Skip to main content

Advertisement

Log in

Phosphorus amendment alters soil arbuscular mycorrhizal fungal functional guild compositions in a subtropical forest

  • Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Nitrogen (N) and phosphorus (P) amendments considerably influence fungal diversity and community composition in various ecosystems. Nevertheless, how N and P additions would change arbuscular mycorrhizal (AM) fungal community and functional guilds in forest soil remains largely unclear.

Materials and methods

A 5-year N and P addition experiment was conducted in a subtropical forest of southeastern China. Soil AM fungal communities were detected by the high throughput sequencing of 18S rRNA gene-fragments. We investigated the six-seasonal responses of AM fungal diversity, community assembly pattern and functional guild composition to N and/or P amendments.

Results and discussion

The AM fungal Shannon index changed from a positive (3–4 years) to a nonsignificant (4–5 years) effect under P and NP additions as the duration of fertilization increased. P addition, but not N addition, changed the AM fungal community assembly pattern from stochastic- to deterministic-dominant processes. In contrast, P and NP additions significantly influenced AM fungal functional guild components, and the relative abundances of ancestral and edaphophilic guilds increased with increasing years of fertilization. Additionally, the AM fungal guild structure was significantly affected by soil P-related parameters.

Conclusions

Our results emphasize the substantial impacts of P amendment on soil AM community assembly pattern and functional guild composition. This study contributes to a better understanding of the temporal dynamics and potential ecological functioning of AM fungi under global environmental changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets analysed during the current study are available from the corresponding author on reasonable request.

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  • Archer E (2016) rfPermute: estimate permutation p-values for random Forest importance metrics. R package version 2.1.5. https://CRAN.R-project.org/package=rfPermute

  • Avolio ML, Koerner SE, La Pierre KJ, Wilcox KR, Wilson GW, Smith MD, Collins SL (2014) Changes in plant community composition, not diversity, during a decade of nitrogen and phosphorus additions drive above–ground productivity in a tallgrass prairie. J Ecol 102:1649–1660

    Article  CAS  Google Scholar 

  • Bahram M, Kohout P, Anslan S, Harend H, Abarenkov K, Tedersoo L (2016) Stochastic distribution of small soil eukaryotes resulting from high dispersal and drift in a local environment. ISME J 10:885–896

    Article  Google Scholar 

  • Bar-Massada A, Kent R, Carmel Y (2014) Environmental heterogeneity affects the location of modelled communities along the niche–neutrality continuum. Proc Roy Soc B Biol Sci 281:20133249

    Article  Google Scholar 

  • 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, Guo LD, Hardtle W, He JS, Hector A, Krober W, Kuhn 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

    Article  Google Scholar 

  • Camenzind T, Hättenschwiler S, Treseder KK, Lehmann A, Rillig MC (2018) Nutrient limitation of soil microbial processes in tropical forests. Ecol Monogr 88:4–21

    Article  Google Scholar 

  • Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3646–3659

    Article  Google Scholar 

  • Cao J, Lin TC, Yang Z, Zheng Y, Xie L, Xiong D, Yang Y (2020) Warming exerts a stronger effect than nitrogen addition on the soil arbuscular mycorrhizal fungal community in a young subtropical Cunninghamia lanceolata plantation. Geoderma 367:114273

    Article  CAS  Google Scholar 

  • 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, Sovinsky JR, Turnbaugh 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

    Article  CAS  Google Scholar 

  • Chase JM (2010) Stochastic community assembly causes higher biodiversity in more productive environments. Science 328:1388–1391

    Article  CAS  Google Scholar 

  • Chaudhary VB, Nolimal S, Sosa-Hernández MA, Egan C, Kastens J (2020) Trait–based aerial dispersal of arbuscular mycorrhizal fungi. New Phytol 228:238–252

    Article  CAS  Google Scholar 

  • Chaudhary VB, O’Dell TE, Rillig MC, Johnson NC (2014) Multiscale patterns of arbuscular mycorrhizal fungal abundance and diversity in semiarid shrublands. Fungal Ecol 12:32–43

    Article  Google Scholar 

  • Chen QL, Hu HW, Yan ZZ, Li CY, Nguyen BAT, Sun AQ, Zhu YG, He JZ (2021) Deterministic selection dominates microbial community assembly in termite mounds. Soil Biol Biochem Soil Biol Biochem 152:108073

    Article  CAS  Google Scholar 

  • Chen YL, Xu ZW, Xu TL, Veresoglou SD, Yang GW, Chen BD (2017) Nitrogen deposition and precipitation induced phylogenetic clustering of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 115:233–242

    Article  CAS  Google Scholar 

  • Cotton TEA (2018) Arbuscular mycorrhizal fungal communities and global change: An uncertain future. FEMS Microbiol Ecol 94:fiy179

