Abstract
Aims
The objective of this study was to analyze the responses of the soil fungal community to the afforestation of cropland with single and mixed tree species.
Methods
We investigated changes in soil fungal community composition, diversity, structure and functional groups in the topsoil (0–20 cm) following afforestation. Six forest types were analyzed in this study: Robinia pseudoacacia (RP), Platycladus orientalis (PO), Pinus tabuliformis (PT), Robinia pseudoacacia + Platycladus orientalis (RPPO), Robinia pseudoacacia + Pinus tabuliformis (RPPT), and Platycladus orientalis + Pinus tabuliformis (POPT).
Results
Soil fungal community composition and diversity significantly varied among cropland and forestland samples. Afforestation generally reduced soil fungal diversity and altered functional groups, and these variations were mainly mediated by tree species. Rare genera play an important role in the soil fungal network among cropland and forestland samples. Soil available phosphorus (AP) explained the largest portion of the variance in the soil fungal community. Soil available nutrients and microclimate were significantly associated with soil fungal diversity and richness.
Conclusions
Our observations indicate that afforestation of cropland fundamentally restructures soil fungal community composition, structure, diversity and functional groups. Nutrient availability was a principal factor regulating fungal community composition following afforestation.
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References
A’Bear AD, Jones TH, Kandeler E, Boddy L (2014) Interactive effects of temperature and soil moisture on fungal-mediated wood decomposition and extracellular enzyme activity. Soil Biol Biochem 70:151–158. https://doi.org/10.1016/j.soilbio.2013.12.017
Adamczyk B, Sietio OM, Biasi C, Heinonsalo J (2019) Interaction between tannins and fungal necromass stabilizes fungal residues in boreal forest soils. New Phytol 223:16–21. https://doi.org/10.1111/nph.15729
Asplund J, Kauserud H, Ohlson M, Nybakken L (2019) Spruce and beech as local determinants of forest fungal community structure in litter, humus and mineral soil. FEMS Microbiol Ecol 95. https://doi.org/10.1093/femsec/fiy232
Bastian M, Heymann S, Jacomy M (2009) Gephi: An open source software for exploring and manipulating networks. In: International conference on weblogs and social media
Bokulich NA, Mills DA (2013) Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microb 79:2519–2526. https://doi.org/10.1128/Aem.03870-12
Bray SR, Kitajima K, Mack MC (2012) Temporal dynamics of microbial communities on decomposing leaf litter of 10 plant species in relation to decomposition rate. Soil Biol Biochem 49:30–37. https://doi.org/10.1016/j.soilbio.2012.02.009
Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Castano C et al (2018) Soil microclimate changes affect soil fungal communities in a Mediterranean pine forest. New Phytol 220:1211–1221. https://doi.org/10.1111/nph.15205
Chavez-Vergara B, Rosales-Castillo A, Merino A, Vazquez-Marrufo G, Oyama K, Garcia-Oliva F (2016) Quercus species control nutrients dynamics by determining the composition and activity of the forest floor fungal community. Soil Biol Biochem 98:186–195. https://doi.org/10.1016/j.soilbio.2016.04.015
Csardi G, Nepusz TJI (2006) The igraph software package for complex network research. Int J Complex Syst 1695. http://igraph.org
Doelman JC et al (2020) Afforestation for climate change mitigation: Potentials, risks and trade-offs. Global Change Biol 26:1576–1591. Doi:https://doi.org/10.1111/gcb.14887
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Fiegna F, Moreno-Letelier A, Bell T, Barraclough TG (2015) Evolution of species interactions determines microbial community productivity in new environments. ISME J 9(5):1235–1245. https://doi.org/10.1038/ISMEJ.2014.215
Gilliam FS (2014) The herbaceous layer in forests of eastern North America. Oxford University Press, Oxford
Guimera R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433(7028):895–900. https://doi.org/10.1038/nature03288
