Skip to main content
Log in

Dynamics of Microbial Community Structure, Function and Assembly Mechanism with Increasing Stand Age of Slash Pine (Pinus elliottii) Plantations in Houtian Sandy Area, South China

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Establishing slash pine plantations is the primary method for restoring sandification land in the Houtian area of South China. However, the microbial variation pattern with increasing stand age remains unclear. In this study, we investigated microbial community structure and function in bare sandy land and four stand age gradients, exploring ecological processes that determine their assembly. We did not observe a significant increase in the absolute abundance of bacteria or fungi with stand age. Bacterial communities were dominated by Chloroflexi, Actinobacteria, Proteobacteria, and Acidobacteria; the relative abundance of Chloroflexi significantly declined while Proteobacteria and Acidobacteria significantly increased with stand age. Fungal communities showed succession at the genus level, with Pisolithus most abundant in soils of younger stands (1- and 6-year-old). Turnover of fungal communities was primarily driven by stochastic processes; both deterministic and stochastic processes influenced the assembly of bacterial communities, with the relative importance of stochastic processes gradually increasing with stand age. Bacterial and fungal communities showed the strongest correlation with the diameter at breast height, followed by soil available phosphorus and water content. Notably, there was a significant increase in the relative abundance of functional groups involved in nitrogen fixation and uptake as stand age increased. Overall, this study highlights the important effects of slash pine stand age on microbial communities in sandy lands and suggests attention to the nitrogen and phosphorus requirements of slash pine plantations in the later stages of sandy management.

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
Fig. 6

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files]. Sequences generated for this study have been made available on the NCBI Sequence Reading Archive (SRA) database with SRA accession numbers PRJNA979784 for 16S rDNA sequences and PRJNA979787 for ITS region sequences. Other data will be made available on request.

Code Availability

The software used in this study is R (version 4.1.3) and its open-source packages.

References

  • Agerer, R. (2001). Exploration types of ectomycorrhizae. Mycorrhiza, 11, 107–114.

    Article  Google Scholar 

  • Allsup, C. M., George, I., & Lankau, R. A. (2023). Shifting microbial communities can enhance tree tolerance to changing climates. Science, 380, 835–840.

    Article  PubMed  CAS  Google Scholar 

  • Anthony, M. A., Crowther, T. W., van der Linde, S., Suz, L. M., Bidartondo, M. I., Cox, F., Schaub, M., Rautio, P., Ferretti, M., Vesterdal, L., et al. (2022). Forest tree growth is linked to mycorrhizal fungal composition and function across Europe. The ISME Journal, 16, 1327–1336.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bi, B., Yuan, Y., Zhang, H., Wu, Z., Wang, Y., & Han, F. (2022). Rhizosphere soil metabolites mediated microbial community changes of Pinus sylvestris var. mongolica across stand ages in the Mu Us Desert. Applied Soil Ecology, 169, 104222.

    Article  Google Scholar 

  • Bi, B., Zhang, H., Yuan, Y., Wu, Z., Wang, Y., & Han, F. (2021). Dynamic changes of soil microbial community in Pinus sylvestris var. mongolica plantations in the Mu Us Sandy Land. Journal of Environmental Management, 287, 112306.

    Article  PubMed  CAS  Google Scholar 

  • Coban, O., De Deyn, G. B., & van der Ploeg, M. (2022). Soil microbiota as game-changers in restoration of degraded lands. Science, 375, abe0725.

    Article  PubMed  Google Scholar 

  • Delgado-Baquerizo, M., Oliverio, A. M., Brewer, T. E., Benavent-González, A., Eldridge, D. J., Bardgett, R. D., Maestre, F. T., Singh, B. K., et al. (2018). A global atlas of the dominant bacteria found in soil. Science, 359, 320–325.

    Article  PubMed  CAS  Google Scholar 

  • Fierer, N. (2017). Embracing the unknown: Disentangling the complexities of the soil microbiome. Nature Review Microbiology, 15, 579–590.

    Article  PubMed  CAS  Google Scholar 

  • Fierer, N., Bradford, M. A., & Jackson, R. B. (2007). Toward an ecological classification of soil bacteria. Ecology, 88, 1354–1364.

    Article  PubMed  Google Scholar 

  • Fierer, N., Wood, S. A., & Bueno de Mesquita, C. P. (2021). How microbes can, and cannot, be used to assess soil health. Soil Biology and Biochemistry, 153, 108111.

