Elucidating dynamics of soil microbial communities after disturbance is crucial for understanding ecosystem restoration and sustainability. However, despite the widespread practice of swidden agriculture in tropical forests, knowledge about microbial community succession in this system is limited. Here, amplicon sequencing was used to investigate effects of soil ages (spanning at least 60 years) after disturbance, geographic distance (from 0.1 to 10 km) and edaphic property gradients (soil pH, conductivity, C, N, P, Ca, Mg, and K), on soil bacterial and fungal communities along a chronosequence of sites representing the spontaneous succession following swidden agriculture in lowland forests in Papua New Guinea. During succession, bacterial communities (OTU level) as well as its abundant (OTU with relative abundance > 0.5%) and rare (<0.05%) subcommunities, showed less variation but more stage-dependent patterns than those of fungi. Fungal community dynamics were significantly associated only with geographic distance, whereas bacterial community dynamics were significantly associated with edaphic factors and geographic distance. During succession, more OTUs were consistently abundant (n = 12) or rare (n = 653) for bacteria than fungi (abundant = 6, rare = 5), indicating bacteria were more tolerant than fungi to environmental gradients. Rare taxa showed higher successional dynamics than abundant taxa, and rare bacteria (mainly from Actinobacteria, Proteobacteria, Acidobacteria, and Verrucomicrobia) largely accounted for bacterial community development and niche differentiation during succession.

Biology Centre of the Czech Academy of Sciences Institute of Soil Biology and SoWa Research Infrastructure České Budějovice Czechia

Department of Geosciences and Natural Resource Management Faculty of Science University of Copenhagen Frederiksberg Denmark

Engineering Research Center of Soil Remediation of Fujian Province University College of Resources and Environment Fujian Agriculture and Forestry University Fuzhou China

Faculty of Science Institute for Environmental Studies Charles University Praha Czechia

Institute of Entomology Biology Centre of the Czech Academy of Sciences and University of South Bohemia České Budějovice Czechia

Laboratory of Environmental Microbiology Institute of Microbiology of the CAS Praha Czechia

New Guinea Binatang Research Center Madang Papua New Guinea

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Are K. S., Oluwatosin G. A., Adeyolanu O. D., Oke A. O. (2009). Slash and burn effect on soil quality of an Alfisol: soil physical properties. DOI

Banning N. C., Gleeson D. B., Grigg A. H., Grant C. D., Andersen G. L., Brodie E. L., et al. (2011). Soil microbial community successional patterns during forest ecosystem restoration. PubMed DOI PMC

Blanchet F. G., Legendre P., Borcard D. (2008). Forward selection of explanatory variables. PubMed DOI

Brown S. P., Jumpponen A. (2014). Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils. PubMed DOI

Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. PubMed DOI PMC

Chai Y., Cao Y., Yue M., Tian T., Yin Q., Dang H., et al. (2019). Soil abiotic properties and plant functional traits mediate associations between soil microbial and plant communities during a secondary forest succession on the Loess Plateau. PubMed DOI PMC

Chase J. M., Kraft N. J., Smith K. G., Vellend M., Inouye B. D. (2011). Using null models to disentangle variation in community dissimilarity from variation in α−diversity.

Dawkins K., Esiobu N. (2018). The Invasive Brazilian Pepper Tree ( PubMed DOI PMC

de Boer W., Folman L. B., Summerbell R. C., Boddy L. (2005). Living in a fungal world: impact of fungi on soil bacterial niche development. PubMed DOI

De Mandal S., Chatterjee R., Kumar N. S. (2017). Dominant bacterial phyla in caves and their predicted functional roles in C and N cycle. PubMed DOI PMC

Dini-Andreote F., Stegen J. C., van Elsas J. D., Salles J. F. (2015). Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. PubMed DOI PMC

Edgar R. C., Flyvbjerg H. (2015). Error filtering, pair assembly and error correction for next-generation sequencing reads. PubMed DOI

Edwards P., Grubb P. (1977). Studies of mineral cycling in a montane rain forest in New Guinea: I. The distribution of organic matter in the vegetation and soil. DOI

Franzetti A., Pittino F., Gandolfi I., Azzoni R., Diolaiuti G., Smiraglia C., et al. (2020). Early ecological succession patterns of bacterial, fungal and plant communities along a chronosequence in a recently deglaciated area of the Italian Alps. PubMed

Garrido-Benavent I., Pérez-Ortega S., Durán J., Ascaso C., Pointing S. B., Rodríguez-Cielos R., et al. (2020). Differential colonization and succession of microbial communities in rock and soil substrates on a maritime antarctic glacier forefield. PubMed DOI PMC

Gkarmiri K., Mahmood S., Ekblad A., Alstrom S., Hogberg N., Finlay R. (2017). Identifying the active microbiome associated with roots and rhizosphere soil of Oilseed Rape. PubMed DOI PMC

Goslee S. C., Urban D. L. (2007). The ecodist package for dissimilarity-based analysis of ecological data.

