The rhizosphere is the hotspot for microbial enzyme activities and contributes to carbon cycling. Precipitation is an important component of global climate change that can profoundly alter belowground microbial communities. However, the impact of precipitation on conifer rhizospheric microbial populations has not been investigated in detail. In the present study, using high-throughput amplicon sequencing, we investigated the impact of precipitation on the rhizospheric soil microbial communities in two Norway Spruce clonal seed orchards, Lipová Lhota (L-site) and Prenet (P-site). P-site has received nearly double the precipitation than L-site for the last three decades. P-site documented higher soil water content with a significantly higher abundance of Aluminium (Al), Iron (Fe), Phosphorous (P), and Sulphur (S) than L-site. Rhizospheric soil metabolite profiling revealed an increased abundance of acids, carbohydrates, fatty acids, and alcohols in P-site. There was variance in the relative abundance of distinct microbiomes between the sites. A higher abundance of Proteobacteria, Acidobacteriota, Ascomycota, and Mortiellomycota was observed in P-site receiving high precipitation, while Bacteroidota, Actinobacteria, Chloroflexi, Firmicutes, Gemmatimonadota, and Basidiomycota were prevalent in L-site. The higher clustering coefficient of the microbial network in P-site suggested that the microbial community structure is highly interconnected and tends to cluster closely. The current study unveils the impact of precipitation variations on the spruce rhizospheric microbial association and opens new avenues for understanding the impact of global change on conifer rizospheric microbial associations.

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Kamýcká 129 Suchdol 165 21 Prague Czech Republic

Faculty of Science Charles University Prague BIOCEV Průmyslová 595 Vestec 252 42 Prague Czech Republic

Molecular Plant and Microbiology Laboratory Post Graduate Department of Botany Ramakrishna Mission Vivekananda Centenary College Rahara Kolkata 700118 India

See more in PubMed

Baldrian P. Forest microbiome: Diversity, complexity and dynamics. FEMS Microbiol. Rev. 2017;41:109–130. doi: 10.1093/femsre/fuw040. PubMed DOI

Lladó S., López-Mondéjar R., Baldrian P. Forest soil bacteria: Diversity, involvement in ecosystem processes, and response to global change. Microbiol. Mol. Biol. Rev. 2017;81:10–1128. doi: 10.1128/MMBR.00063-16. PubMed DOI PMC

Malhi Y., Baldocchi D., Jarvis P. The carbon balance of tropical, temperate and boreal forests. Plant Cell Environ. 1999;22:715–740. doi: 10.1046/j.1365-3040.1999.00453.x. DOI

Martinović T., Mašínová T., López-Mondéjar R., Jansa J., Štursová M., Starke R., Baldrian P. Microbial utilization of simple and complex carbon compounds in a temperate forest soil. Soil Biol. Biochem. 2022;173:108786. doi: 10.1016/j.soilbio.2022.108786. DOI

Li X., Yan Y., Lu X., Fu L., Liu Y. Responses of soil bacterial communities to precipitation change in the semi-arid alpine grassland of Northern Tibet. Front. Plant Sci. 2022;13:1036369. doi: 10.3389/fpls.2022.1036369. PubMed DOI PMC

He R., Yang K., Li Z., Schädler M., Yang W., Wu F., Tan B., Zhang L., Xu Z. Effects of forest conversion on soil microbial communities depend on soil layer on the eastern Tibetan Plateau of China. PLoS ONE. 2017;12:e0186053. doi: 10.1371/journal.pone.0186053. PubMed DOI PMC

Philippot L., Raaijmakers J.M., Lemanceau P., Van Der Putten W.H. Going back to the roots: The microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 2013;11:789–799. doi: 10.1038/nrmicro3109. PubMed DOI

Mohanram S., Kumar P. Rhizosphere microbiome: Revisiting the synergy of plant-microbe interactions. Ann. Microbiol. 2019;69:307–320. doi: 10.1007/s13213-019-01448-9. DOI