    Article  CAS  Google Scholar 

  • Friendly, M. (2002). Corrgrams: Exploratory displays for correlation matrices. The American Statistician, 56, 316–324.

    Article  Google Scholar 

  • Gao, C., Montoya, L., Xu, L., Madera, M., Hollingsworth, J., Purdom, E., Singan, V., Vogel, J., Hutmacher, R. B., Dahlberg, J. A., et al. (2020). Fungal community assembly in drought-stressed sorghum shows stochasticity, selection, and universal ecological dynamics. Nature Communications, 11, 34.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao, C., Zhang, Y., Shi, N. N., Zheng, Y., Chen, L., Wubet, T., Bruelheide, H., Both, S., Buscot, F., Ding, Q., et al. (2015). Community assembly of ectomycorrhizal fungi along a subtropical secondary forest succession. The New Phytologist, 205, 771–785.

    Article  PubMed  Google Scholar 

  • Gao, Y., Song, H., Zhou, F., Chen, S., He, G., Yan, J., Sun, Q., Long, H., Zhai, Z., Hu, D., et al. (2022). Community of soil-inhabiting myxomycetes shares similar assembly mechanisms with fungi, and is affected by bacterial community in subtropical forests of China. Soil Biology and Biochemistry, 175, 108854.

    Article  CAS  Google Scholar 

  • Hermans, S. M., Buckley, H. L., Case, B. S., Curran-Cournane, F., Taylor, M., & Lear, G. (2017). Bacteria as emerging indicators of soil condition. Applied and Environmental Microbiology, 83, e02826-16.

    Article  PubMed  CAS  Google Scholar 

  • Hobbie, E. A., & Agerer, R. (2010). Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant and Soil, 327, 71–83.

    Article  CAS  Google Scholar 

  • Hu, Y., Wang, Z., Zhang, Z., Song, N., Zhou, H., Li, Y., Wang, Y., Li, C., & Hale, L. (2021). Alteration of desert soil microbial community structure in response to agricultural reclamation and abandonment. CATENA, 207, 105678.

    Article  CAS  Google Scholar 

  • Hua, X., Jiang, C., & Liu, G. (1995). Floristic survey of ectomycorrhizal fungi for the southern pine in China. Journal of Nanjing Forestry University, 19, 29–36.

    Google Scholar 

  • Huo, X., Ren, C., Wang, D., Wu, R., Wang, Y., Li, Z., Huang, D., & Qi, H. (2023). Microbial community assembly and its influencing factors of secondary forests in Qinling Mountains. Soil Biology and Biochemistry, 184, 109075.

    Article  CAS  Google Scholar 

  • Izumi, H., Cairney, J. W., Killham, K., Moore, E., Alexander, I. J., & Anderson, I. C. (2008). Bacteria associated with ectomycorrhizas of slash pine (Pinus elliottii) in south-eastern Queensland, Australia. FEMS Microbiology Letters, 282, 196–204.

    Article  PubMed  CAS  Google Scholar 

  • Jiang, S., Xing, Y., Liu, G., Hu, C., Wang, X., Yan, G., & Wang, Q. (2021). Changes in soil bacterial and fungal community composition and functional groups during the succession of boreal forests. Soil Biology and Biochemistry, 161, 108393.

    Article  CAS  Google Scholar 

  • Jörgensen, K., Clemmensen, K. E., Wallander, H., & Lindahl, B. D. (2023). Do ectomycorrhizal exploration types reflect mycelial foraging strategies? The New Phytologist, 237, 576–584.

    Article  PubMed  Google Scholar 

  • Kang, P., Pan, Y., Yang, P., Hu, J., Zhao, T., Zhang, Y., Ding, X., & Yan, X. (2022). A comparison of microbial composition under three tree ecosystems using the stochastic process and network complexity approaches. Frontiers in Microbiology, 13, 1018077.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koizumi, T., Hattori, M., & Nara, K. (2018). Ectomycorrhizal fungal communities in alpine relict forests of Pinus pumila on Mt. Norikura. Japan. Mycorrhiza, 28, 129–145.

    Article  PubMed  CAS  Google Scholar 

  • Kranabetter, J. M., Durall, D. M., & MacKenzie, W. H. (2009). Diversity and species distribution of ectomycorrhizal fungi along productivity gradients of a southern boreal forest. Mycorrhiza, 19, 99–111.

