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Divergent responses of soil bacterial and fungal community structures and functional groups to secondary succession after rubber plantation abandonment

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Abstract

Background and aims

There is still limited knowledge regarding the dynamics of soil microbial community structures and functional groups during forest secondary succession after rubber monocultures (RP) abandonment.

Methods

Bacterial and fungal communities and functions were investigated for the soil from six forest stands with three replicate plots. Selected stands included an RP, four spontaneous secondary forest stands that formed after RP abandonment at 1 (SF_1), 10 (SF_10), 20 (SF_20), and 40 (SF_40) years, as well as a primary forest (PF, approximately 100 years).

Results

After RP abandonment, the alpha-diversity metrics of soil microbial communities increased during the first 40 years of succession but decreased in PF. The biomarkers Proteobacteria and Mortierellomycota increased significantly (P < 0.05) by 84% and 633% in PF, respectively, while Firmicutes showed a significant decrease of 89% in comparison with SF_1. Secondary succession increased the relative abundance of bacterial functional groups related to carbon cycling and fungal functional groups (especially ericoid mycorrhizal). Soil pH was the main edaphic factor in shaping microbial communities and functions. In addition, soil moisture and seasonal variations had direct impacts on fungal communities and bacterial functions.

Conclusions

Collectively, these findings suggest that different successional trajectories occur in bacteria and fungi, owing to their divergent responses to the changes in season, soil moisture, and nutrients. Specifically, the frequent shifts in bacterial dominant phyla during succession, as well as the increased susceptibility of diversity and functional groups to season, indicate that bacteria respond more quickly to disturbances compared to fungi.

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Data availability

The data that support the findings of this study is available from the corresponding author upon reasonable request.

References

  • Annala MJ, Lehosmaa K, Ahonen SHK, Karttunen K, Markkola AM, Puumala I, Mykrä H (2022) Effect of riparian soil moisture on bacterial, fungal and plant communities and microbial decomposition rates in boreal stream-side forests. For Ecol Manag 519:120344

    Google Scholar 

  • Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90

    PubMed  PubMed Central  Google Scholar 

  • Cai ZQ, Zhang YH, Yang C, Wang S (2018) Land-use type strongly shapes community composition, but not always diversity of soil microbes in tropical China. CATENA 165:369–380

    CAS  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583

    CAS  PubMed  PubMed Central  Google Scholar 

  • Canty A, Ripley BD (2022) boot: Bootstrap R (S-Plus) Functions. R package version 1.3–28.1. https://CRAN.R-project.org/package=boot. Accessed date 4 Dec 2023

  • Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  • Chen CF, Liu WJ, Wu JE, Jiang XJ, Zhu XA (2019) Can intercropping with the cash crop help improve the soil physico-chemical properties of rubber plantations? Geoderma 335:149–160

    CAS  Google Scholar 

  • Company J, Valiente N, Fortesa J, García-Comendador J, Lucas-Borja ME, Ortega R, Miralles I, Estrany J (2022) Secondary succession and parent material drive soil bacterial community composition in terraced abandoned olive groves from a Mediterranean hyper-humid mountainous area. Agr Ecosyst Environ 332: p 107932 

  • Cui YX, Wang X, Zhang XC, Ju WL, Duan CJ, Guo XB, Wang YQ, Fang LC (2020) Soil moisture mediates microbial carbon and phosphorus metabolism during vegetation succession in a semiarid region. Soil Biol Biochem 147:107814

    CAS  Google Scholar 

  • Damgaard C (2019) A critique of the space–for–time substitution practice in community ecology. Trends Ecol Evol 34:416–421

    PubMed  Google Scholar 

  • Feng XH, Uriarte M, González G, Reed S, Thompson J, Zimmerman JK, Murphy L (2017) Improving predictions of tropical forest response to climate change through integration of field studies and ecosystem modeling. Global Change Biol 00:1–20

    Google Scholar 

  • Feng J, Wu JJ, Zhang Q, Zhang DD, Li QX, Long CY, Yang F, Chen Q, Cheng XL (2018) Stimulation of nitrogen-hydrolyzing enzymes in soil aggregates mitigates nitrogen constraint for carbon sequestration following afforestation in subtropical China. Soil Biol Biochem 123:136–144

