Applied Microbiology and Biotechnology

, Volume 103, Issue 13, pp 5421–5433 | Cite as

Contrasting patterns and drivers of soil fungal communities in subtropical deciduous and evergreen broadleaved forests

  • Liang Chen
  • Wenhua XiangEmail author
  • Huili Wu
  • Shuai Ouyang
  • Pifeng Lei
  • Yajun Hu
  • Tida Ge
  • Jun Ye
  • Yakov Kuzyakov
Environmental biotechnology


Subtropical broadleaved forests play a crucial role in supporting terrestrial ecosystem functions, but little is known about their belowground soil fungal communities despite that they have central functions in C, N, and P cycles. This study investigated the structures and identified the drivers of soil fungal communities in subtropical deciduous and evergreen broadleaved forests, using high-throughput sequencing and FUNGuild for fungal identification and assignment to the trophic guild. Fungal richness was much higher in the deciduous than in the evergreen forest. Both forests were dominated by Ascomycota and Basidiomycota phyla, but saprophytic fungi were more abundant in the deciduous forest and ectomycorrhizal fungi predominated in the evergreen forest. Fungal communities had strong links to plant and soil properties. Specifically, plant diversity and litter biomass were the main aboveground drivers of fungal diversity and composition in the deciduous forest, while host effects were prominent in the evergreen forest. The belowground factors, i.e., soil pH, water content, and nutrients especially available P, were identified as the primary drivers of soil fungal communities in the broadleaved forests. Co-occurrence network analysis revealed assembly of fungal composition in broadleaved forest soils was non-random. The smaller modularity of the network in the deciduous forest reflects lower resistance to environment changes. Concluding, these results showed that plant community attributes, soil properties, and potential interactions among fungal functional guilds operate jointly on the divergence of soil fungal community assembly in the two broadleaved forest types.


Assembly Broadleaved forests Co-occurrence network FUNGuild High-throughput sequencing 



We would like to thank Prof. Simon Queenborough at the Yale University for his assistance with the English language and grammar editing of the manuscript. We are also grateful to all the staff of the administration office of Dashanchong Forest Park for their labor support.

Authors’ contributions

LC and WhX designed the study. HlW, SO, and LC carried out the soil sampling. LC and HlW performed the experiment and sequencing and analyzed data. LC wrote the paper, and all authors improved the manuscript.


This study was funded by the National Natural Science Foundation of China (31870431, 31570447, 41671253, and 41601272), Hunan Provincial Natural Science Foundation of China (2017JJ3372), and the Huitong Forest Ecological Station funded by the State Forestry Administration of the People’s Republic of China.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2019_9867_MOESM1_ESM.xlsx (48 kb)
ESM 1 (XLSX 47 kb)
253_2019_9867_MOESM2_ESM.pdf (437 kb)
ESM 2 (PDF 436 kb)


