Abstract
Aim
Soil microbes can significantly influence restoration outcomes via interaction with plant community assembly processes, yet knowledge about variation in soil microbial communities – in particular functional variation – during oldfield succession is limited.
Methods
We divided a well-dated successional chronosequence on the Tibetan Plateau into five stages: stage 1 (continued arable land), stage 2 (arable abandoned for 2 years), stage 3 (arable abandoned for 10 years), stage 4 (arable abandoned for 20 years), and natural grassland. We investigated the changes in taxonomic and functional composition of bacterial and fungal communities in these successional stages.
Results
The richness of bacterial and fungal communities had a unimodal relationship with successional age, as the both were initially low and decreased again in natural grasslands. These changes were more correlated to soil properties. For both bacterial and fungal communities, taxonomic similarity to natural grasslands increased monotonously with successional age. The functional composition of bacterial communities shifted with successional age towards increased importance of strains involved in the C cycle rather than the N cycle, due to higher plant richness. For fungal communities, saprotrophs showed an increasing trend with successional age although low relative abundance in natural grasslands, which was regulated by belowground biomass. Symbiotrophs did not change during succession, but pathotrophic fungal relative abundance decreased rapidly after agricultural abandonment because of increased plant richness.
Conclusions
Overall, twenty years of oldfield succession did not appear to restore richness of soil bacterial and fungal communities to the levels of natural grasslands. Community taxonomic and functional composition in successional stages up to 20 y old were also different from natural grasslands. Our results suggest more important role of plant community than microbial community to soil nutrient cycling during restoration in oldfields.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The raw sequence data were submitted to the NCBI Sequence Read Archive under BioProject ID PRJNA850533 for bacteria and PRJNA997942 for fungi. Other data will be made available from the corresponding author on reasonable request.
References
An SS, Huang YM, Zheng FL (2009) Evaluation of soil microbial indices along a revegetation chronosequence in grassland soils on the Loess Plateau, Northwest China. Appl Soil Ecol 41:286–292. https://doi.org/10.1016/j.apsoil.2008.12.001
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Bahram M, Netherway T, Hildebrand F, Pritsch K, Drenkhan R, Loit K, Anslan S, Bork P, Tedersoo L (2020) Plant nutrient acquisition strategies drive topsoil microbiome structure and function. New Phytol 227:1189–1199. https://doi.org/10.1111/nph.16598
Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241. https://doi.org/10.1038/ismej.2013.104
Baumane M, Zak DH, Riis T, Kotowski W, Hoffmann CC, Baattrup-Pedersen A (2021) Danish wetlands remained poor with plant species 17-years after restoration. Sci Total Environ 798:149146. https://doi.org/10.1016/j.scitotenv.2021.149146
Bergelson J, Vivanco JM, Manter DK, Broz AK, Broeckling CD (2007) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744. https://doi.org/10.1128/AEM.02188-07
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Bordez L, Jourand P, Ducousso M, Carriconde F, Cavaloc Y, Santini S, Amir H (2016) Distribution patterns of microbial communities in ultramafic landscape: A metagenetic approach highlights the strong relationships between diversity and environmental traits. Mol Ecol 25:2258–2272. https://doi.org/10.1111/mec.13621
Breiman L (2001) Random forests. Machine Learning 45:5–32
Bullock JM, Aronson J, Newton AC, Pywell RF, Rey-Benayas JM (2011) Restoration of ecosystem services and biodiversity: conflicts and opportunities. Trends Ecol Evol 26:541–549. https://doi.org/10.1016/j.tree.2011.06.011
Burns JH, Anacker BL, Strauss SY, Burke DJ (2015) Soil microbial community variation correlates most strongly with plant species identity, followed by soil chemistry, spatial location and plant genus. AoB Plants 7:plv030. https://doi.org/10.1093/aobpla/plv030.
