant production and soil microorganisms in late-successional ecosystems: a continental-scale study. Ecology 75:2333–47.CrossRefGoogle Scholar
  88. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D. 2003. Plant diversity, microbial communities, and ecosystem function: are there any links? Ecology 84:2042–50.CrossRefGoogle Scholar
  89. Zelles L, Bai QY, Beck T, Beese F. 1992. Signature fatty acids in phospholipids and lipopolysaccharides as indicators of microbial biomass and community structure in agricultural soils. Soil Biol Biochem 24:317–23.CrossRefGoogle Scholar
  90. Zhang QH, Zak JC. 1995. Effects of gap size on litter decomposition and microbial activity in a subtropical forest. Ecology 76:2196–204.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Yu Ting Wu
    • 1
    • 2
    Email author
  • Jessica Gutknecht
    • 1
  • Karin Nadrowski
    • 3
  • Christian Geißler
    • 4
  • Peter Kühn
    • 4
  • Thomas Scholten
    • 4
  • Sabine Both
    • 5
  • Alexandra Erfmeier
    • 5
  • Martin Böhnke
    • 5
  • Helge Bruelheide
    • 5
  • Tesfaye Wubet
    • 1
  • François Buscot
    • 1
    • 2
  1. 1.Department of Soil EcologyUFZ-Helmholtz Centre for Environmental ResearchHalle (Saale)Germany
  2. 2.Group of Terrestrial Ecology, Institute of BiologyUniversity of LeipzigLeipzigGermany
  3. 3.Group of Special Botany and Functional Biodiversity, Institute of BiologyUniversity of LeipzigLeipzigGermany
  4. 4.Department of Physical Geography and Soil ScienceUniversity of TübingenTübingenGermany
  5. 5.Department of Biology and GeobotanyMartin Luther University Halle-WittenbergHalle (Saale)Germany

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