Abstract
Purpose
Elucidating the interactions of above- and below-ground communities in forest ecosystems is of great importance for comprehending biodiversity maintenance and ecosystem functioning.
Methods
In the context of a Biodiversity and Ecosystem Functioning experiment conducted in China (BEF-China), we explored the combined effects of tree species richness (1, 2, and 4) and shrub species richness (0, 2, 4, and 8) on soil fungal community diversity and structure under tree species with different mycorrhizal types (i.e., arbuscular mycorrhizal (AM) tree and ectomycorrhizal (EM) tree) using the Illumina sequencing method.
Results
Results demonstrated that the fungal alpha diversity, community composition and network structure were significantly different between EM trees and AM trees. Although tree and shrub species richness had no significant interactive effect on soil fungal alpha diversity regardless of tree mycorrhizal types, however, their interactions did influence fungal community composition and co-occurrence network structure. Specifically, the interactive effect of tree and shrub species richness on soil fungal community composition was observed in AM trees, and their interactions affected the soil fungal co-occurrence network structure in EM trees.
Conclusions
These findings highlight the tree mycorrhizal type dependence of the interactive effects of tree and shrub species richness on soil fungal communities in a subtropical forest.
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Data availability
The datasets generated for this study can be found in the National Centre for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under bioproject Number PRJNA940324.
References
Abarenkov K, Henrik Nilsson R, Larsson KH et al (2010) The UNITE database for molecular identification of fungi – recent updates and future perspectives. New Phytol 186:281–285. https://doi.org/10.1111/j.1469-8137.2009.03160.x
Aguilar-Trigueros CA, Hempel S, Powell JR et al (2015) Branching out: towards a trait-based understanding of fungal ecology. Fungal Biol Rev 29:34–41. https://doi.org/10.1016/j.fbr.2015.03.001
Ampoorter E, Barbaro L, Jactel H et al (2020) Tree diversity is key for promoting the diversity and abundance of forest-associated taxa in Europe. Oikos 129:133–146. https://doi.org/10.1111/oik.06290
Bahram M, Põlme S, Kõljalg U et al (2012) Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytol 193:465–473. https://doi.org/10.1111/j.1469-8137.2011.03927.x
Bahram M, Netherway T, Hildebrand F et al (2020) Plant nutrient-acquisition strategies drive topsoil microbiome structure and function. New Phytol 227:1189–1199. https://doi.org/10.1111/nph.16598
Banerjee S, Walder F, Büchi L et al (2019) Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J 13:1722–1736. https://doi.org/10.1038/s41396-019-0383-2
Bastian M, Heymann S, Jacomy M (2009) Gephi: An open source software for exploring and manipulating networks. https://doi.org/10.13140/2.1.1341.1520
Beidler KV, Pritchard SG (2017) Maintaining connectivity: understanding the role of root order and mycelial networks in fine root decomposition of woody plants. Plant Soil 420:19–36. https://doi.org/10.1007/s11104-017-3393-8
Bennett JA, Maherali H, Reinhart KO et al (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. https://doi.org/10.1126/science.aai8212
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219. https://doi.org/10.3389/fmicb.2014.00219
Betts MG, Wolf C, Ripple WJ et al (2017) Global forest loss disproportionately erodes biodiversity in intact landscapes. Nature 547:441–444. https://doi.org/10.1038/nature23285
Bödeker ITM, Lindahl BD, Olson Ã, Clemmensen KE (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol 30:1967–1978. https://doi.org/10.1111/1365-2435.12677
Bonfante P, Anca IA (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. https://doi.org/10.1146/annurev.micro.091208.073504
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. https://doi.org/10.1016/0038-0717(85)90144-0
Bruelheide H, Nadrowski K, Assmann T et al (2014) Designing forest biodiversity experiments: general considerations illustrated by a new large experiment in subtropical China. Methods Ecol Evol 5:74–89. https://doi.org/10.1111/2041-210X.12126