Berendsen R.L., Pieterse C.M., Bakker P.A. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–486. doi: 10.1016/j.tplants.2012.04.001. PubMed DOI

Park I., Seo Y.-S., Mannaa M. Recruitment of the rhizo-microbiome army: Assembly determinants and engineering of the rhizosphere microbiome as a key to unlocking plant potential. Front. Microbiol. 2023;14:1163832. doi: 10.3389/fmicb.2023.1163832. PubMed DOI PMC

Bakker P.A., Berendsen R.L., Doornbos R.F., Wintermans P.C., Pieterse C.M. The rhizosphere revisited: Root microbiomics. Front. Plant Sci. 2013;4:165. doi: 10.3389/fpls.2013.00165. PubMed DOI PMC

Trivedi P., Leach J.E., Tringe S.G., Sa T., Singh B.K. Plant–microbiome interactions: From community assembly to plant health. Nat. Rev. Microbiol. 2020;18:607–621. doi: 10.1038/s41579-020-0412-1. PubMed DOI

Masson-Delmotte V., Zhai P., Pirani A., Connors S.L., Péan C., Berger S., Caud N., Chen Y., Goldfarb L., Gomis M. Climate change 2021: The physical science basis. Contrib. Work. Group I Sixth Assess. Rep. Intergov. Panel Clim. Chang. 2021;2:2391.

Dietzen C.A., Larsen K.S., Ambus P.L., Michelsen A., Arndal M.F., Beier C., Reinsch S., Schmidt I.K. Accumulation of soil carbon under elevated CO2 unaffected by warming and drought. Glob. Chang. Biol. 2019;25:2970–2977. doi: 10.1111/gcb.14699. PubMed DOI

Zhou Z., Wang C., Luo Y. Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality. Nat. Commun. 2020;11:3072. doi: 10.1038/s41467-020-16881-7. PubMed DOI PMC

Meena M., Yadav G., Sonigra P., Nagda A., Mehta T., Swapnil P., Harish, Marwal A., Kumar S. Multifarious responses of forest soil microbial community toward climate change. Microb. Ecol. 2023;86:49–74. doi: 10.1007/s00248-022-02051-3. PubMed DOI

Li H., Xu Z., Yang S., Li X., Top E.M., Wang R., Zhang Y., Cai J., Yao F., Han X. Responses of soil bacterial communities to nitrogen deposition and precipitation increment are closely linked with aboveground community variation. Microb. Ecol. 2016;71:974–989. doi: 10.1007/s00248-016-0730-z. PubMed DOI

Wu K., Xu W., Yang W. Effects of precipitation changes on soil bacterial community composition and diversity in the Junggar desert of Xinjiang, China. PeerJ. 2020;8:e8433. doi: 10.7717/peerj.8433. PubMed DOI PMC

Bian H., Li C., Zhu J., Xu L., Li M., Zheng S., He N. Soil moisture affects the rapid response of microbes to labile organic C addition. Front. Ecol. Evol. 2022;10:857185. doi: 10.3389/fevo.2022.857185. DOI

Gomez E.J., Delgado J.A., Gonzalez J.M. Influence of water availability and temperature on estimates of microbial extracellular enzyme activity. PeerJ. 2021;9:e10994. doi: 10.7717/peerj.10994. PubMed DOI PMC

Schimel J.P. Life in dry soils: Effects of drought on soil microbial communities and processes. Annu. Rev. Ecol. Evol. Syst. 2018;49:409–432. doi: 10.1146/annurev-ecolsys-110617-062614. DOI

Shi S., Nuccio E., Herman D.J., Rijkers R., Estera K., Li J., Da Rocha U.N., He Z., Pett-Ridge J., Brodie E.L. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio. 2015;6 doi: 10.1128/mBio.00746-15. PubMed DOI PMC

