INTRODUCTION: Revegetation of barren substrates is often determined by the composition and distance of the nearest plant community, serving as a source of colonizing propagules. Whether such dispersal effect can be observed during the development of soil microbial communities, is not clear. In this study, we aimed to elucidate which factors structure plant and soil bacterial and fungal communities during primary succession on a limestone quarry spoil heap, focusing on the effect of distance to the adjoining xerophilous grassland. METHODS: We established a grid of 35 plots covering three successional stages - initial barren substrate, early successional community and late successional grassland ecosystem, the latter serving as the primary source of soil colonization. On these plots, we performed vegetation surveys of plant community composition and collected soil cores to analyze soil chemical properties and bacterial and fungal community composition. RESULTS: The composition of early successional plant community was significantly affected by the proximity of the source late successional community, however, the effect weakened when the distance exceeded 20 m. Early successional microbial communities were structured mainly by the local plant community composition and soil chemical properties, with minimal contribution of the source community proximity. DISCUSSION: These results show that on small spatial scales, species migration is an important determinant of plant community composition during primary succession while the establishment of soil microbial communities is not limited by dispersal and is primarily driven by local biotic and abiotic conditions.

Department of Botany Faculty of Science Charles University Prague Prague Czechia

Department of Forest Ecology and Management Swedish University of Agricultural Sciences Umeå Sweden

Institute of Botany of the CAS Průhonice Czechia

Institute of Microbiology of the CAS Prague Czechia

University of Chemistry and Technology Praha Czechia

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Anderson M. J., Ellingsen K. E., McArdle B. H. (2006). Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9, 683–693. doi: 10.1111/J.1461-0248.2006.00926.X, PMID: PubMed DOI

Aronesty E. (2013). Comparison of sequencing utility programs. Open Bioinf. J. 7, 1–8. doi: 10.2174/1875036201307010001 DOI

Barbour K. M., Barrón-Sandoval A., Walters K. E., Martiny J. B. H. (2023). Towards quantifying microbial dispersal in the environment. Environ. Microbiol. 25, 137–142. doi: 10.1111/1462-2920.16270, PMID: PubMed DOI PMC

Bengtsson-Palme J., Ryberg M., Hartmann M., Branco S., Wang Z., Godhe A., et al. . (2013). Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 4, 914–919. doi: 10.1111/2041-210X.12073 DOI

Bever J. D., Platt T. G., Morton E. R. (2012). Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Ann. Rev. Microbiol. 66, 265–283. doi: 10.1146/annurev-micro-092611-150107, PMID: PubMed DOI PMC

Borcard D., Legendre P. (2002). All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol. Model. 153, 51–68. doi: 10.1016/S0304-3800(01)00501-4 DOI

Broeckling C. D., Broz A. K., Bergelson J., Manter D. K., Vivanco J. M. (2008). Root exudates regulate soil fungal community composition and diversity. Appl. Environ. Microbiol. 74, 738–744. doi: 10.1128/AEM.02188-07, PMID: PubMed DOI PMC

Caporaso J. G., Lauber C. L., Walters W. A., Berg-Lyons D., Huntley J., Fierer N., et al. . (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624. doi: 10.1038/ismej.2012.8, PMID: PubMed DOI PMC

Chen Y. L., Xu T.-L., Veresoglou S. D., Hu H. W., Hao Z. P., Hu Y. J., et al. . (2017). Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in northern China. Soil Biol. Biochem. 110, 12–21. doi: 10.1016/j.soilbio.2017.02.015 DOI

Cheplick G. P. (2022). Philomatry in plants: why do so many species have limited seed dispersal? Am. J. Bot. 109, 29–45. doi: 10.1002/AJB2.1791, PMID: PubMed DOI

Cline L. C., Zak D. R. (2015). Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96, 3374–3385. doi: 10.1890/15-0184.1, PMID: PubMed DOI

Cole J. R., Wang Q., Fish J. A., Chai B., McGarrell D. M., Sun Y., et al. . (2014). Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633–D642. doi: 10.1093/nar/gkt1244, PMID: PubMed DOI PMC