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. DOI

Harris J. (2009). Soil microbial communities and restoration ecology: facilitators or followers? PubMed DOI

Hartmann M., Niklaus P. A., Zimmermann S., Schmutz S., Kremer J., Abarenkov K., et al. (2014). Resistance and resilience of the forest soil microbiome to logging-associated compaction. PubMed DOI PMC

Hol W. G., De Boer W., Termorshuizen A. J., Meyer K. M., Schneider J. H., Van Dam N. M., et al. (2010). Reduction of rare soil microbes modifies plant–herbivore interactions. PubMed DOI

Huon S., De Rouw A., Bonté P., Robain H., Valentin C., Lefèvre I., et al. (2013). Long-term soil carbon loss and accumulation in a catchment following the conversion of forest to arable land in northern Laos. DOI

Jia X., Dini-Andreote F., Falcao Salles J. (2018). Community assembly processes of the microbial rare biosphere. PubMed DOI

Jiang Y. L., Song H. F., Lei Y. B., Korpelainen H., Li C. Y. (2019). Distinct co-occurrence patterns and driving forces of rare and abundant bacterial subcommunities following a glacial retreat in the eastern Tibetan Plateau. DOI

Jiao S., Chen W., Wei G. (2017). Biogeography and ecological diversity patterns of rare and abundant bacteria in oil-contaminated soils. PubMed DOI

Jousset A., Bienhold C., Chatzinotas A., Gallien L., Gobet A., Kurm V., et al. (2017). Where less may be more: how the rare biosphere pulls ecosystems strings. PubMed DOI PMC

Kukla J., Whitfeld T., Cajthaml T., Baldrian P., Veselá - Šimáčková H., Novotnı V., et al. (2018). The effect of traditional slash-and-burn agriculture on soil organic matter, nutrient content and microbiota in tropical ecosystems of New Guinea. DOI

Legendre P., Borcard D., Peres-Neto P. R. (2008). Analyzing or explaining beta diversity? PubMed DOI

Li W., Godzik A. (2006). Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. PubMed DOI

Lynch M. D., Neufeld J. D. (2015). Ecology and exploration of the rare biosphere. PubMed DOI

McAlpine J. R. (1983).

Melbourne B. A., Hastings A. (2008). Extinction risk depends strongly on factors contributing to stochasticity. PubMed DOI

Mo Y., Zhang W., Yang J., Lin Y., Yu Z., Lin S. (2018). Biogeographic patterns of abundant and rare bacterioplankton in three subtropical bays resulting from selective and neutral processes. PubMed DOI PMC

Murphy J., Riley J. P. (1962). A modified single solution method for the determination of phosphate in natural waters. DOI

Nguyen N. H., Song Z., Bates S. T., Branco S., Tedersoo L., Menke J., et al. (2016). FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. DOI

Ogle S. M., Breidt F. J., Paustian K. (2005). Agricultural management impacts on soil organic carbon storage under moist and dry climatic conditions of temperate and tropical regions. DOI

Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O’hara R., et al. (2013). Package ‘vegan’.

Pester M., Bittner N., Deevong P., Wagner M., Loy A. (2010). A ‘rare biosphere’microorganism contributes to sulfate reduction in a peatland. PubMed DOI PMC

Rivett D. W., Bell T. (2018). Abundance determines the functional role of bacterial phylotypes in complex communities. PubMed DOI PMC

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. PubMed DOI PMC

Shu D., Zhang B., He Y., Wei G. (2018). Abundant and rare microbial sub-communities in anammox granules present contrasting assemblage patterns and metabolic functions in response to inorganic carbon stresses. PubMed DOI

Sun S., Li S., Avera B. N., Strahm B. D., Badgley B. D. (2017). Soil bacterial and fungal communities show distinct recovery patterns during forest ecosystem restoration. PubMed DOI PMC

Urbanova M., Snajdr J., Baldrian P. (2015). Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. DOI

Wagg C., Bender S. F., Widmer F., van der Heijden M. G. A. (2014). Soil biodiversity and soil community composition determine ecosystem multifunctionality. PubMed DOI PMC

Wang J., Shen J., Wu Y., Tu C., Soininen J., Stegen J. C., et al. (2013). Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. PubMed DOI PMC

Wang N. F., Zhang T., Yang X., Wang S., Yu Y., Dong L. L., et al. (2016). Diversity and composition of bacterial community in soils and lake sediments from an Arctic Lake Area. PubMed DOI PMC

Whitfeld T. J. S., Kress W. J., Erickson D. L., Weiblen G. D. (2012). Change in community phylogenetic structure during tropical forest succession: evidence from New Guinea. DOI

Whitfeld T. J. S., Lasky J. R., Damas K., Sosanika G., Molem K., Montgomery R. A. (2014). Species richness, forest structure, and functional diversity during succession in the New Guinea Lowlands. DOI

Wood A. W. (1982). “The soils of New Guinea,” in DOI

Wu W., Logares R., Huang B., Hsieh C. H. (2017). Abundant and rare picoeukaryotic sub-communities present contrasting patterns in the epipelagic waters of marginal seas in the northwestern Pacific Ocean. PubMed DOI

Xiao X., Liang Y., Zhou S., Zhuang S., Sun B. (2018). Fungal community reveals less dispersal limitation and potentially more connected network than that of bacteria in bamboo forest soils. PubMed DOI

Yachi S., Loreau M. (1999). Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. PubMed DOI PMC

Yan W., Ma H., Shi G., Li Y., Sun B., Xiao X., et al. (2017). Independent shifts of abundant and rare bacterial populations across East Antarctica Glacial Foreland. PubMed DOI PMC

Zhang J., Zhang B., Liu Y., Guo Y., Shi P., Wei G. (2018). Distinct large-scale biogeographic patterns of fungal communities in bulk soil and soybean rhizosphere in China. PubMed DOI

Zhou J., Deng Y., Zhang P., Xue K., Liang Y., Van Nostrand J. D., et al. (2014). Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. PubMed DOI PMC

Zimmermann M., Leifeld J., Schmidt M., Smith P., Fuhrer J. (2007). Measured soil organic matter fractions can be related to pools in the RothC model. DOI

Regional biogeography versus intra-annual dynamics of the root and soil microbiome