Buée M, De Boer W, Martin F et al (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212. https://doi.org/10.1007/s11104-009-9991-3
Bürkner PC (2017) Brms: an R package for bayesian multilevel models using stan. J Stat Softw 80:1–28. https://doi.org/10.18637/jss.v080.i01
Caporaso JG, Kuczynski J, Stombaugh J 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
Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522
Chaffron S, Rehrauer H, Pernthaler J, von Mering C (2010) A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res 20:947–959. https://doi.org/10.1101/gr.104521.109
Cheeke TE, Phillips RP, Brzostek ER et al (2017) Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. New Phytol 214:432–442. https://doi.org/10.1111/nph.14343
Chen X, Ding Z, Tang M, Zhu B (2018) Greater variations of rhizosphere effects within mycorrhizal group than between mycorrhizal group in a temperate forest. Soil Biol Biochem 126:237–246. https://doi.org/10.1016/j.soilbio.2018.08.026
Chen Y, Chen L, Cheng Y et al (2020) Afforestation promotes the enhancement of forest LAI and NPP in China. For Ecol Manag 462:117990. https://doi.org/10.1016/j.foreco.2020.117990
Chen K, Hu L, Wang C et al (2021) Herbaceous plants influence bacterial communities, while shrubs influence fungal communities in subalpine coniferous forests. For Ecol Manag 500:119656. https://doi.org/10.1016/j.foreco.2021.119656
Churchland C, Grayston SJ (2014) Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil C cycling. Front Microbiol 5:261. https://doi.org/10.3389/fmicb.2014.00261
Collins CG, Stajich JE, Weber SE et al (2018) Shrub range expansion alters diversity and distribution of soil fungal communities across an alpine elevation gradient. Mol Ecol 27:2461–2476. https://doi.org/10.1111/mec.14694
Cornelissen J, Aerts R, Cerabolini B et al (2001) Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129:611–619. https://doi.org/10.1007/s004420100752
Csardi G, Nepusz T (2006) The igraph software package for complex network research. Inter Journal, Complex Systems, 16951704.
Delgado-Baquerizo M, Maestre FT, Reich PB et al (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Deng Y, Jiang YH, Yang Y et al (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113. https://doi.org/10.1186/1471-2105-13-113
Deng M, Hu S, Guo L et al (2023) Tree mycorrhizal association types control biodiversity-productivity relationship in a subtropical forest. Sci Adv 9:eadd4468. https://doi.org/10.1126/sciadv.add4468
Dietrich P, Ferlian O, Huang Y et al (2023) Tree diversity effects on productivity depend on mycorrhizae and life strategies in a temperate forest experiment. Ecology 104:e3896. https://doi.org/10.1002/ecy.3896
Ding X, Liu G, Fu S, Chen HYH (2021) Tree species composition and nutrient availability affect soil microbial diversity and composition across forest types in subtropical China. Catena 201:105224. https://doi.org/10.1016/j.catena.2021.105224
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks
Freilich S, Kreimer A, Meilijson I et al (2010) The large-scale organization of the bacterial network of ecological co-occurrence interactions. Nucleic Acids Res 38:3857–3868. https://doi.org/10.1093/nar/gkq118
Gan H, Li X, Wang Y et al (2022) Plants play stronger effects on soil fungal than bacterial communities and co-occurrence network structures in a subtropical tree diversity experiment. Microbiol Spectr 0:e00134–e00122. https://doi.org/10.1128/spectrum.00134-22
Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270. https://doi.org/10.1146/annurev.phyto.42.012604.135455
Guerra CA, Heintz-Buschart A, Sikorski J et al (2020) Blind spots in global soil biodiversity and ecosystem function research. Nat Commun 11:3870. https://doi.org/10.1038/s41467-020-17688-2
Huang Y, Chen Y, Castro-Izaguirre N et al (2018) Impacts of species richness on productivity in a large-scale subtropical forest experiment. Science 362:80–83. https://doi.org/10.1126/science.aat6405
Jacobs LM, Sulman BN, Brzostek ER et al (2018) Interactions among decaying leaf litter, root litter and soil organic matter vary with mycorrhizal type. J Ecol 106:502–513. https://doi.org/10.1111/1365-2745.12921