Kokalis-Burelle N., McSorley R., Wang K.-H., Saha S.K., McGovern R.J. Rhizosphere microorganisms affected by soil solarization and cover cropping in Capsicum annuum and Phaseolus lunatus agroecosystems. Appl. Soil Ecol. 2017;119:64–71. doi: 10.1016/j.apsoil.2017.06.001. DOI

Smalla K., Wieland G., Buchner A., Zock A., Parzy J., Kaiser S., Roskot N., Heuer H., Berg G. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: Plant-dependent enrichment and seasonal shifts revealed. Appl. Environ. Microbiol. 2001;67:4742–4751. doi: 10.1128/AEM.67.10.4742-4751.2001. PubMed DOI PMC

Mercado-Blanco J., Abrantes I., Barra Caracciolo A., Bevivino A., Ciancio A., Grenni P., Hrynkiewicz K., Kredics L., Proença D.N. Belowground microbiota and the health of tree crops. Front. Microbiol. 2018;9:347012. doi: 10.3389/fmicb.2018.01006. PubMed DOI PMC

Yu L., Zi H., Zhu H., Liao Y., Xu X., Li X. Rhizosphere microbiome of forest trees is connected to their resistance to soil-borne pathogens. Plant Soil. 2022;479:143–158. doi: 10.1007/s11104-022-05505-2. DOI

Heděnec P., Zheng H., Siqueira D.P., Lin Q., Peng Y., Schmidt I.K., Frøslev T.G., Kjøller R., Rousk J., Vesterdal L. Tree species traits and mycorrhizal association shape soil microbial communities via litter quality and species mediated soil properties. For. Ecol. Manag. 2023;527:120608. doi: 10.1016/j.foreco.2022.120608. DOI

Maitra P., Hrynkiewicz K., Szuba A., Jagodziński A.M., Al-Rashid J., Mandal D., Mucha J. Metabolic niches in the rhizosphere microbiome: Dependence on soil horizons, root traits and climate variables in forest ecosystems. Front. Plant Sci. 2024;15:1344205. doi: 10.3389/fpls.2024.1344205. PubMed DOI PMC

Fu F., Li Y., Zhang B., Zhu S., Guo L., Li J., Zhang Y., Li J. Differences in soil microbial community structure and assembly processes under warming and cooling conditions in an alpine forest ecosystem. Sci. Total Environ. 2024;907:167809. doi: 10.1016/j.scitotenv.2023.167809. PubMed DOI

Morales-Rodríguez C., Martín-García J., Ruiz-Gómez F.J., Poveda J., Diez J.J. Relationships between rhizosphere microbiota and forest health conditions in Pinus pinaster stands at the Iberian Peninsula. Appl. Soil Ecol. 2024;193:105142. doi: 10.1016/j.apsoil.2023.105142. DOI

Zheng H., Liu Y., Chen Y., Zhang J., Li H., Wang L., Chen Q. Short-term warming shifts microbial nutrient limitation without changing the bacterial community structure in an alpine timberline of the eastern Tibetan Plateau. Geoderma. 2020;360:113985. doi: 10.1016/j.geoderma.2019.113985. DOI

White III R.A., Rivas-Ubach A., Borkum M.I., Köberl M., Bilbao A., Colby S.M., Hoyt D.W., Bingol K., Kim Y.-M., Wendler J.P. The state of rhizospheric science in the era of multi-omics: A practical guide to omics technologies. Rhizosphere. 2017;3:212–221. doi: 10.1016/j.rhisph.2017.05.003. DOI

Štraus D., Redondo M.Á., Castaño C., Juhanson J., Clemmensen K.E., Hallin S., Oliva J. Plant–soil feedbacks among boreal forest species. J. Ecol. 2024;112:138–151. doi: 10.1111/1365-2745.14224. DOI

Ault T.R. On the essentials of drought in a changing climate. Science. 2020;368:256–260. doi: 10.1126/science.aaz5492. PubMed DOI