  1. Abarenkov K, Nilsson RH, Larsson KH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi–recent updates and future perspectives. New Phytol 186:281–285. CrossRefGoogle Scholar
  2. Awad A, Majcherczyk A, Schall P, Schröter K, Schöning I, Schrumpf M, Ehbrecht M, Boch S, Kahl T, Bauhus J, Seidel D, Ammer C, Fischer M, Kües U, Pena R (2019) Ectomycorrhizal and saprotrophic soil fungal biomass are driven by different factors and vary among broadleaf and coniferous temperate forests. Soil Biol Biochem 131:9–18. CrossRefGoogle Scholar
  3. Baldrian P (2017) Microbial activity and the dynamics of ecosystem processes in forest soils. Curr Opin Microbiol 37:128–134. CrossRefGoogle Scholar
  4. Bokulich NA, Mills DA (2013) Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microbiol 79:2519–2526. CrossRefGoogle Scholar
  5. Bol R, Julich D, Brödlin D, Siemens J, Kaiser K, Dippold MA, Spielvogel S, Zilla T, Mewes D, von Blanckenburg F, Puhlmann H, Holzmann S, Weiler M, Amelung W, Lang F, Kuzyakov Y, Feger KH, Gottselig N, Klumpp E, Missong A, Winkelmann C, Uhlig D, Sohrt J, von Wilpert K, Wu B, Hagedorn F (2016) Dissolved and colloidal phosphorus fluxes in forest ecosystems - an almost blind spot in ecosystem research. J Plant Nutr Soil Sc 179:425–438. CrossRefGoogle Scholar
  6. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure bacterial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. CrossRefGoogle Scholar
  7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. CrossRefGoogle Scholar
  8. Chen L, Xiang WH, Wu HL, Ouyang S, Zhou B, Zeng YL, Chen YL, Kuzyakov Y (2019) Tree species identity surpasses richness in affecting soil microbial richness and community composition in subtropical forests. Soil Biol Biochem 130:113–121. CrossRefGoogle Scholar
  9. Coince A, Caël O, Bach C, Lengellé J, Cruaud C, Gavory F, Morin E, Murat C, Marçais B, Buée M (2013) Below-ground fine-scale distribution and soil versus fine root detection of fungal and soil oomycete communities in a French beech forest. Fungal Ecol 6:223–235. CrossRefGoogle Scholar
  10. Condit R, Engelbrecht BMJ, Pino D, Pérez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. P Natl Acad Sci USA 110:5064–5068. CrossRefGoogle Scholar
  11. Ding JJ, Zhang YG, Wang MM, Sun X, Cong J, Deng Y, Lu H, Yuan T, Van Nostrand JD, Li DQ, Zhou JZ, Yang YF (2015) Soil organic matter quantity and quality shape microbial community compositions of subtropical broadleaved forests. Mol Ecol 24:5175–5185. CrossRefGoogle Scholar
  12. Edgar RC (2013) UPARSE: Highly accurate OUT sequences from microbial amplicon reads. Nat Methods 10:996–998. CrossRefGoogle Scholar
  13. Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199. CrossRefGoogle Scholar
  14. Gao C, Shi NN, Liu YX, Peay KG, Zheng Y, Ding Q, Mi XC, Ma KP, Wubet T, Buscot F, Guo LD (2013) Host plant genus-level diversity is the best predictor of ectomycorrhizal fungal diversity in a Chinese subtropical forest. Mol Ecol 22:3403–3414. CrossRefGoogle Scholar
  15. Gao C, Zhang Y, Shi NN, Zheng Y, Chen L, Wubet T, Bruelheide H, Both S, Buscot F, Ding Q, Erfmeier A, Kühn P, Nadrowski K, Scholten T, Guo LD (2015) Community assembly of ectomycorrhizal fungi along a subtropical secondary forest succession. New Phytol 205:771–785. CrossRefGoogle Scholar
  16. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. CrossRefGoogle Scholar
  17. Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743CrossRefGoogle Scholar
  18. Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol 26:6960–6973. CrossRefGoogle Scholar
  19. Goldmann K, Schröter K, Pena R, Schöning I, Schrumpf M, Buscot F, Polle A, Wubet T (2016) Divergent habitat filtering of root and soil fungal communities in temperate beech forests. Sci Rep-UK 6:31439. CrossRefGoogle Scholar