Gunina A, Smith AR, Godbold DL, Jones DL, Kuzyakov Y (2017) Response of soil microbial community to afforestation with pure and mixed species. Plant Soil 412:357–368. https://doi.org/10.1007/s11104-016-3073-0
He D, Shen W, Eberwein J, Zhao Q, Ren L, Wu QL (2017) Diversity and co-occurrence network of soil fungi are more responsive than those of bacteria to shifts in precipitation seasonality in a subtropical forest. Soil Biol Biochem 115:499–510. https://doi.org/10.1016/j.soilbio.2017.09.023
Jousset A et al (2017) Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J 11(4):853–862
Kang HZ, Gao HH, Yu WJ, Yi Y, Wang Y, Ning ML (2018) Changes in soil microbial community structure and function after afforestation depend on species and age: Case study in a subtropical alluvial island. Sci Total Environ 625:1423–1432. https://doi.org/10.1016/j.scitotenv.2017.12.180
Keeney D, Nelson D, Page A (1982) Methods of soil analysis. Part. 2. Chemical and microbiological properties. Black CA et al. (eds). pp 711–733
Li Y, Li Y, Chang SX, Liang X, Qin H, Chen J, Xu Q (2017) Linking soil fungal community structure and function to soil organic carbon chemical composition in intensively managed subtropical bamboo forests. Soil Biol Biochem 107:19–31. https://doi.org/10.1016/j.soilbio.2016.12.024
Li J, Delgado-Baquerizo M, Wang JT, Hu HW, Cai ZJ, Zhu YN, Singh BK (2019) Fungal richness contributes to multifunctionality in boreal forest soil. Soil Biol Biochem 136. https://doi.org/10.1016/j.soilbio.2019.107526
Liu J et al (2015) Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Biol Biochem 83:29–39. https://doi.org/10.1016/j.soilbio.2015.01.009
Liu J, Dang P, Gao Y, Zhu H, Zhu H, Zhao F, Zhao Z (2018) Effects of tree species and soil properties on the composition and diversity of the soil bacterial community following afforestation. For Ecol Manag 427:342–349. https://doi.org/10.1016/j.foreco.2018.06.017
Liu JL, Yang ZL, Dang P, Zhu HL, Gao Y, Ha VN, Zhao Z (2018b) Response of soil microbial community dynamics to Robinia pseudoacacia L. afforestation in the loess plateau: a chronosequence approach. Plant Soil 423:327–338. https://doi.org/10.1007/s11104-017-3516-2
Long D, Liu J, Han Q, Wang X, Huang J (2016) Ectomycorrhizal fungal communities associated with Populus simonii and Pinus tabuliformis in the hilly-gully region of the Loess Plateau, China. Sci rep 6:24336. https://doi.org/10.1038/srep24336
Lundberg DS et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-86+. https://doi.org/10.1038/nature11237
Lynch MD, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13(4):217–229. https://doi.org/10.1038/nrmicro3400
McGee KM, Eaton WD, Shokralla S, Hajibabaei M (2019) Determinants of soil bacterial and fungal community composition toward carbon-use efficiency across primary and secondary forests in a costa rican conservation area. Microb Ecol 77:148–167. https://doi.org/10.1007/s00248-018-1206-0
Morrison EW, Frey SD, Sadowsky JJ, van Diepen LTA, Thomas WK, Pringle A (2016) Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest. Fungal Ecol 23:48–57. https://doi.org/10.1016/j.funeco.2016.05.011
Nagati M, Roy M, Manzi S, Richard F, Desrochers A, Gardes M, Bergeron Y (2018) Impact of local forest composition on soil fungal communities in a mixed boreal forest. Plant Soil 432:345–357. https://doi.org/10.1007/s11104-018-3806-3
Nguyen NH et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Noll L et al (2016) Fungal biomass and extracellular enzyme activities in coarse woody debris of 13 tree species in the early phase of decomposition. For Ecol Manag 378:181–192. https://doi.org/10.1016/j.foreco.2016.07.035
Nunez-Mir GC, Iannone BV, Curtis K, Fei SL (2015) Evaluating the evolution of forest restoration research in a changing world: a "big literature" review. New Forest 46:669–682. https://doi.org/10.1007/s11056-015-9503-7
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests MJCep (2007) The vegan package. https://cran.r-project.org/web/packages/vegan/vegan.pdf
Orwin KH, Dickie IA, Holdaway R, Wood JR (2018) A comparison of the ability of PLFA and 16S rRNA gene metabarcoding to resolve soil community change and predict ecosystem functions. Soil Biol Biochem 117:27–35. https://doi.org/10.1016/J.SOILBIO.2017.10.036