  • Dueñas JF, Camenzind T, Roy J, Hempel S, Homeier J, Suárez JP, Rillig MC (2020) Moderate phosphorus additions consistently affect community composition of arbuscular mycorrhizal fungi in tropical montane forests in southern Ecuador. New Phytol 227:1505–1518

    Article  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In Sustain Agric 153–188. Springer, Dordrecht

  • Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23

    Article  Google Scholar 

  • Gao C, Montoya L, Xu L, Madera M, Hollingsworth J, Purdom E, Singan V, Vogel J, Hutmacher RB, Dahlberg JA, Coleman-Derr D, Lemaux PG, Taylor JW (2020) Fungal community assembly in drought–stressed sorghum shows stochasticity, selection, and universal ecological dynamics. Nat Commun 11:34

    Article  CAS  Google Scholar 

  • Gormsen D, Olsson PA, Hedlund K (2004) The influence of collembolans and earthworms on AM fungal mycelium. Appl Soil Ecol 27:211–220

    Article  Google Scholar 

  • Han Y, Feng J, Han M, Zhu B (2020) Responses of arbuscular mycorrhizal fungi to nitrogen addition: a meta-analysis. Glob Chang Biol 26:7229–7241

    Article  Google Scholar 

  • Huang YY, Ma YL, Zhao K, Niklaus PA, Schmid B, He JS (2017) Positive effects of tree species diversity on litterfall quantity and quality along a secondary successional chronosequence in a subtropical forest. J Plant Ecol 10:28–35

    Article  Google Scholar 

  • Hubbell SP (2001) The Unified Neutral Theory of Biodiversity and Biogeography, vol 32. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Jach-Smith LC, Jackson RD (2018) N addition undermines N supplied by arbuscular mycorrhizal fungi to native perennial grasses. Soil Biol Biochem 116:148–157

    Article  CAS  Google Scholar 

  • Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci USA 107:2093–2098

    Article  CAS  Google Scholar 

  • Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, Delaux PM, Klingl V, von Röpenack-Lahaye E, Wang TL, Eisenreich W, Dörmann P, Parniske M, Gutjahr C (2017) Lipid transfer from plants to arbuscular mycorrhiza fungi. eLife 6:e29107

  • Kraft NJB, Comita LS, Chase JM, Sanders NJ, Swenson NG, Crist TO, Stegen JC, Vellend M, Boyle B, Anderson MJ, Cornell HV, Davies KF, Freestone AL, Inouye BD, Harrison SP, Myers JA (2011) Disentangling the drivers of beta diversity along latitudinal and elevational gradients. Science 333:1755–1758

    Article  CAS  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  Google Scholar 

  • Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EA (2019) Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: A review. Environ Pollut 246:148–162

    Article  CAS  Google Scholar 

  • Liu Y, Zhang G, Luo X, Hou E, Zheng M, Zhang L, He X, Shen W, Wen D (2021) Mycorrhizal fungi and phosphatase involvement in rhizosphere phosphorus transformations improves plant nutrition during subtropical forest succession. Soil Biol Biochem 153:108099

    Article  CAS  Google Scholar 

  • Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: A meta-analysis. Ecology 87:53–63

    Article  Google Scholar 

  • Ma X, Geng Q, Zhang H, Bian C, Chen HY, Jiang D, Xu X (2021) Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multifunctionality. New Phytol 229:2957–2969

    Article  CAS  Google Scholar 

  • Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748

    Article  CAS  Google Scholar 

  • Maitra P, Zheng Y, Wang YL, Mandal D, Lü PP, Gao C, Babalola BJ, Ji NN, Li XC, Guo LD (2021) Phosphorus fertilization rather than nitrogen fertilization, growing season and plant successional stage structures arbuscular mycorrhizal fungal community in a subtropical forest. Biol Fertil Soils 57:685–697

    Article  CAS  Google Scholar 

  • Mori AS, Isbell F, Seidl R (2018) β-diversity, community assembly, and ecosystem functioning. Trends Ecol Evol 33:549–564

    Article  Google Scholar 

  • Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356

    Article  Google Scholar 

  • Ning D, Deng Y, Tiedje JM, Zhou J (2019) A general framework for quantitatively assessing ecological stochasticity. Proc Natl Acad Sci USA 116:16892–16898

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package v.2.0–10. https://CRAN.R-project.org/package=vegan

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    Article  Google Scholar 

  • Phillips ML, Weber SE, Andrews LV, Aronson EL, Allen MF, Allen EB (2019) Fungal community assembly in soils and roots under plant invasion and nitrogen deposition. Fungal Ecol 40:107–117

    Article  Google Scholar 

  • Powell JR, Bennett AE (2016) Unpredictable assembly of arbuscular mycorrhizal fungal communities. Pedobiologia 59:11–15

    Article  Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/

  • Sato K, Suyama Y, Saito M, Sugawara K (2005) A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction–denature gradient gel electrophoresis. Grassl Sci 51:179–181

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Schwarzott D, Schüßler A (2001) A simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza 10:203–207