    CAS  Google Scholar 

  • Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2:94

    PubMed  PubMed Central  Google Scholar 

  • Good IJ (1953) The population frequency of species and the estimation of population parameters. Biometrika 40:237–264

    Google Scholar 

  • Ji L, Yang YC, Yang LX (2021) Seasonal variations in soil fungal communities and co-occurrence networks along an altitudinal gradient in the cold temperate zone of China: a case study on Oakley Mountain. Catena 204:105448

    CAS  Google Scholar 

  • Jiang S, Xing YJ, Liu GC, Hu CY, Wang XC, Yan GY, Wang QG (2021) Changes in soil bacterial and fungal community composition and functional groups during the succession of boreal forests. Soil Biol Biochem 161:108393

    CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ke PJ, Zee PC, Fukami T (2021) Dynamic plant–soil microbe interactions: the neglected effect of soil conditioning time. New Phytol 231:1546–1558

    CAS  PubMed  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    PubMed  Google Scholar 

  • Lammel DR, Barth G, Ovaskainen O, Cruz LM, Zanatta JA, Ryo M, de Souza EM, Pedrosa FO (2018) Direct and indirect effects of a pH gradient bring insights into the mechanisms driving prokaryotic community structures. Microbiome 6:106

    PubMed  PubMed Central  Google Scholar 

  • Lan GY, Li YW, Lesueur D, Wu ZX, Xie GS (2018) Seasonal changes impact soil bacterial communities in a rubber plantation on Hainan Island, China. Sci Total Environ 626:826–834

    CAS  PubMed  Google Scholar 

  • Lan GY, Quan F, Yang C, Sun R, Chen BQ, Zhang XC, Wu ZX (2022) Driving factors for soil fungal and bacterial community assembly in topical forest of China. Appl Soil Ecol 177:104520

    Google Scholar 

  • Leopold DR, Peay KG, Vitousek PM, Fukami T (2021) Diversity of putative ericoid mycorrhizal fungi increases with soil age and progressive phosphorus limitation across a 4.1-million-year chronosequence. FEMS Microbiol Ecol 97:fiab016

    CAS  PubMed  Google Scholar 

  • Li JW, Shangguan ZP, Deng L (2020) Dynamics of soil microbial metabolic activity during grassland succession after farmland abandonment. Geoderma 363:114167

    CAS  Google Scholar 

  • Li XL, Zhou J, Peng F, Zhong HT, Lambers H (2021) Temporal trends of plant nutrient-acquisition strategies with soil age and their ecological significance. Chin J Plant Ecol 45:714–727 (In Chinese)

    Google Scholar 

  • Liu J, Linderman M, Ouyang Z, An L, Yang J, Zhang H (2001) Ecological degradation in protected areas: the case of Wolong Nature Reserve for giant pandas. Science 292:98–101

    CAS  PubMed  Google Scholar 

  • Liu JL, Dang P, Gao Y, Zhu HL, Zhu HN, 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

    Google Scholar 

  • Liu WJ, Hughes AC, Bai Y, Li ZJ, Mei CC, Ma YX (2020a) Using landscape connectivity tools to identify conservation priorities in forested areas and potential restoration priorities in rubber plantation in Xishuangbanna, Southwest China. Landsc Ecol 35:389–402

    Google Scholar 

  • Liu YL, Zhu GY, Hai XY, Li JW, Shangguan ZP, Peng CH, Deng L (2020b) Long-term forest succession improves plant diversity and soil quality but not significantly increase soil microbial diversity: evidence from the Loess Plateau. Ecol Eng 142:105631

    Google Scholar 

  • Liu J, Jia XY, Yan WM, Zhong YQW, Shangguan ZP (2020c) Changes in soil microbial community structure during long-term secondary succession. Land Degrad Dev 31:1151–1166

    Google Scholar 

  • Liu L, Zhu K, Krause SMB, Li SP, Wang X, Zhang ZC, Shen MW, Yang QS, Lian JY, Wang XH, Ye WH, Zhang J (2021) Changes in assembly processes of soil microbial communities during secondary succession in two subtropical forests. Soil Biol Biochem 154:108144

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ma JC, Nergui S, Han ZM, Huang GN, Li HR, Zhang R, Zhu LY, Liao JF (2019) The variation of the soil bacterial and fungal community is linked to land use types in Northeast China. Sustainability 11:3286