    Article  PubMed  CAS  Google Scholar 

  • Kyaschenko, J., Clemmensen, K. E., Hagenbo, A., Karltun, E., & Lindahl, B. D. (2017). Shift in fungal communities and associated enzyme activities along an age gradient of managed Pinus sylvestris stands. The ISME Journal, 11, 863–874.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, C., Cui, Y., Li, X., & Yao, M. (2021a). microeco: An R package for data mining in microbial community ecology. FEMS Microbiology Ecology, 97, fiaa255.

    Article  PubMed  CAS  Google Scholar 

  • Liu, D., Wang, H., An, S., Bhople, P., & Davlatbekov, F. (2019a). Geographic distance and soil microbial biomass carbon drive biogeographical distribution of fungal communities in Chinese Loess Plateau soils. Science of the Total Environment, 660, 1058–1069.

    Article  PubMed  CAS  Google Scholar 

  • Liu, G., Chen, L., Shi, X., Yuan, Z., Yuan, L. Y., Lock, T. R., & Kallenbach, R. L. (2019b). Changes in rhizosphere bacterial and fungal community composition with vegetation restoration in planted forests. Land Degradation & Development, 30, 1147–1157.

    Article  Google Scholar 

  • Liu, L., Zhu, K., Krause, S. M., Li, S., Wang, X., Zhang, Z., Shen, M., Yang, Q., Lian, J., Wang, X., et al. (2021b). Changes in assembly processes of soil microbial communities during secondary succession in two subtropical forests. Soil Biology and Biochemistry, 154, 108144.

    Article  CAS  Google Scholar 

  • Liu, Y., Chen, L., Ma, T., Li, X., Zheng, M., Zhou, X., Chen, L., Qian, X., Xi, J., Lu, H., et al. (2023). EasyAmplicon: An easy-to-use, open-source, reproducible, and community-based pipeline for amplicon data analysis in microbiome research. iMeta, 2, e83.

    Article  Google Scholar 

  • Long, H., Wu, X., Wang, Y., Yan, J., Guo, X., An, X., Zhang, Q., Li, Z., & Huo, G. (2021). Effects of revegetation on the composition and diversity of bacterial and fungal communities of sandification land soil, in Southern China. Environmental Monitoring and Assessment, 193, 706.

    Article  PubMed  CAS  Google Scholar 

  • Louca, S., Parfrey, L. W., & Doebeli, M. (2016). Decoupling function and taxonomy in the global ocean microbiome. Science, 353, 1272–1277.

    Article  PubMed  CAS  Google Scholar 

  • Maechler, M. (2019). Finding groups in data: Cluster analysis extended Rousseeuw et al. R package version, 2.

  • Nguyen, N. H., Song, Z., Bates, S. T., Branco, S., Tedersoo, L., Menke, J., Schilling, J. S., & Kennedy, P. G. (2016). FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology, 20, 241–248.

    Article  Google Scholar 

  • Nilsson, R. H., Larsson, K. H., Taylor, A. F. S., Bengtsson-Palme, J., Jeppesen, T. S., Schigel, D., Kennedy, P., Picard, K., Glöckner, F. O., Tedersoo, L., et al. (2019). The UNITE database for molecular identification of fungi: Handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research, 47, D259–D264.

    Article  PubMed  CAS  Google Scholar 

  • Ning, C., Egerton-Warburton, L. M., Mueller, G. M., Xiang, W., Yan, W., & Liu, S. (2021). Shifts in ectomycorrhizal fungal community composition during the early establishment of native and exotic pine seedlings. Applied Soil Ecology, 157, 103722.

    Article  Google Scholar 

  • Ning, C., Mueller, G. M., Egerton-Warburton, L. M., Xiang, W., & Yan, W. (2019a). Host phylogenetic relatedness and soil nutrients shape ectomycorrhizal community composition in native and exotic pine plantations. Forests, 10, 263.

    Article  Google Scholar 

  • Ning, C., Xiang, W., Mueller, G. M., Egerton-Warburton, L. M., Yan, W., & Liu, S. (2019b). Differences in ectomycorrhizal community assembly between native and exotic pines are reflected in their enzymatic functional capacities. Plant and Soil, 446, 179–193.

    Article  Google Scholar 

  • Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, M., Oksanen, M., & Suggests, M. (2007). The Vegan Package. Community Ecology Package, 10, 631–637.