Kadowaki K, Yamamoto S, Sato H et al (2018) Mycorrhizal fungi mediate the direction and strength of plant–soil feedbacks differently between arbuscular mycorrhizal and ectomycorrhizal communities. Commun Biol 1:1–11. https://doi.org/10.1038/s42003-018-0201-9
Kauppi PE, Mielikäinen K, Kuusela K (1992) Biomass and carbon budget of european forests, 1971 to 1990. Science 256:70–74. https://doi.org/10.1126/science.256.5053.70
Keller AB, Phillips RP (2019) Leaf litter decay rates differ between mycorrhizal groups in temperate, but not tropical, forests. New Phytol 222:556–564. https://doi.org/10.1111/nph.15524
Keller AB, Brzostek ER, Craig ME et al (2021) Root-derived inputs are major contributors to soil carbon in temperate forests, but vary by mycorrhizal type. Ecol Lett 24:626–635. https://doi.org/10.1111/ele.13651
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Liang M, Johnson D, Burslem DFRP et al (2020) Soil fungal networks maintain local dominance of ectomycorrhizal trees. Nat Commun 11:2636. https://doi.org/10.1038/s41467-020-16507-y
Likulunga LE, Rivera Pérez CA, Schneider D et al (2021) Tree species composition and soil properties in pure and mixed beech-conifer stands drive soil fungal communities. For Ecol Manag 502:119709. https://doi.org/10.1016/j.foreco.2021.119709
Lin G, McCormack ML, Ma C, Guo D (2017) Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytol 213:1440–1451. https://doi.org/10.1111/nph.14206
Liu X, Tan N, Zhou G et al (2021) Plant diversity and species turnover co-regulate soil nitrogen and phosphorus availability in Dinghushan forests, southern China. Plant Soil 464:257–272. https://doi.org/10.1007/s11104-021-04940-x
Ma B, Wang H, Dsouza M et al (2016) Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME J 10:1891–1901. https://doi.org/10.1038/ismej.2015.261
Ma K, He JS, Bruelheide H et al (2017) Biodiversity–ecosystem functioning research in chinese subtropical forests. J Plant Ecol 10:1–3. https://doi.org/10.1093/jpe/rtw129
Ma J, Chen L, Mi X et al (2023) The interactive effects of soil fertility and tree mycorrhizal association explain spatial variation of diversity-biomass relationships in a subtropical forest. J Ecol. https://doi.org/10.1111/1365-2745.14076
Muneer MA, Huang X, Hou W et al (2021) Response of fungal diversity, community composition, and functions to nutrients management in red soil. J Fungi 7:554. https://doi.org/10.3390/jof7070554
Nguyen NH, Song Z, Bates ST 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
Oksanen J, Blanchet FG, Friendly M et al (2018) Vegan: community ecology package. https://cran.r-project.org/web/packages/vegan/index.html
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci 104:19891–19896. https://doi.org/10.1073/pnas.0706375104
Pan Y, Birdsey RA, Phillips OL, Jackson RB (2013) The structure, distribution, and biomass of the world’s forests. Annu Rev Ecol Evol Syst 44:593–622. https://doi.org/10.1146/annurev-ecolsys-110512-135914
Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol 14:434–447. https://doi.org/10.1038/nrmicro.2016.59
Penone C, Allan E, Soliveres S et al (2019) Specialisation and diversity of multiple trophic groups are promoted by different forest features. Ecol Lett 22:170–180. https://doi.org/10.1111/ele.13182
Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51. https://doi.org/10.1111/nph.12221
Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manag 309:19–27. https://doi.org/10.1016/j.foreco.2013.02.034
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rivest M, Whalen JK, Rivest D (2019) Tree diversity is not always a strong driver of soil microbial diversity: a 7-yr-old diversity experiment with trees. Ecosphere 10:e02685. https://doi.org/10.1002/ecs2.2685
Shi S, Nuccio EE, Shi ZJ et al (2016) The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol Lett 19:926–936. https://doi.org/10.1111/ele.12630
Singavarapu B, Beugnon R, Bruelheide H et al (2021) Tree mycorrhizal type and tree diversity shape the forest soil microbiota. Environ Microbiol. https://doi.org/10.1111/1462-2920.15690
Soudzilovskaia NA, van Bodegom PM, Terrer C et al (2019) Global mycorrhizal plant distribution linked to terrestrial carbon stocks. Nat Commun 10:5077. https://doi.org/10.1038/s41467-019-13019-2