  20. Greenblum S, Chiu HC, Levy R, Carr R, Borenstein E (2013) Towards a predictive system-level model of the human microbiome: progress, challenges, and opportunities. Curr Opin Biotechnol 24:810–820. CrossRefGoogle Scholar
  21. Gunina A, Smith AR, Godbold D, Jones DL, Kuzyakov Y (2017) Response of soil microbial community to afforestation with pure and mixed species. Plant Soil 412:357–368. CrossRefGoogle Scholar
  22. Hackl E, Pfeffer M, Donat C, Bachmann G, Zechmeister-Boltenstern S (2005) Composition of the microbial communities in the mineral soil under different types of natural forest. Soil Biol Biochem 37:661–671. CrossRefGoogle Scholar
  23. Hannula SE, Morriën E, de Hollander M, van der Putten WH, van Veen JA, de Boer W (2017) Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture. ISME J 11:294–2304. CrossRefGoogle Scholar
  24. Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytol 17:430–440. CrossRefGoogle Scholar
  25. Jiang F, Wu XH, Xiang WH, Fang X, Zeng YL, Ouyang S, Lei PF, Deng XW, Peng CH (2017) Spatial variations in soil organic carbon, nitrogen and phosphorus concentration related to stand characteristics in subtropical areas. Plant Soil 413:289–301. CrossRefGoogle Scholar
  26. Keylock CJ (2005) Simpson diversity and the Shannon-Wiener index as special cases of a generalized entropy. Oikos 109:203–207. CrossRefGoogle Scholar
  27. Kira T (1991) Forest ecosystems of east and southeast Asia in a global perspective. Ecol Res 6:185–200. CrossRefGoogle Scholar
  28. Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal diversity composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25. CrossRefGoogle Scholar
  29. Kong Y (2011) Btrim: A fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics 98:152–153. CrossRefGoogle Scholar
  30. Kuzyakov Y, Xu XL (2013) Competition between roots and microorganisms for N: mechanisms and ecological relevance. New Phytol 198:656–669. CrossRefGoogle Scholar
  31. Lamb EG, Kennedy N, Siciliano SD (2011) Effects of plant species richness and evenness on soil microbial community diversity and function. Plant Soil 338:483–495. CrossRefGoogle Scholar
  32. Lang C, Seven J, Polle A (2011) Host preferences and differential contributions of deciduous tree species shape mycorrhizal species richness in a mixed Central European forest. Mycorrhiza 21:297–308. CrossRefGoogle Scholar
  33. Langfelder P, Horvath S (2012) Fast R functions for robust correlations and hierarchical clustering. J Stat Softw 46:1–17CrossRefGoogle Scholar
  34. Li H, Ye DD, Wang XG, Settles ML, Wang J, Hao ZQ, Zhou LS, Dong P, Jiang Y, Ma ZS (2014) Soil bacterial communities of different natural forest types in Northeast China. Plant Soil 383:203–216. CrossRefGoogle Scholar
  35. Liu C, Xiang WH, Lei P, Deng XW, Tian DL, Fang X, Peng CH (2014) Standing fine root mass and production in four Chinese subtropical forests along succession and species diversity gradient. Plant Soil 376:445–459. CrossRefGoogle Scholar
  36. Lladó S, López-Mondéjar R, Baldrian P (2018) Drivers of microbial community structure in forest soils. Appl Microbiol Biotechnol 102:4331–4338. CrossRefGoogle Scholar
  37. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. CrossRefGoogle Scholar
  38. Mehlich A (1984) Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun Soil Sci Plant 15:1409–1416CrossRefGoogle Scholar
  39. Montoya JM, Pimm SL, Solé RV (2006) Ecological networks and their fragility. Nature 442:259–264. CrossRefGoogle Scholar
  40. Nguyen NH, Song ZW, Bates ST, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016a) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. CrossRefGoogle Scholar