    CAS  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12

    Google Scholar 

  • Meerhoff M, Mello F, Kruk C, Alonso C, González-Bergonzoni I, Pacheco J, Lacerot G, Arim M, Beklioğlu M, Brucet S, Goyenola G, Iglesias C, Mazzeo N, Kosten S, Jeppesen E (2012) 4 - environmental warming in shallow lakes: a review of potential changes in community structure as evidenced from space–for–time substitution approaches. Adv Ecol Res 46:259–349

    Google Scholar 

  • Miao R, Qiu X, Guo M, Musa A, Jiang D (2018) Accuracy of space–for–time substitution for vegetation state prediction following shrub restoration. J Plant Ecol 11:208–217

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  PubMed  Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Google Scholar 

  • Ni YY, Yang T, Ma YY, Zhang KP, Soltis PS, Soltis DE, Gilbert JA, Zhao YP, Fu CX, Chu HY (2021) Soil pH determines bacterial distribution and assembly processes in natural mountain forests of eastern China. Global Ecol Biogeogr 30:2164–2177

    Google Scholar 

  • Pickett STA (1989) Space–for–time substitution as an alternative to long-term studies. In: Likens GE (ed) Long-term studies in ecology. Springer, New York, pp 110–135

    Google Scholar 

  • Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144

    Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi DD, Feng FJ, Lu C, Fu YM (2022) C:N:P stoichiometry of different soil components after the transition of temperate primary coniferous and broad-leaved mixed forests to secondary forests. Soil Tillage Res 216:105260

    Google Scholar 

  • Qu ZL, Liu B, Ma Y, Xu J, Sun H (2020) The response of the soil bacterial community and function to forest succession caused by forest disease. Funct Ecol 34:2548–2559

    Google Scholar 

  • R Core Team (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from https://www.R-project.org/. Accessed date 6 Feb 2023

  • Raiesi F, Beheshti A (2015) Microbiological indicators of soil quality and degradation following conversion of native forests to continuous croplands. Ecol Indic 50:173–185

    CAS  Google Scholar 

  • Rasche F, Knapp D, Kaiser C, Koranda M, Kitzler B, Zechmeister-Boltenstern S, Richter A, Sessitsch A (2011) Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. ISME J 5:389–402

    CAS  PubMed  Google Scholar 

  • Ren CJ, Liu WC, Zhao FZ, Zhong ZK, Deng J, Han XH, Yang GH, Feng YZ, Ren GX (2019) Soil bacterial and fungal diversity and compositions respond differently to forest development. Catena 181:104071

    CAS  Google Scholar 

  • Romanowicz KJ, Freedman ZB, Upchurch RA, Argiroff WA, Zak DR, Baldrian P (2016) Active microorganisms in forest soils differ from the total community yet are shaped by the same environmental factors: the influence of pH and soil moisture. FEMS Microbiol Ecol 92:fiw149

    PubMed  Google Scholar 

  • Rosseel Y (2012) Lavaan: an R Package for Structural equation modeling. J Stat Softw 48:1–36

    Google Scholar 

  • Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:623–656

    Google Scholar 

  • Sultana N, Zhao J, Cai YF, Rahman GKMM, Alam MS, Faheem M, Ho A, Jia ZJ (2022) Methanotrophy-driven accumulation of organic carbon in four paddy soils of Bangladesh. Pedosphere 32:348–358

    CAS  Google Scholar 

  • Tang M, Liu J, Hou WP, Stubbendieck RM, Xiong H, Jin J, Gong JY, Cheng C, Tang XX, Liu YL, Li ZF, Wang JF, Yi Y (2022) Structural variability in the bulk soil, rhizosphere, and root endophyte fungal communities of Themeda Japonica plants under different grades of karst rocky desertification. Plant Soil 475:105–122

    CAS  Google Scholar 

  • Tripathi BM, Stegen JC, Kim M, Dong K, Adams JM, Lee YK (2018) Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J 12:1072–1083

    CAS  PubMed  PubMed Central  Google Scholar 

  • Urbanová M, Šnajdr 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

    Google Scholar 

  • Wallenstein MD, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Global Chang Biol 15:1631–1639

    Google Scholar 

  • Wang SJ, Chen MK, Cao R, Cao QB, Zuo QQ, Wang P, Yang B, Zhao S (2020) Contribution of plant litter and soil variables to organic carbon pools following tropical forest development after slash-and-burn agriculture. Land Degrad Dev 31:1071–1077