    Google Scholar 

  • Peay, K. G., Kennedy, P. G., & Bruns, T. D. (2011). Rethinking ectomycorrhizal succession: Are root density and hyphal exploration types drivers of spatial and temporal zonation? Fungal Ecology, 4, 233–240.

    Article  Google Scholar 

  • Pennisi, E., & Cornwall, W. (2020). Hidden web of fungi could shape the future of forests. Science, 369, 1042–1043.

    Article  PubMed  CAS  Google Scholar 

  • Policelli, N., Bruns, T. D., Vilgalys, R., & Nunez, M. A. (2019). Suilloid fungi as global drivers of pine invasions. The New Phytologist, 222, 714–725.

    Article  PubMed  Google Scholar 

  • Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, D590–D596.

    Article  PubMed  CAS  Google Scholar 

  • Sebastiana, M., Corrêa, A., Castro, P., & Ramos, M. (2020). Pisolithus. In N. Amaresan, M. Senthil Kumar, K. Annapurna, K. Kumar, & A. Sankaranarayanan (Eds.), Beneficial microbes in agro-ecology (pp. 707–726). Academic Press.

    Chapter  Google Scholar 

  • Sloan, W. T., Lunn, M., Woodcock, S., Head, I. M., Nee, S., & Curtis, T. P. (2006). Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environmental Microbiology, 8, 732–740.

    Article  PubMed  Google Scholar 

  • Stegen, J. C., Lin, X., Fredrickson, J. K., Chen, X., Kennedy, D. W., Murray, C. J., Rockhold, M. L., & Konopka, A. (2013). Quantifying community assembly processes and identifying features that impose them. The ISME Journal, 7, 2069–2079.

    Article  PubMed  PubMed Central  Google Scholar 

  • Strickland, M. S., Callaham, M. A., Gardiner, E. S., Stanturf, J. A., Leff, J. W., Fierer, N., & Bradford, M. A. (2017). Response of soil microbial community composition and function to a bottomland forest restoration intensity gradient. Applied Soil Ecology, 119, 317–326.

    Article  Google Scholar 

  • Stuart, E. K., Castañeda-Gómez, L., Macdonald, C. A., Wong-Bajracharya, J., Anderson, I. C., Carrillo, Y., Plett, J. M., & Plett, K. L. (2022). Species-level identity of Pisolithus influences soil phosphorus availability for host plants and is moderated by nitrogen status, but not CO2. Soil Biology and Biochemistry, 165, 108520.

    Article  CAS  Google Scholar 

  • Tai, X. S., Mao, W. L., Liu, G. X., Chen, T., Zhang, W., Wu, X. K., Long, H. Z., Zhang, B. G., & Zhang, Y. (2013). High diversity of nitrogen-fixing bacteria in the upper reaches of the Heihe River, northwestern China. Biogeosciences, 10, 5589–5600.

    Article  Google Scholar 

  • Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T., & Singh, B. K. (2020). Plant-microbiome interactions: From community assembly to plant health. Nature Reviews Microbiology, 18, 607–621.

    Article  PubMed  CAS  Google Scholar 

  • Wang, B., Huang, S., Li, Z., Zhou, Z., Huang, J., Yu, H., Peng, T., Song, Y., & Na, X. (2022a). Factors driving the assembly of prokaryotic communities in bulk soil and rhizosphere of Torreya grandis along a 900-year age gradient. Science of the Total Environment, 837, 155573.

    Article  PubMed  CAS  Google Scholar 

  • Wang, C., Zheng, Y., Sakai, Y., Toyoda, A., Minakuchi, Y., Abe, K., Yokota, A., & Yabe, S. (2019a). Tengunoibacter tsumagoiensis gen. nov., sp. nov., Dictyobacter kobayashii sp. nov., Dictyobacter alpinus sp. nov., and description of Dictyobacteraceae fam. nov. within the order Ktedonobacterales isolated from Tengu-no-mugimeshi, a soil-like granular mass of micro-organisms, and emended descriptions of the genera Ktedonobacter and Dictyobacter. International Journal of Systematic and Evolutionary Microbiology, 69, 1910–1918.

    Article  PubMed  CAS  Google Scholar 

  • Wang, D. D., Zhao, W., Reyila, M., Huang, K. C., Liu, S., & Cui, B. K. (2022b). Diversity of microbial communities of Pinus sylvestris var. mongolica at Spatial Scale. Microorganisms, 10, 371.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, K., Zhang, Y., Tang, Z., Shangguan, Z., Chang, F., Jia, F., Chen, Y., He, X., Shi, W., & Deng, L. (2019b). Effects of grassland afforestation on structure and function of soil bacterial and fungal communities. Science of the Total Environment, 676, 396–406.