Dassen S., Cortois R., Martens H., de Hollander M., Kowalchuk G. A., van der Putten W. H., et al. . (2017). Differential responses of soil bacteria, fungi, archaea and protists to plant species richness and plant functional group identity. Mol. Ecol. 26, 4085–4098. doi: 10.1111/mec.14175, PMID: PubMed DOI

Dray S., Bauman D., Blanchet G., Borcard D., Clappe S., Guénard G., et al. , (2023), {adespatial}: Multivariate Multiscale Spatial Analysis.

Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998. doi: 10.1038/nmeth.2604 PubMed DOI

Eisenhauer N., Lanoue A., Strecker T., Scheu S., Steinauer K., Thakur M. P., et al. . (2017). Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci. Rep. 7:44641. doi: 10.1038/srep44641, PMID: PubMed DOI PMC

Fischer C., Leimer S., Roscher C., Ravenek J., de Kroon H., Kreutziger Y., et al. . (2019). Plant species richness and functional groups have different effects on soil water content in a decade-long grassland experiment. J. Ecol. 107, 127–141. doi: 10.1111/1365-2745.13046 DOI

García de León D., Moora M., Öpik M., Jairus T., Neuenkamp L., Vasar M., et al. . (2016). Dispersal of arbuscular mycorrhizal fungi and plants during succession. Acta Oecol. 77, 128–135. doi: 10.1016/j.actao.2016.10.006 DOI

Golan J. J., Pringle A. (2017). Long-distance dispersal of fungi. Microbiol. Spectrum 5:FUNK-0047-2016. doi: 10.1128/microbiolspec.funk-0047-2016 PubMed DOI

Grosdidier M., Ioos R., Husson C., Cael O., Scordia T., Marçais B. (2018). Tracking the invasion: dispersal of Hymenoscyphus fraxineus airborne inoculum at different scales. FEMS Microbiol. Ecol. 94:fiy049. doi: 10.1093/FEMSEC/FIY049 PubMed DOI

Guasconi D., Juhanson J., Clemmensen K. E., Cousins S. A. O., Hugelius G., Manzoni S., et al. . (2023). Vegetation, topography, and soil depth drive microbial community structure in two Swedish grasslands. FEMS Microbiol. Ecol. 99:fiad080. doi: 10.1093/FEMSEC/FIAD080 PubMed DOI PMC

Harantová L., Mudrák O., Kohout P., Elhottová D., Frouz J., Baldrian P. (2017). Development of microbial community during primary succession in areas degraded by mining activities. Land Degrad. Dev. 28, 2574–2584. doi: 10.1002/ldr.2817 DOI

Hawkins H. J., Cargill R. I. M., Van Nuland M. E., Hagen S. C., Field K. J., Sheldrake M., et al. . (2023). Mycorrhizal mycelium as a global carbon pool. Curr. Biol. 33, R560–R573. doi: 10.1016/J.CUB.2023.02.027 PubMed DOI

Herrera Paredes S., Lebeis S. L. (2016). Giving back to the community: microbial mechanisms of plant–soil interactions. Funct. Ecol. 30, 1043–1052. doi: 10.1111/1365-2435.12684 DOI

Hiiesalu I., Pärtel M., Davison J., Gerhold P., Metsis M., Moora M., et al. . (2014). Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol. 203, 233–244. doi: 10.1111/nph.12765, PMID: PubMed DOI

Huffman J. A., Prenni A. J., Demott P. J., Pöhlker C., Mason R. H., Robinson N. H., et al. . (2013). High concentrations of biological aerosol particles and ice nuclei during and after rain. Atmos. Chem. Phys. 13, 6151–6164. doi: 10.5194/acp-13-6151-2013 DOI

Ihrmark K., Bödeker I. T. M., Cruz-Martinez K., Friberg H., Kubartova A., Schenck J., et al. . (2012). New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol. Ecol. 82, 666–677. doi: 10.1111/j.1574-6941.2012.01437.x, PMID: PubMed DOI