Byrnes RC, Nunez J, Arenas L, Rao I, Trujillo C, Alvarez C, Arango J, Rasche F, Chirinda N (2017) Biological nitrification inhibition by Brachiaria grasses mitigates soil nitrous oxide emissions from bovine urine patches. Soil Biol Biochem 107:156–163. https://doi.org/10.1016/j.soilbio.2016.12.029
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. https://doi.org/10.1038/nmeth.3869
Castle SC, Nemergut DR, Grandy AS, Leff JW, Graham EB, Hood E, Schmidt SK, Wickings K, Cleveland CC (2016) Biogeochemical drivers of microbial community convergence across actively retreating glaciers. Soil Biol Biochem 101:74–84. https://doi.org/10.1016/j.soilbio.2016.07.010
Chang CC, Turner BL (2019) Ecological succession in a changing world. J Ecol 107:503–509. https://doi.org/10.1111/1365-2745.13132
Chen D, Cheng JH, Chu PF, Hu SJ, Xie YC, Tuvshintogtokh I, Bai YF (2015) Regional-scale patterns of soil microbes and nematodes across grasslands on the Mongolian plateau: Relationships with climate, soil, and plants. Ecography 38:622–631. https://doi.org/10.1111/ecog.01226
Cline LC, Hobbie SE, Madritch MD, Buyarski CR, Tilman D, Cavender-Bares JM (2018) Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem. Ecology 99:204–216. https://doi.org/10.1002/ecy.2075
Cline LC, Zak DR (2015) Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96:3374–3385. https://doi.org/10.1890/15-0184.1
Cong J, Yang Y, Liu X, Lu H, Liu X, Zhou J, Li D, Yin H, Ding J, Zhang Y (2015) Analyses of soil microbial community compositions and functional genes reveal potential consequences of natural forest succession. Sci Rep 5:10007. https://doi.org/10.1038/srep10007
Dini-Andreote F, Pylro VS, Baldrian P, van Elsas JD, Salles JF (2016) Ecological succession reveals potential signatures of marine–terrestrial transition in salt marsh fungal communities. ISME J 10:1984–1997. https://doi.org/10.1038/ismej.2015.254
Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep 7:44641. https://doi.org/10.1038/srep44641
Fahey C, Koyama A, Antunes PM, Dunfield K, Luke FS (2020) Plant communities mediate the interactive effects of invasion and drought on soil microbial communities. ISME J 14:1396–1409. https://doi.org/10.1038/s41396-020-0614-6
Fierer N, Nemergut D, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161:635–642. https://doi.org/10.1016/j.resmic.2010.06.002
Fierer N (2017) Embracing the unknown: Disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590. https://doi.org/10.1038/nrmicro.2017.87
Garcia de Leon D, Moora M, Opik M, Neuenkamp L, Gerz M, Jairus T, Zobel M (2016) Symbiont dynamics during ecosystem succession: Co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 92:1–9. https://doi.org/10.1093/femsec/fiw097
Gawecka KA, Bascompte J (2023) Habitat restoration and the recovery of metacommunities. J Appl Ecol 00:1–15. https://doi.org/10.1111/1365-2664.14445
Gerrits GM, Waenink R, Aradottir AL, Buisson E, Dutoit T, Ferreira MC et al (2023) Synthesis on the effectiveness of soil translocation for plant community restoration. J Appl Ecol 00:1–11. https://doi.org/10.1111/1365-2664.14364
Grace JB (2006) Structural Equation Modeling and Natural Systems. Cambridge University Press, Cambridge
Grime JP (2001) Plant Strategies, Vegetation Processes, and Ecosystem Properties. John Wiley and Sons, Chichester
Guo Y, Hou L, Zhang Z, Zhang J, Cheng J, Wei G, Lin Y (2019) Soil microbial diversity during 30 years of grassland restoration on the Loess Plateau, China: Tight linkages with plant diversity. Land Degrad Dev 30:1172–1182. https://doi.org/10.1002/ldr.3300
Jackson ML (2005) Soil chemical analysis: Advanced course. UW-Madison Libraries parallel press
Jacoby R, Peukert M, Succurro A, Koprivova A, Kopriva S (2017) The role of soil microorganisms in plant mineral nutrition—Current knowledge and future directions. Front Plant Sci 8:1617. https://doi.org/10.3389/fpls.2017.01617
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 Biol Biochem 161. https://doi.org/10.1016/j.soilbio.2021.108393
Kaiser K, Wemheuer B, Korolkow V, Wemheuer F, Nacke H, Schoning I, Schrumpf M, Daniel R (2016) Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests. Sci Rep 6:33696. https://doi.org/10.1038/srep33696
Kitson RE, Mellon MG (1944) Colorimetric determination of phosphorus as molybdivanadophosphoric acid. Ind Eng Chem Ana Ed 16:379–383. https://doi.org/10.1021/i560130a017
Koziol L, Bever JD, Nuñez M (2017) The missing link in grassland restoration: Arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession. J Appl Ecol 54:1301–1309. https://doi.org/10.1111/1365-2664.12843
Kreyling J, Tanneberger F, Jansen F, van der Linden S, Aggenbach C, Blüml V (2021) Rewetting does not return drained fen peatlands to their old selves. Nat Commun 12:5693. https://doi.org/10.1038/s41467-021-25619-y
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microb 75:5111–5120. https://doi.org/10.1128/AEM.00335-09
Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. P Natl Acad Sci USA 112:10967–10972. https://doi.org/10.1073/pnas.1508382112
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2018) Emmeans: Estimated marginal means, aka least-squares means. R package version 1:3
Liu J, Jia X, Yan W, Zhong Y, Shangguan Z (2020) Changes in soil microbial community structure during long-term secondary succession. Land Degrad Dev 31:1151–1166. https://doi.org/10.1002/ldr.3505
Loreau M (2004) Does functional redundancy exist? Oikos 104:606–611. https://doi.org/10.1111/j.0030-1299.2004.12685.x
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277. https://doi.org/10.1126/science.aaf4507
Lozano YM, Hortal S, Armas C, Pugnaire FI (2014) Interactions among soil, plants, and microorganisms drive secondary succession in a dry environment. Soil Biol Biochem 78:298–306. https://doi.org/10.1016/j.soilbio.2014.08.007
Ma M, Baskin CC, Li W, Zhao Y, Zhao Y, Zhao L, Ning C, Du G (2019) Seed banks trigger ecological resilience in subalpine meadows abandoned after arable farming on the Tibetan Plateau. Ecol Appl 0:e01959. https://doi.org/10.1002/eap.1959.