  41. Nguyen NH, Williams LJ, Vincent JB, Stefanski A, Cavender-Bares J, Messier C, Paquette A, Gravel D, Reich PB, Kennedy PC (2016b) Ectomycorrhizal fungal diversity and saprotrophic fungal diversity are linked to different tree community attributes in a field-based tree experiment. Mol Ecol 25:4032–4046. CrossRefGoogle Scholar
  42. Osona T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974. CrossRefGoogle Scholar
  43. Ouyang S, Xiang WH, Wang XP, Zeng YL, Lei PF, Deng XW, Peng CH (2016) Significant effects of biodiversity on forest biomass during the succession of subtropical forest in south China. Forest Ecol Manag 372:291–302. CrossRefGoogle Scholar
  44. Peay KG, Baraloto C, Fine PVA (2013) Strong coupling of plant and fungal community structure across western Amazonian rainforests. ISME J 7:1852–1861. CrossRefGoogle Scholar
  45. Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. Forest Ecol Manag 309:19–27. CrossRefGoogle Scholar
  46. Schappe T, Albornoz FE, Turner BL, Neat A, Condit R, Jones FA (2017) The role of soil chemistry and plant neighbourhoods in structuring fungal communities in three Panamanian rainforests. J Ecol 105:569–579. CrossRefGoogle Scholar
  47. Schröter K, Wembeuer B, Pena R, Schöning I, Ehbrecht M, Schall P, Ammer C, Daniel R, Polle A (2018) Assembly processes of trophic guilds in the root mycobiome of temperate forests. Mol Ecol 28:348–364. CrossRefGoogle Scholar
  48. Stock S, Köster M, Dippold MA, Nájera F, Matus F, Merino C, Boy J, Spielvogel S, Gorbushina A, Kuzyakov Y (2019) Environmental drivers and stoichiometric constraints on enzyme activities in soils from rhizosphere to continental scales. Geoderma 337:973–982. CrossRefGoogle Scholar
  49. Su JQ, Ding LJ, Xue K, Yao HY, Quensen J, Bai SJ, Wei WX, Wu JS, Zhou JZ, Tiedje JM, Zhu YG (2015) Long-term balanced fertilization increase the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol 24:136–150. CrossRefGoogle Scholar
  50. Sun RB, Dsouza M, Gilbert JA, Guo XS, Wang DZ, Guo ZB, Ni YY, Chu HY (2016) Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ Microbiol 18:5137–5150. CrossRefGoogle Scholar
  51. Tedersoo L, Bahram M, Cajthaml T, Põlme S, Hiiesalu I, Anslan S, Harend H, Buegger F, Pritsch K, Koricheva J, Abarenkov K (2016) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346–362. CrossRefGoogle Scholar
  52. Tilman D (1982) Resource competition and community structure. Monogr Popul Biol 17:1–296Google Scholar
  53. Toju H, Kishida O, Katayama N, Takagi K (2016) Networks depicting the fine-scale co-occurrences of fungi in soil horizons. PLoS One 11:e0165987. CrossRefGoogle Scholar
  54. Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370. CrossRefGoogle Scholar
  55. Uroz S, Buée M, Deveau A, Mieszkin S, Martin F (2016) Ecology of the forest microbiome: highlights of temperate and boreal ecosystems. Soil Biol Biochem 103:471–488. CrossRefGoogle Scholar
  56. Van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microorganisms as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. CrossRefGoogle Scholar
  57. Villar R, Robleto JR, de Jong Y, Poorter H (2006) Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant Cell Environ 29:1629–1643. CrossRefGoogle Scholar
  58. Voríšková J, Baldrian P (2013) Fungal community on decomposing leaf litter undergoes rapid successional changes. ISME J 7:477–486. CrossRefGoogle Scholar
  59. Waldrop MP, Zak DR, Blackwood CB, Curtis CD, Tilman D (2006) Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9:1127–1135. CrossRefGoogle Scholar
  60. Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils-effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–264. CrossRefGoogle Scholar
  61. Wang Q, Wang C, Yu WW, Turak A, Chen DW, Huang Y, Ao JH, Jiang Y, Huang ZR (2018) Effects of nitrogen and phosphorus inputs on soil bacterial abundance, diversity, and community composition in Chinese fir plantations. Front Microbiol 9:1543. CrossRefGoogle Scholar