Junker R. R., He X., Otto J. C., Ruiz-Hernández V., Hanusch M. (2021). Divergent assembly processes? A comparison of the plant and soil microbiome with plant communities in a glacier forefield. FEMS Microbiol. Ecol. 97:fiab135. doi: 10.1093/femsec/fiab135, PMID: PubMed DOI PMC

Kallenbach C. M., Frey S. D., Grandy A. S. (2016). Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7:13630. doi: 10.1038/ncomms13630, PMID: PubMed DOI PMC

Knappová J., Münzbergová Z. (2015). Low seed pressure and competition from resident vegetation restricts dry grassland specialists to edges of abandoned fields. Agric. Ecosyst. Environ. 200, 200–207. doi: 10.1016/J.AGEE.2014.11.008 DOI

Knelman J. E., Legg T. M., O’Neill S. P., Washenberger C. L., González A., Cleveland C. C., et al. . (2012). Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biol. Biochem. 46, 172–180. doi: 10.1016/j.soilbio.2011.12.001 DOI

Kubát K., Bělohlávková R. (2002). Klíč ke květeně České republiky:927.

Kuťáková E., Mészárošová L., Baldrian P., Münzbergová Z. (2020). Evaluating the role of biotic and chemical components of plant-soil feedback of primary successional plants. Biol. Fertil. Soils 56, 345–358. doi: 10.1007/s00374-019-01425-z DOI

Lal R., Rattan Lal C. (2020). Soil organic matter and water retention. Agron. J. 112, 3265–3277. doi: 10.1002/AGJ2.20282 DOI

Lanta V., Lepš J. (2009). How does surrounding vegetation affect the course of succession: a five-year container experiment. J. Veg. Sci. 20, 686–694. doi: 10.1111/J.1654-1103.2009.01061.X DOI

Legendre P., Borcard D., Peres-Neto P. R. (2005). Analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol. Monogr. 75, 435–450. doi: 10.1890/05-0549 DOI

Lemoine N. P., Adams B. J., Diaz M., Dragone N. B., Franco A. L. C., Fierer N., et al. . (2023). Strong dispersal limitation of microbial communities at Shackleton glacier. MSystems 8:e0125422. doi: 10.1128/msystems.01254-22, PMID: PubMed DOI PMC

Lepinay C., Větrovský T., Chytrý M., Dřevojan P., Fajmon K., Cajthaml T., et al. . (2024). Effect of plant communities on bacterial and fungal communities in a central European grassland. Environ. Microb. 19, 1–19. doi: 10.1186/s40793-024-00583-4, PMID: PubMed DOI PMC

Lichter J. (2000). Colonization constraints during primary succession on coastal Lake Michigan sand dunes. J. Ecol. 88, 825–839. doi: 10.1046/J.1365-2745.2000.00503.X DOI

Liu X., Zhang L., Huang M., Zhou S. (2021). Plant diversity promotes soil fungal pathogen richness under fertilization in an alpine meadow. J. Plant Ecol. 14, 323–336. doi: 10.1093/JPE/RTAA099 DOI

López-Mondéjar R., Brabcová V., Štursová M., Davidová A., Jansa J., Cajthaml T., et al. . (2018). Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling. ISME J. 12, 1768–1778. doi: 10.1038/s41396-018-0084-2, PMID: PubMed DOI PMC

Makoto K., Wilson S. D. (2019). When and where does dispersal limitation matter in primary succession? J. Ecol. 107, 559–565. doi: 10.1111/1365-2745.12988 DOI

Mészárošová L., Kuťáková E., Kohout P., Münzbergová Z., Baldrian P. (2024). Plant effects on microbiome composition are constrained by environmental conditions in a successional grassland. Environ. Microb. 19:8. doi: 10.1186/s40793-024-00550-z, PMID: PubMed DOI PMC