Hu Y., Ganjurjav H., Hu G., Wang X., Wan Z., Gao Q. Seasonal patterns of soil microbial community response to warming and increased precipitation in a semiarid steppe. Appl. Soil Ecol. 2023;182:104712. doi: 10.1016/j.apsoil.2022.104712. DOI

Fontaine S., Barot S., Barré P., Bdioui N., Mary B., Rumpel C. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature. 2007;450:277–280. doi: 10.1038/nature06275. PubMed DOI

Kuzyakov Y. Priming effects: Interactions between living and dead organic matter. Soil Biol. Biochem. 2010;42:1363–1371. doi: 10.1016/j.soilbio.2010.04.003. DOI

Li C., Liu L., Zheng L., Yu Y., Mushinski R.M., Zhou Y., Xiao C. Greater soil water and nitrogen availability increase C: N ratios of root exudates in a temperate steppe. Soil Biol. Biochem. 2021;161:108384. doi: 10.1016/j.soilbio.2021.108384. DOI

Chakraborty A., Zádrapová D., Dvořák J., Faltinová Z., Žáček P., Cajthaml T., Korecký J., Roy A. Impact of 30 years precipitation regime differences on forest soil physiology and microbial assemblages. Front. For. Glob. Chang. 2023;6:1142979. doi: 10.3389/ffgc.2023.1142979. DOI

Zhang Y.-Y., Wu W., Liu H. Factors affecting variations of soil pH in different horizons in hilly regions. PLoS ONE. 2019;14:e0218563. PubMed PMC

Barnard R.L., Osborne C.A., Firestone M.K. Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J. 2013;7:2229–2241. doi: 10.1038/ismej.2013.104. PubMed DOI PMC

Elbert W., Weber B., Burrows S., Steinkamp J., Büdel B., Andreae M.O., Pöschl U. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 2012;5:459–462. doi: 10.1038/ngeo1486. DOI

Song Y., Yao S., Li X., Wang T., Jiang X., Bolan N., Warren C.R., Northen T.R., Chang S.X. Soil metabolomics: Deciphering underground metabolic webs in terrestrial ecosystems. Eco-Environ. Health. 2024;3:227–237. doi: 10.1016/j.eehl.2024.03.001. PubMed DOI PMC

Butcher K.R., Nasto M.K., Norton J.M., Stark J.M. Physical mechanisms for soil moisture effects on microbial carbon-use efficiency in a sandy loam soil in the western United States. Soil Biol. Biochem. 2020;150:107969. doi: 10.1016/j.soilbio.2020.107969. DOI

Zhao Y., Yao Y., Xu H., Xie Z., Guo J., Qi Z., Jiang H. Soil metabolomics and bacterial functional traits revealed the responses of rhizosphere soil bacterial community to long-term continuous cropping of Tibetan barley. PeerJ. 2022;10:e13254. doi: 10.7717/peerj.13254. PubMed DOI PMC

Bi B., Wang K., Zhang H., Wang Y., Fei H., Pan R., Han F. Plants use rhizosphere metabolites to regulate soil microbial diversity. Land Degrad. Dev. 2021;32:5267–5280. doi: 10.1002/ldr.4107. DOI

Shi S., Richardson A.E., O’Callaghan M., DeAngelis K.M., Jones E.E., Stewart A., Firestone M.K., Condron L.M. Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol. Ecol. 2011;77:600–610. doi: 10.1111/j.1574-6941.2011.01150.x. PubMed DOI

Mashabela M.D., Tugizimana F., Steenkamp P.A., Piater L.A., Dubery I.A., Mhlongo M.I. Untargeted metabolite profiling to elucidate rhizosphere and leaf metabolome changes of wheat cultivars (Triticum aestivum L.) treated with the plant growth-promoting rhizobacteria Paenibacillus alvei (T22) and Bacillus subtilis. Front. Microbiol. 2022;13:971836. doi: 10.3389/fmicb.2022.971836. PubMed DOI PMC