  62. Wei XM, Hu YJ, Razavi BS, Zhou J, Shen JL, Nannipieri P, Wu JS, Ge TD (2019) Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization. Soil Biol Biochem 131:62–70. CrossRefGoogle Scholar
  63. Widder S, Besemer K, Singer GA, Ceola S, Bertuzzo E, Quince C, Sloan WT, Rinaldo A, Battin TJ (2014) Fluvial network organization imprints on microbial co-occurrence networks. P Natl Acad Sci USA 111:12799–12804. CrossRefGoogle Scholar
  64. Williams-Linera G (1997) Phenology of deciduous and broadleaved-evergreen tree species in a Mexican tropical lower montane forest. Glob Ecol Biogeogr Lett 6:115–127. CrossRefGoogle Scholar
  65. Wubet T, Christ S, Schöning I, Boch S, Gawlich M, Schnabel B, Fischer M, Buscot F (2012) Differences in soil fungi communities between European beech (Fagus sylvatica L.) dominated forests are related to soil and understory vegetation. PLoS One 7:e47500. CrossRefGoogle Scholar
  66. Xiang WH, Liu SH, Lei XD, Frank SC, Tian DL, Wang GJ, Deng XW (2013) Secondary forest floristic composition, structure, and spatial pattern in subtropical China. J Forest Res 18:111–120. CrossRefGoogle Scholar
  67. Xiang WH, Zhou J, Ouyang S, Zhang SL, Lei PF, Li JX, Deng XW, Fang X, Forrester DI (2016) Species-specific and general allometric equating tree biomass components of subtropical forests in southern China. Eur J Forest Res 135:963–979. CrossRefGoogle Scholar
  68. Xue L, Ren HD, Li S, Leng XH, Yao XH (2017) Soil bacterial community structure and co-occurrence pattern during vegetation restoration in Karst rocky desertification area. Front Microbiol 8:2377. CrossRefGoogle Scholar
  69. Yang JK, Zhang JJ, Yu HY, Cheng JW, Miao LH (2014) Community composition and cellulase activity of cellulolytic bacteria from forest soils planted with broad-leaved deciduous and evergreen trees. Appl Microbiol Biotechnol 98:449–1458. Google Scholar
  70. Yang T, Adams JM, Shi Y, He JS, Jing X, Chen LT, Tedersoo L, Chu HY (2017a) Soil fungal diversity in natural grasslands of the Tibetan Plateau: associations with plant diversity and productivity. New Phytol 215:756–765. CrossRefGoogle Scholar
  71. Yang Y, Dou YX, Huang YM, An SS (2017b) Links between soil fungal diversity and plant and soil properties on the Loess Plateau. Front Microbiol 8:2198. CrossRefGoogle Scholar
  72. Yu GR, Chen Z, Piao SL, Peng CH, Ciais P, Wang QF, Li XR, Zhu XJ (2014) High carbon dioxide uptake by subtropical forest ecosystems in the East Asian monsoon region. P Natl Acad Sci USA 111:4910–4915. CrossRefGoogle Scholar
  73. Zhou JZ, Deng Y, Luo F, He ZL, Tu QC, Zhi XY (2010) Functional molecular ecological networks. mBio 1:e00169–e00110. Google Scholar
  74. Zhu ZK, Ge TD, Luo Y, Liu SL, Xu XL, Tong CL, Shibistova O, Guggenberger G, Wu JS (2018) Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biol Biochem 121:67–76. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Faculty of Life Science and TechnologyCentral South University of Forestry and TechnologyChangshaChina
  2. 2.Huitong National Station for Scientific Observation and Research of Chinese Fir Plantation Ecosystems in Hunan ProvinceHuaihuaChina
  3. 3.Key Laboratory of Agro-ecological Processes in Subtropical Regions, Changsha Research Station for Agricultural & Environmental Monitoring, Institute of Subtropical AgricultureChinese Academy of SciencesChangshaChina
  4. 4.Australian Centre for EcogenomicsThe University of QueenslandSt. LuciaAustralia
  5. 5.Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil ScienceUniversity of GoettingenGöttingenGermany
  6. 6.Institute of Physicochemical and Biological Problems in Soil ScienceRussian Academy of SciencesPushchinoRussia

Personalised recommendations