Mehlich A (1984) Mehlich 3 soil test extractant: A modification of Mehlich 2 extractant. Commun Soil Sci Plan 15:1409–1416. https://doi.org/10.1080/00103628409367568
Midgley MG, Brzostek E, Phillips RP (2015) Decay rates of leaf litters from arbuscular mycorrhizal trees are more sensitive to soil effects than litters from ectomycorrhizal trees. J Ecol 103:1454–1463. https://doi.org/10.1111/1365-2745.12467
Moreno-Mateos D, Alberdi A, Morriën E, van der Putten WH, Rodríguez-Uña A, Montoya D (2020) The long-term restoration of ecosystem complexity. Nat Ecol Evol 4:676–685. https://doi.org/10.1038/s41559-020-1154-1
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Kennedy PG (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
Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glӧckner FO, Tedersoo L (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264. https://doi.org/10.1093/nar/gky1022
Pasternak Z, Al-Ashhab A, Gatica J, Gafny R, Avraham S, Minz D, Jurkevitch E (2013) Spatial and temporal biogeography of soil microbial communities in arid and semiarid regions. PLoS One 8:e69705. https://doi.org/10.1371/journal.pone.0069705
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
Prach K, Walker LR (2011) Four opportunities for studies of ecological succession. Trends Ecol Evol 26:119–123. https://doi.org/10.1016/j.tree.2010.12.007
Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, Fierer N (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18:85–95. https://doi.org/10.1111/ele.12381
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. https://doi.org/10.1111/1365-2435.13665
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
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. https://doi.org/10.1038/ismej.2010.138
Richter A, Schöning I, Kahl T, Bauhus J, Ruess L (2018) Regional environmental conditions shape microbial community structure stronger than local forest management intensity. Forest Ecol Manag 409:250–259. https://doi.org/10.1016/j.foreco.2017.11.027
Semchenko M, Leff JW, Lozano YM, Saar S, Davison J, Wilkinson A, Jackson BG, Pritchard WJ, DeLong JR, Oakley S, Mason KE, Ostle NJ, Baggs EM, Johnson D, Fierer N, Bardgett RD (2018) Fungal diversity regulates plant-soil feedbacks in temperate grassland. Sci Adv 4:eaau4578. https://doi.org/10.1126/sciadv.aau457
Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368. https://doi.org/10.1890/08-1034.1
Smith AP, Marin-Spiotta E, Balser T (2015) Successional and seasonal variations in soil and litter microbial community structure and function during tropical postagricultural forest regeneration: a multiyear study. Glob Change Biol 21:3532–3547. https://doi.org/10.1111/gcb.12947
Sun S, Li S, Avera BN, Strahm BD, Badgley BD (2017) Soil bacterial and fungal communities show distinct recovery patterns during forest ecosystem restoration. Appl Environ Microbiol 83:e00966–e00917. https://doi.org/10.1128/AEM.00966-17
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. https://doi.org/10.1038/s41396-018-0082-4
Turley NE, Bell-Dereske L, Evans SE, Brudvig LA (2020) Agricultural land-use history and restoration impact soil microbial biodiversity. J Appl Ecol 57:852–863. https://doi.org/10.1111/1365-2664.13591
Turner BL, Zemunik G, Laliberté E, Drake JJ, Jones FA, Saltonstall K (2019) Contrasting patterns of plant and microbial diversity during long-term ecosystem development. J Ecol 107:606–621. https://doi.org/10.1111/1365-2745.13127
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.1461-0248.2008.01199.x
Walker LR, Wardle DA (2014) Plant succession as an integrator of contrasting ecological time scales. Trends Ecol Evol 29:504–510. https://doi.org/10.1016/j.tree.2014.07.002
Walker LR, Walker J, Hobbs RJ (2007) Linking Restoration and Ecological Succession. Springer, The Netherlands, pp. 5e21.