    Article  PubMed  CAS  Google Scholar 

  • Wang, X., Kou, Y., Liu, J., Zhao, W., & Liu, Q. (2023a). Soil microbial legacy determines mycorrhizal colonization and root traits of conifer seedlings during subalpine forest succession. Plant and Soil, 485, 361–375.

    Article  CAS  Google Scholar 

  • Wang, Y., Dong, L., Zhang, M., Cui, Y., Bai, X., Song, B., Zhang, J., & Yu, X. (2023b). Dynamic microbial community composition, co-occurrence pattern and assembly in rhizosphere and bulk soils along a coniferous plantation chronosequence. CATENA, 223, 106914.

    Article  CAS  Google Scholar 

  • Wang, Y. L., Zhang, X., Xu, Y., Babalola, B. J., Xiang, S. M., Zhao, Y. L., & Fan, Y. J. (2021). Fungal diversity and community assembly of ectomycorrhizal fungi associated with five pine species in Inner Mongolia. China. Frontiers in Microbiology, 12, 646821.

    Article  PubMed  Google Scholar 

  • Wu, N., Li, Z., Meng, S., & Wu, F. (2021). Soil properties and microbial community in the rhizosphere of Populus alba var. pyramidalis along a chronosequence. Microbiological Research, 250, 126812.

    Article  PubMed  CAS  Google Scholar 

  • Wu, Z., Haack, S. E., Lin, W., Li, B., Wu, L., Fang, C., & Zhang, Z. (2015). Soil microbial community structure and metabolic activity of Pinus elliottii plantations across different stand ages in a subtropical area. PLoS ONE, 10, e0135354.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu, L., & Coleman-Derr, D. (2019). Causes and consequences of a conserved bacterial root microbiome response to drought stress. Current Opinion in Microbiology, 49, 1–6.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, X., Liu, S., Li, X., Wang, J., Ding, Q., Wang, H., Tian, C., Yao, M., An, J., & Huang, Y. (2016). Changes of soil prokaryotic communities after clear-cutting in a karst forest: Evidences for cutting-based disturbance promoting deterministic processes. FEMS Microbiology Ecology, 92, fiw026.

    Article  PubMed  Google Scholar 

  • Zhao, P. S., Guo, M. S., Gao, G. L., Zhang, Y., Ding, G. D., Ren, Y., & Akhtar, M. (2020). Community structure and functional group of root-associated Fungi of Pinus sylvestris var. mongolica across stand ages in the Mu Us Desert. Ecology and Evolution, 10, 3032–3042.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, J., & Ning, D. (2017). Stochastic community assembly: Does it matter in microbial ecology? Microbiology and Molecular Biology Reviews, 81, e00002-17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, X., Guo, Z., Chen, C., & Jia, Z. (2017). Soil microbial community structure and diversity are largely influenced by soil pH and nutrient quality in 78-year-old tree plantations. Biogeosciences, 14, 2101–2111.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Jennifer Smith (University of Otago) for language editing, and the two anonymous reviewers for their valuable insights and suggestions. This study was supported by grants from the National Natural Science Foundation of China (32160029), and the Foundation of Key Laboratory of Extreme Environmental Microbial Resources and Engineering, Gansu Province (EEMRE201803).

Author information

Authors and Affiliations

Authors

Contributions

XZ and SYX conceived and designed the study with the help of HL and YG; XZ, SYX, QW, BBZ, YMM, and ZCD performed the experiments; XZ, SYX, XW, and HL analyzed the data, and XZ drafted the manuscript; LC, JL, and HL helped to revise the manuscript.

Corresponding author

Correspondence to Haozhi Long.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this study.

Ethical statements and consent to participate

Not applicable.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 4169 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

Zhang, X., Xiong, SY., Wu, X. et al. Dynamics of Microbial Community Structure, Function and Assembly Mechanism with Increasing Stand Age of Slash Pine (Pinus elliottii) Plantations in Houtian Sandy Area, South China. J Microbiol. 61, 953–966 (2023). https://doi.org/10.1007/s12275-023-00089-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-023-00089-7

Keywords

Navigation