Massalha H., Korenblum E., Tholl D., Aharoni A. Small Molecules Below-Ground: The Role of Specialized Metabolites in the Rhizosphere. Plant J. 2017;90:788–807. doi: 10.1111/tpj.13543. PubMed DOI

Yang X., Zhu K., Loik M.E., Sun W. Differential responses of soil bacteria and fungi to altered precipitation in a meadow steppe. Geoderma. 2021;384:114812. doi: 10.1016/j.geoderma.2020.114812. DOI

Engelhardt I.C., Welty A., Blazewicz S.J., Bru D., Rouard N., Breuil M.-C., Gessler A., Galiano L., Miranda J.C., Spor A. Depth matters: Effects of precipitation regime on soil microbial activity upon rewetting of a plant-soil system. ISME J. 2018;12:1061–1071. doi: 10.1038/s41396-018-0079-z. PubMed DOI PMC

Kieft T.L. Microbial biomass response to a rapid increase in water potential when dry soil is wetted. Soil Biol. Biochem. 1987;19:119–126. doi: 10.1016/0038-0717(87)90070-8. DOI

de Boer W., Folman L.B., Summerbell R.C., Boddy L. Living in a fungal world: Impact of fungi on soil bacterial niche development. FEMS Microbiol. Rev. 2005;29:795–811. doi: 10.1016/j.femsre.2004.11.005. PubMed DOI

Conradie T., Jacobs K. Seasonal and agricultural response of Acidobacteria present in two fynbos rhizosphere soils. Diversity. 2020;12:277. doi: 10.3390/d12070277. DOI

Ren H., Wang H., Qi X., Yu Z., Zheng X., Zhang S., Wang Z., Zhang M., Ahmed T., Li B. The damage caused by decline disease in bayberry plants through changes in soil properties, rhizosphere microbial community structure and metabolites. Plants. 2021;10:2083. doi: 10.3390/plants10102083. PubMed DOI PMC

Bi B., Yuan Y., Zhang H., Wu Z., Wang Y., Han F. Rhizosphere soil metabolites mediated microbial community changes of Pinus sylvestris var. mongolica across stand ages in the Mu Us Desert. Appl. Soil Ecol. 2022;169:104222. doi: 10.1016/j.apsoil.2021.104222. DOI

Meena R.S., Vijayakumar V., Yadav G.S., Mitran T. Response and interaction of Bradyrhizobium japonicum and arbuscular mycorrhizal fungi in the soybean rhizosphere. Plant Growth Regul. 2018;84:207–223. doi: 10.1007/s10725-017-0334-8. DOI

Augé R.M. Arbuscular mycorrhizae and soil/plant water relations. Can. J. Soil Sci. 2004;84:373–381. doi: 10.4141/S04-002. DOI

Heinemeyer A., Fitter A. Impact of temperature on the arbuscular mycorrhizal (AM) symbiosis: Growth responses of the host plant and its AM fungal partner. J. Exp. Bot. 2004;55:525–534. doi: 10.1093/jxb/erh049. PubMed DOI

Wang J., Zhang J., Wang C., Ren G., Yang Y., Wang D. Precipitation exerts a strong influence on arbuscular mycorrhizal fungi community and network complexity in a semiarid steppe ecosystem. Eur. J. Soil Biol. 2021;102:103268. doi: 10.1016/j.ejsobi.2020.103268. DOI

Frey-Klett P., Garbaye J., Tarkka M. The mycorrhiza helper bacteria revisited. New Phytol. 2007;176:22–36. doi: 10.1111/j.1469-8137.2007.02191.x. PubMed DOI

Sharma P. Winter School. ICAR; Bharatpur, India: 2015. Bio fungicides: Their role in plant disease management; p. 113.