    Article  CAS  Google Scholar 

  • Selosse MA, Rousset FO (2011) The plant-fungal marketplace. Science 333:828–829

    Article  CAS  Google Scholar 

  • Sheldrake M, Rosenstock NP, Mangan S, Revillini D, Sayer EJ, Olsson PA, Verbruggen E, Tanner EVJ, Turner BL, Wright SJ (2018) Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest. ISME J 12:2433–2445

    Article  CAS  Google Scholar 

  • Shen Y, Ryser ET, Li H, Zhang W (2021) Bacterial community assembly and antibiotic resistance genes in the lettuce-soil system upon antibiotic exposure. Sci Total Environ 778:146255

    Article  CAS  Google Scholar 

  • Sikes BA, Powell JR, Rillig MC (2010) Deciphering the relative contributions of multiple functions within plant-microbe symbioses. Ecology 91:1591–1597

    Article  Google Scholar 

  • Simon L, Lalonde M, Bruns T (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295

    Article  CAS  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic Press, Cambridge, UK

    Google Scholar 

  • Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079

    Article  Google Scholar 

  • Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6:1653–1664

    Article  CAS  Google Scholar 

  • Treseder KK (2004) A meta–analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Article  Google Scholar 

  • Treseder KK, Allen EB, Egerton-Warburton LM, Hart MM, Klironomos JN, Maherali H, Tedersoo L (2018) Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: A trait–based predictive framework. J Ecol 106:480–489

    Article  CAS  Google Scholar 

  • Vályi K, Mardhiah U, Rillig MC, Hempel S (2016) Community assembly and coexistence in communities of arbuscular mycorrhizal fungi. ISME J 10:2341–2351

    Article  Google Scholar 

  • Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart–how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15

    Article  Google Scholar 

  • Wang C, Lu X, Mori T, Mao Q, Zhou K, Zhou G, Nie Y, Mo J (2018) Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen–rich tropical forest. Soil Biol Biochem 121:103–112

    Article  CAS  Google Scholar 

  • Wang QC, Yang LM, Song G, Jin SS, Hu HW, Wu F, Zheng Y, He JZ (2022) The accumulation of microbial residues and plant lignin phenols are more influenced by fertilization in young than mature subtropical forests. Forest Ecol Manag 509:120074

    Article  Google Scholar 

  • Weber SE, Diez JM, Andrews LV, Goulden ML, Aronson EL, Allen MF (2019) Responses of arbuscular mycorrhizal fungi to multiple coinciding global change drivers. Fungal Ecol 40:62–71

    Article  Google Scholar 

  • Xu X, Qiu Y, Zhang K, Yang F, Chen M, Luo X, Yan X, Wang P, Zhang Y, Chen H, Guo H, Jiang L, Hu S (2022) Climate warming promotes deterministic assembly of arbuscular mycorrhizal fungal communities. Glob Chang Biol 28:1147–1161

    Article  CAS  Google Scholar 

  • Zheng Y, Chen L, Ji NN, Wang YL, Gao C, Jin SS, Hu HW, Huang ZQ, He JZ, Guo LD, Powell JR (2021) Assembly processes lead to divergent soil fungal communities within and among twelve forest ecosystems along a latitudinal gradient. New Phytol 231:1183–1194

    Article  Google Scholar 

  • Zheng Y, Kim YC, Tian XF, Chen L, Yang W, Gao C, Song MH, Xu XL, Guo LD (2014) Differential responses of arbuscular mycorrhizal fungi to nitrogen addition in a near pristine Tibetan alpine meadow. FEMS Microbiol Ecol 89:594–605

    Article  CAS  Google Scholar 

  • Zhou J, Deng Y, Zhang P, Xue K, Liang Y, Van Nostrand JD, Yang Y, He Z, Wu L, Stahl DA, Hazen TC, Tiedje JM, Arkin AP (2014) Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proc Natl Acad Sci USA 111:E836–E845

    Article  CAS  Google Scholar 

  • Zhou J, Ning D (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol Rev 81:e00002-17

    Article  Google Scholar 

  • Zhou Z, Zheng M, Xia J, Wang C (2022) Nitrogen addition promotes soil microbial beta diversity and the stochastic assembly. Sci Total Environ 806:150569

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We appreciate Mr. Zai-Gen Jiang for fertilization and field management. We are grateful to the Zhejiang Qianjiangyuan Forest Biodiversity National Observation and Research Station for experiment permission and sample collection.

Funding

This study was supported by the National Natural Science Foundation of China (31971447, 41930756) and the Natural Science Foundation of Fujian Province (2022J02025).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sheng-Sheng Jin or Yong Zheng.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Dulce Flores-Rentería

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 801 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, QC., Jin, SS., Liu, S. et al. Phosphorus amendment alters soil arbuscular mycorrhizal fungal functional guild compositions in a subtropical forest. J Soils Sediments 23, 2700–2711 (2023). https://doi.org/10.1007/s11368-023-03510-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-023-03510-1

Keywords

Navigation