Taylor MK, Lankau RA, Wurzburger N (2016) Mycorrhizal associations of trees have different indirect effects on organic matter decomposition. J Ecol 104:1576–1584. https://doi.org/10.1111/1365-2745.12629
Tedersoo L, Bahram M (2019) Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes. Biol Rev 94:1857–1880. https://doi.org/10.1111/brv.12538
Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688. https://doi.org/10.1126/science.1256688
Tedersoo L, Bahram M, Cajthaml T et al (2016) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346–362. https://doi.org/10.1038/ismej.2015.116
Terrer C, Vicca S, Stocker BD et al (2018) Ecosystem responses to elevated CO2 governed by plant–soil interactions and the cost of nitrogen acquisition. New Phytol 217:507–522. https://doi.org/10.1111/nph.14872
Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of Ascomycetes and Basidiomycetes in environmental samples. PLoS ONE 7:e40863. https://doi.org/10.1371/journal.pone.0040863
Uroz S, Buée M, Deveau A et al (2016) Ecology of the forest microbiome: highlights of temperate and boreal ecosystems. Soil Biol Biochem 103:471–488. https://doi.org/10.1016/j.soilbio.2016.09.006
van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
van der Linde S, Suz LM, Orme CDL et al (2018) Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558:243–248. https://doi.org/10.1038/s41586-018-0189-9
van der Plas F, Manning P, Allan E et al (2016) Jack-of-all-trades effects drive biodiversity–ecosystem multifunctionality relationships in european forests. Nat Commun 7:11109. https://doi.org/10.1038/ncomms11109
Várnai A, Mäkelä MR, Djajadi DT et al (2014) Carbohydrate-binding modules of fungal cellulases. Advances in Applied Microbiology. Elsevier, Amsterdam, pp 103–165
Vehtari A, Gelman A, Gabry J (2017) Practical bayesian model evaluation using leave-one-out cross-validation and WAIC. Stat Comput 27:1413–1432. https://doi.org/10.1007/s11222-016-9696-4
Wagner RG, Little KM, Richardson B, Mcnabb K (2006) The role of vegetation management for enhancing productivity of the world’s forests. For Int J For Res 79:57–79. https://doi.org/10.1093/forestry/cpi057
Wang Y, Li S, Lang X et al (2022) Effects of microtopography on soil fungal community diversity, composition, and assembly in a subtropical monsoon evergreen broadleaf forest of Southwest China. Catena 211:106025. https://doi.org/10.1016/j.catena.2022.106025
Weißbecker C, Wubet T, Lentendu G et al (2018) Experimental evidence of functional group-dependent effects of tree diversity on soil fungi in subtropical forests. Front Microbiol 9:2312. https://doi.org/10.3389/fmicb.2018.02312
Yang X, Bauhus J, Both S et al (2013) Establishment success in a forest biodiversity and ecosystem functioning experiment in subtropical China (BEF-China). Eur J For Res 132:593–606. https://doi.org/10.1007/s10342-013-0696-z
Yang B, Li Y, Ding B et al (2017) Impact of tree diversity and environmental conditions on the survival of shrub species in a forest biodiversity experiment in subtropical China. J Plant Ecol 10:179–189. https://doi.org/10.1093/jpe/rtw099
Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221. https://doi.org/10.1016/j.soilbio.2014.07.022
Acknowledgements
Thanks to Tianhe Yu and Sirong Zhang for their help with sampling and Dr. Lifen Jiang for comments and English proofing. This research was financially supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB310304) and the National Key R&D Program of China (2022 YFF1303200).
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Naili Zhang and Laiye Qu designed the research; Haolei Xiong performed the analysis; Haolei Xiong, Naili Zhang and Laiye Qu wrote the first draft. Koike Takayoshi and Siqi Tao reviewed and edited the manuscript. All authors have read and agreed to this version of the manuscript.
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Xiong, H., Zhang, N., Takayoshi, K. et al. Tree mycorrhizal types and the interaction between tree and shrub species richness shape soil fungal communities in a subtropical forest in China. Plant Soil 493, 61–77 (2023). https://doi.org/10.1007/s11104-023-06211-3
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DOI: https://doi.org/10.1007/s11104-023-06211-3