Navrátilová D., Tláskalová P., Kohout P., Dřevojan P., Fajmon K., Chytrý M., et al. . (2018). Diversity of fungi and bacteria in species-rich grasslands increases with plant diversity in shoots but not in roots and soil. FEMS Microbiol. Ecol. 95:fiy208. doi: 10.1093/femsec/fiy208 PubMed DOI

Nemergut D. R., Anderson S. P., Cleveland C. C., Martin A. P., Miller A. E., Seimon A., et al. . (2007). Microbial community succession in an unvegetated, recently deglaciated soil. Microb. Ecol. 53, 110–122. doi: 10.1007/s00248-006-9144-7, PMID: PubMed DOI

Nilsson R. H., Larsson K. H., Taylor A. F. S., Bengtsson-Palme J., Jeppesen T. S., Schigel D., et al. . (2019). The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 47, D259–D264. doi: 10.1093/nar/gky1022, PMID: PubMed DOI PMC

Novák J., Konvička M. (2006). Proximity of valuable habitats affects succession patterns in abandoned quarries. Ecol. Eng. 26, 113–122. doi: 10.1016/j.ecoleng.2005.06.008 DOI

Oksanen J., Simpson G. L., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., et al. , (2022). Vegan: community ecology package

Peay K. G., Schubert M. G., Nguyen N. H., Bruns T. D. (2012). Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol. Ecol. 21, 4122–4136. doi: 10.1111/j.1365-294X.2012.05666.x, PMID: PubMed DOI

Põlme S., Abarenkov K., Henrik Nilsson R., Lindahl B. D., Clemmensen K. E., Kauserud H., et al. . (2020). FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 105, 1–16. doi: 10.1007/s13225-020-00466-2 DOI

Powell J. R., Karunaratne S., Campbell C. D., Yao H., Robinson L., Singh B. K. (2015). Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat. Commun. 6:8444. doi: 10.1038/ncomms9444, PMID: PubMed DOI PMC

Prober S. M., Leff J. W., Bates S. T., Borer E. T., Firn J., Harpole W. S., et al. . (2015). Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol. Lett. 18, 85–95. doi: 10.1111/ele.12381 PubMed DOI

R Core Team and R Development Core Team , (2021). R: a Language and Environment for Statistical Computing

Redondo M. A., Berlin A., Boberg J., Oliva J. (2020). Vegetation type determines spore deposition within a forest-agricultural mosaic landscape. FEMS Microbiol. Ecol. 96:fiaa082. doi: 10.1093/femsec/fiaa082, PMID: PubMed DOI PMC

Řezáčová V., Slavíková R., Konvalinková T., Zemková L., Řezáč M., Gryndler M., et al. . (2019). Geography and habitat predominate over climate influences on arbuscular mycorrhizal fungal communities of mid-European meadows. Mycorrhiza 29, 567–579. doi: 10.1007/s00572-019-00921-2, PMID: PubMed DOI

Sagova-Mareckova M., Cermak L., Novotna J., Plhackova K., Forstova J., Kopecky J. (2008). Innovative methods for soil DNA purification tested in soils with widely differing characteristics. Appl. Environ. Microbiol. 74, 2902–2907. doi: 10.1128/AEM.02161-07, PMID: PubMed DOI PMC

Santonja M., Rancon A., Fromin N., Baldy V., Hättenschwiler S., Fernandez C., et al. . (2017). Plant litter diversity increases microbial abundance, fungal diversity, and carbon and nitrogen cycling in a Mediterranean shrubland. Soil Biol. Biochem. 111, 124–134. doi: 10.1016/J.SOILBIO.2017.04.006 DOI

Scherling C., Roscher C., Giavalisco P., Schulze E. D., Weckwerth W. (2010). Metabolomics unravel contrasting effects of biodiversity on the performance of individual plant species. PLoS One 5:e12569. doi: 10.1371/journal.pone.0012569, PMID: PubMed DOI PMC