Wang CY, Zhou X, Guo D, Zhao JH, Yan L, Feng GZ, Gao Q, Yu H, Zhao LP (2019) Soil pH is the primary factor driving the distribution and function of microorganisms in farmland soils in northeastern China. Ann Microbiol 69:1461–1473. https://doi.org/10.1007/s13213-019-01529-9
Wang H, Liu SR, Wang JX, Shi ZM, Xu J, Hong PZ, Ming AG, Yu HL, Chen L, Lu LH, Cai DX (2016) Differential effects of conifer and broadleaf litter inputs on soil organic carbon chemical composition through altered soil microbial community composition. Sci Rep 6:27097. https://doi.org/10.1038/srep27097
Wang S, Wang X, Han X, Deng Y (2018) Higher precipitation strengthens the microbial interactions in semi-arid grassland soils. Glob Ecol Biogeogr 27:570–580. https://doi.org/10.1111/geb.12718
Wubs ERJ, van der Putten WH, Bosch M, Bezemer TM (2016) Soil inoculation steers restoration of terrestrial ecosystems. Nat Plants 2:16107. https://doi.org/10.1038/nplants.2016.107
Xu Z, Ma Y, Zhang L, Han Y, Luo W (2021) Relating bacterial dynamics and functions to gaseous emissions during composting of kitchen and garden wastes. Sci Total Environ 767:144210. https://doi.org/10.1016/j.scitotenv.2020.144210
Yang F, Wu J, Zhang D, Chen Q, Zhang Q, Cheng X (2018) Soil bacterial community composition and diversity in relation to edaphic properties and plant traits in grasslands of southern China. Appl Soil Ecol 128:43–53. https://doi.org/10.1016/j.apsoil.2018.04.001
Yeomans JC, Bremner JM (1988) A rapid and precise method for routine determination of organic carbon in soil. Commun Soil Sci Plan 19:1467–1476. https://doi.org/10.1080/00103628809368027
Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: Are there any links? Ecology 84:2042–2050. https://doi.org/10.1890/02-0433
Zhang C, Liu G, Xue S, Wang G (2016a) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biol Biochem 97:40–49. https://doi.org/10.1016/j.soilbio.2016.02.013
Zhang C, Liu GB, Xue S, Wang GL (2015) Changes in rhizospheric microbial community structure and function during the natural recovery of abandoned cropland on the Loess Plateau, China. Ecol Eng 75:161–171. https://doi.org/10.1016/j.ecoleng.2014.11.059
Zhang H, Qi W, John R, Wang WB, Song FF, Zhou SR (2016b) Using functional trait diversity to evaluate the contribution of multiple ecological processes to community assembly during succession. Ecography 38:1176–1186. https://doi.org/10.1111/ecog.01123
Zhong Z, Zhang X, Wang X, Fu SY, Wu SJ, Lu XQ, Ren CJ, Han XH, Yang GH (2020) Soil bacteria and fungi respond differently to plant diversity and plant family composition during the secondary succession of abandoned farmland on the Loess Plateau China. Plant Soil 448:183–200. https://doi.org/10.1007/s11104-019-04415-0
Acknowledgements
We thank Pengpeng Wang for invaluable help in fieldwork. We are grateful to Prof. Manuel Delgado Baquerizo for his comments on the manuscript. This study was financially supported by the National Key R&D Program of China (2017YFC0504801), and the Key Research Program of Gansu (20ZD7FA005, 22ZD6NA007). Hui Ma is supported by the Chinese Scholarship Council joint PhD scholarship.
Author information
Authors and Affiliations
Contributions
ZGZ, HM, XMS, ZZH conceived the ideas and designed methodology; ZGZ received the funding; HM, XPY, YZQ, ELG, XFS, SW and YXW finished filed and laboratory work; HM performed the data processing and statistical analysis; HM, ZGZ, HHB and XMS led the writing and comment of the manuscript. All authors contributed critically to the writing and editing drafts and gave final approval for publication.
Corresponding authors
Ethics declarations
Competing interests
The authors declare that the research was no conflict of any commercial or financial relationships.
Additional information
Responsible Editor: Matthew A. Bowker.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOC 150 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.
About this article
Cite this article
Ma, H., Yan, X., Gao, E. et al. Changes in composition and function of soil microbial communities during secondary succession in oldfields on the Tibetan Plateau. Plant Soil 495, 429–443 (2024). https://doi.org/10.1007/s11104-023-06336-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06336-5