    Google Scholar 

  • Wogan GOU, Wang IJ (2018) The value of space–for–time substitution for studying fine-scale microevolutionary processes. Ecography 41:1456–1468

    Google Scholar 

  • Yan GY, Han SJ, Wang QG, Wang XC, Hu CY, Xing YJ (2021) Variations of the effects of reduced precipitation and N addition on microbial diversity among different seasons in a temperate forest. Appl Soil Ecol 166:103995

    Google Scholar 

  • Yu J, Li FT, Wang Y, Lin Y, Peng ZW, Cheng K (2020) Spatiotemporal evolution of tropical forest degradation and its impact on ecological sensitivity: a case study in Jinghong, Xishuangbanna, China. Sci Total Environ 727:138678

    CAS  PubMed  Google Scholar 

  • Zhang KR, Cheng XL, Shu X, Liu Y, Zhang QF (2018) Linking soil bacterial and fungal communities to vegetation succession following agricultural Abandonment. Plant Soil 431:19–36

    CAS  Google Scholar 

  • Zhang JQ, Corlett RT, Zhai DL (2019) After the rubber boom: good news and bad news for biodiversity in Xishuangbanna, Yunnan, China. Reg Environ Change 19:1713–1724

    Google Scholar 

  • Zhong YQW, Yan WM, Wang RW, Wang W, Shangguan ZP (2018) Decreased occurrence of carbon cycle functions in microbial communities along with long-term secondary succession. Soil Biol Biochem 123:207–217

    CAS  Google Scholar 

  • Zhu XA, Chen CF, Wu JE, Yang JB, Zhang WJ, Zou X, Liu WJ, Jiang XJ (2019) Can intercrops improve soil water infiltrability and preferential flow in rubber-based agroforestry system? Soil Tillage Res 191:327–339

    Google Scholar 

  • Zhu XH, Yuan FH, He LY, Guo ZY, Wang NN, Zuo YJ, Liu JZ, Li KX, Wang YH, Sun Y, Zhang LH, Song CC, Song YY, Gong C, Son Y, Guo DF, Xu XF (2022) Wetland conversion to cropland alters the microbes along soil profiles and over seasons. Catena 214:106282

    CAS  Google Scholar 

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Acknowledgements

This research was supported by grants from the “Biodiversity Investigation, Observation, and Assessment Program” (2019–2023) of the Ministry of Ecology and Environment of China, the National Natural Science Foundation of China (No.41961144022), the National key research and development program (No.2020YFC1806305-04), the China Scholarship Council (CSC), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Authors and Affiliations

  1. Co-Innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing, 210037, China

    Qiang Lu & Xiangxiang Fu

  2. Key Laboratory for Biodiversity and Biosafety of National Environmental Protection, Biodiversity Conservation and Biosafety Research Center, Nanjing Institute of Environmental Sciences, Ministry of Ecology and Environment, Nanjing, 210042, China

    Qiang Lu, Xiaoqiang Lu, Jiaqi Li & Yan Liu

  3. Department of Renewable Resources, University of Alberta, Edmonton, AB, T6G 2E3, Canada

    Qiang Lu & Zhengfeng An

  4. Jiangsu Vocational College of Agriculture and Forestry, Zhenjiang, 212400, China

    Xia Mao

  5. Mohan Forestry Service Center, Xishuangbanna, 666308, China

    Weiguo Chen

Authors
  1. Qiang Lu
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Contributions

Qiang Lu and Xiaoqiang Lu contributed equally to this work and shared the first authorship. Yan Liu and Xiangxiang Fu conceived the experiments. Material preparation and analysis were performed by Qiang Lu and Xiaoqiang Lu. The first draft of the manuscript was written by Qiang Lu. Review, editing, and revision were conducted by Zhengfeng An and Xiaoqiang Lu. Investigation and experimental work were conducted by Xia Mao and Weiguo Chen. All authors read and approved the final manuscript.

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Correspondence to Yan Liu or Xiangxiang Fu.

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Lu, Q., Lu, X., An, Z. et al. Divergent responses of soil bacterial and fungal community structures and functional groups to secondary succession after rubber plantation abandonment. Plant Soil 498, 579–597 (2024). https://doi.org/10.1007/s11104-023-06456-y

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