Qin Z et al (2020) Soil phosphorus availability modifies the relationship between AM fungal diversity and mycorrhizal benefits to maize in an agricultural soil. Soil Biol Biochem:107790. https://doi.org/10.1016/j.soilbio.2020.107790
Sánchez C (2009) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194. https://doi.org/10.1016/j.biotechadv.2008.11.001
Santonja M et al (2017) Plant litter diversity increases microbial abundance, fungal diversity, and carbon and nitrogen cycling in a Mediterranean shrubland. Soil Biol Biochem 111:124–134. https://doi.org/10.1016/j.soilbio.2017.04.006
Schutte UME et al (2019) Effect of permafrost thaw on plant and soil fungal community in a boreal forest: Does fungal community change mediate plant productivity response? J Ecol 107:1737–1752. https://doi.org/10.1111/1365-2745.13139
Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19(8):926–936. https://doi.org/10.1111/ele.12630
Stursova M, Žifcakova L, Leigh MB, Burgess R, Baldrian PJFME (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol 80:735–746. https://doi.org/10.1111/j.1574-6941.2012.01343.x
Sun H et al (2016a) Dominant tree species and soil type affect the fungal community structure in a boreal peatland forest. Appl Environ Microb 82:2632–2643. https://doi.org/10.1128/Aem.03858-15
Sun R et al (2016b) Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ Microbiol 18:5137. https://doi.org/10.1111/1462-2920.13512
Tedersoo L et al (2016) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346. https://doi.org/10.1038/ismej.2015.116
Urbanova M, Snajdr J, Baldrian P (2015) Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Biol Biochem 84:53–64. https://doi.org/10.1016/j.soilbio.2015.02.011
Vitkova M, Tonika J, Mullerova J (2015) Black locust-Successful invader of a wide range of soil conditions. Sci Total Environ 505:315–328. https://doi.org/10.1016/j.scitotenv.2014.09.104
Wagg C, Schlaeppi K, Banerjee S, Kuramae EE, van der Heijden MGJNc (2019) Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nat Commun 10:1–10. https://doi.org/10.1038/s41467-019-12798-y
Wang QK, Wang SL, He TX, Liu L, Wu JB (2014) Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils. Soil Biol Biochem 71:13–20. https://doi.org/10.1016/j.soilbio.2014.01.004
Wang Z, Li T, Li Y, Zhao D, Han J, Liu Y, Liao Y (2019) Relationship between the microbial community and catabolic diversity in response to conservation tillage. Soil Till Res 196:104431. https://doi.org/10.1016/J.STILL.2019.104431
Wei T, Simko V, Levy M, Xie Y, Jin Y, Zemla JJS (2017) Package ‘corrplot’. https://cran.r-project.org/web/packages/corrplot/corrplot.pdf
Wooliver RC, Senior JK, Potts BM, Nuland MEV, Bailey JK, Schweitzer JA (2018) Soil fungi underlie a phylogenetic pattern in plant growth responses to nitrogen enrichment. J Ecol. https://doi.org/10.1111/1365-2745.12983
Zhalnina K et al (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–406. https://doi.org/10.1007/s00248-014-0530-2
Zhalnina K et al (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3(4):470–480. https://doi.org/10.1038/s41564-018-0129-3
Zhao Z, Li P (2002) Researches on vertical root distributions and drought resistance of main planting tree species in weibei loess plateau. J Soil Water Conserv 16(1):96–99. https://doi.org/10.13870/j.cnki.stbcxb.2002.01.024 (In Chinese)
Zhao Q, Classen AT, Wang WW, Zhao XR, Mao B, Zeng DH (2017) Asymmetric effects of litter removal and litter addition on the structure and function of soil microbial communities in a managed pine forest. Plant Soil 414:81–93. https://doi.org/10.1007/s11104-016-3115-7
Acknowledgements
This work was financially supported by the National Key R & D Program (Grant Nos. 2017YFC0504605 and 2016YFC0501706) and the National Natural Science Foundation of China (Grant No. 41977418).
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Liu, J., Le, T., Zhu, H. et al. Afforestation of cropland fundamentally alters the soil fungal community. Plant Soil 457, 279–292 (2020). https://doi.org/10.1007/s11104-020-04739-2
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DOI: https://doi.org/10.1007/s11104-020-04739-2