Schmidt S. K., Nemergut D. R., Darcy J. L., Lynch R. (2014). Do bacterial and fungal communities assemble differently during primary succession? Mol. Ecol. 23, 254–258. doi: 10.1111/mec.12589, PMID: PubMed DOI

Schnitzer S. A., Klironomos J. N., HilleRisLambers J., Kinkel L. L., Reich P. B., Xiao K., et al. . (2011). Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92, 296–303. doi: 10.1890/10-0773.1, PMID: PubMed DOI

Schulz S., Brankatschk R., Dümig A., Kögel-Knabner I., Schloter M., Zeyer J. (2013). The role of microorganisms at different stages of ecosystem development for soil formation. Biogeosciences 10, 3983–3996. doi: 10.5194/bg-10-3983-2013 DOI

Schulz-Bohm K., Gerards S., Hundscheid M., Melenhorst J., De Boer W., Garbeva P. (2018). Calling from distance: attraction of soil bacteria by plant root volatiles. ISME J. 12, 1252–1262. doi: 10.1038/S41396-017-0035-3, PMID: PubMed DOI PMC

Steinauer K., Chatzinotas A., Eisenhauer N. (2016). Root exudate cocktails: the link between plant diversity and soil microorganisms? Ecol. Evol. 6, 7387–7396. doi: 10.1002/ece3.2454, PMID: PubMed DOI PMC

Tláskal V., Voříšková J., Baldrian P. (2016). Bacterial succession on decomposing leaf litter exhibits a specific occurrence pattern of cellulolytic taxa and potential decomposers of fungal mycelia. FEMS Microbiol. Ecol. 92:fiw177. doi: 10.1093/femsec/fiw177, PMID: PubMed DOI

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 Biology and Biochemistry 8453–64. doi: 10.1016/j.soilbio.2015.02.011, PMID: PubMed DOI

Větrovský T., Baldrian P., Morais D. (2018). SEED 2: a user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics 34, 2292–2294. doi: 10.1093/bioinformatics/bty071, PMID: PubMed DOI PMC

Vos M., Wolf A. B., Jennings S. J., Kowalchuk G. A. (2013). Micro-scale determinants of bacterial diversity in soil. FEMS Microbiol. Rev. 37, 936–954. doi: 10.1111/1574-6976.12023, PMID: PubMed DOI

Walker L. R., Moral R. (2011). Primary succession. Encyclopedia of life sciences

Wang C., Ma L., Zuo X., Ye X., Wang R., Huang Z., et al. . (2022a). Plant diversity has stronger linkage with soil fungal diversity than with bacterial diversity across grasslands of northern China. Glob. Ecol. Biogeogr. 31, 886–900. doi: 10.1111/GEB.13462 DOI

Wang J., Wang Y., Qu M., Li J. (2022b). Dispersal limitation dominates the community assembly of abundant and rare fungi in dryland montane forests. Front. Microbiol. 13:929772. doi: 10.3389/FMICB.2022.929772/BIBTEX PubMed DOI PMC

Yang T., Adams J. M., Shi Y., He J. S., Jing X., Chen L., et al. . (2017). Soil fungal diversity in natural grasslands of the Tibetan plateau: associations with plant diversity and productivity. New Phytol. 215, 756–765. doi: 10.1111/nph.14606, PMID: PubMed DOI

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. doi: 10.1016/j.apsoil.2018.04.001 DOI

Zbíral J. (2002). Analýza půd I. Laboratorní odbor: Ústřední kontrolní a zkušební Ústav zemědělský.

Zhang G., Wei G., Wei F., Chen Z., He M., Jiao S., et al. . (2021). Dispersal limitation plays stronger role in the community assembly of fungi relative to bacteria in rhizosphere across the arable area of medicinal plant. Front. Microbiol. 12:713523. doi: 10.3389/FMICB.2021.713523/BIBTEX PubMed DOI PMC

Žifčáková L., Větrovský T., Howe A., Baldrian P. (2016). Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ. Microbiol. 18, 288–301. doi: 10.1111/1462-2920.13026, PMID: PubMed DOI