Adnan M., Islam W., Gang L., Chen H.Y. Advanced research tools for fungal diversity and its impact on forest ecosystem. Environ. Sci. Pollut. Res. 2022;29:45044–45062. doi: 10.1007/s11356-022-20317-8. PubMed DOI

Morvan S., Meglouli H., Lounès-Hadj Sahraoui A., Hijri M. Into the wild blueberry (Vaccinium angustifolium) rhizosphere microbiota. Environ. Microbiol. 2020;22:3803–3822. doi: 10.1111/1462-2920.15151. PubMed DOI

Wang Y.-L., Gao C., Chen L., Ji N.-N., Wu B.-W., Li X.-C., Lü P.-P., Zheng Y., Guo L.-D. Host plant phylogeny and geographic distance strongly structure Betulaceae-associated ectomycorrhizal fungal communities in Chinese secondary forest ecosystems. FEMS Microbiol. Ecol. 2019;95:fiz037. doi: 10.1093/femsec/fiz037. PubMed DOI

Luo Y., Wang F., Huang Y., Zhou M., Gao J., Yan T., Sheng H., An L. Sphingomonas sp. Cra20 increases plant growth rate and alters rhizosphere microbial community structure of Arabidopsis thaliana under drought stress. Front. Microbiol. 2019;10:1221. doi: 10.3389/fmicb.2019.01221. PubMed DOI PMC

Dobrovolskaya T., Golovchenko A., Lysak L., Yurchenko E. Taxonomic structure of bacterial communities of rhizospheric soil under bogs’ plants. Mosc. Univ. Soil Sci. Bull. 2020;75:93–100. doi: 10.3103/S0147687420020039. DOI

Li J., Chen X., Li S., Zuo Z., Zhan R., He R. Variations of rhizospheric soil microbial communities in response to continuous Andrographis paniculata cropping practices. Bot. Stud. 2020;61:1–13. doi: 10.1186/s40529-020-00295-1. PubMed DOI PMC

Zhang X., Gao G., Wu Z., Wen X., Zhong H., Zhong Z., Bian F., Gai X. Agroforestry alters the rhizosphere soil bacterial and fungal communities of moso bamboo plantations in subtropical China. Appl. Soil Ecol. 2019;143:192–200. doi: 10.1016/j.apsoil.2019.07.019. DOI

Pent M., Põldmaa K., Bahram M. Bacterial communities in boreal forest mushrooms are shaped both by soil parameters and host identity. Front. Microbiol. 2017;8:251724. doi: 10.3389/fmicb.2017.00836. PubMed DOI PMC

Warmink J., Nazir R., Van Elsas J. Universal and species-specific bacterial ‘fungiphiles’ in the mycospheres of different basidiomycetous fungi. Environ. Microbiol. 2009;11:300–312. doi: 10.1111/j.1462-2920.2008.01767.x. PubMed DOI

Antony-Babu S., Deveau A., Van Nostrand J.D., Zhou J., Le Tacon F., Robin C., Frey-Klett P., Uroz S. Black truffle-associated bacterial communities during the development and maturation of T uber melanosporum ascocarps and putative functional roles. Environ. Microbiol. 2014;16:2831–2847. doi: 10.1111/1462-2920.12294. PubMed DOI

Liao X., O’Brien T.R., Fang W., St. Leger R.J. The plant beneficial effects of Metarhizium species correlate with their association with roots. Appl. Microbiol. Biotechnol. 2014;98:7089–7096. doi: 10.1007/s00253-014-5788-2. PubMed DOI

Leslie J.F., Summerell B.A., Bullock S. The Fusarium Laboratory Manual. Blackwell Publishing; Ames, IA, USA: 2006.

Farh M.E.-A., Kim Y.-J., Kim Y.-J., Yang D.-C. Cylindrocarpon destructans/Ilyonectria radicicola-species complex: Causative agent of ginseng root-rot disease and rusty symptoms. J. Ginseng Res. 2018;42:9–15. doi: 10.1016/j.jgr.2017.01.004. PubMed DOI PMC

Belosokhov A., Yarmeeva M., Kokaeva L., Chudinova E., Mislavskiy S., Elansky S. Trichocladium solani sp. nov.—A new pathogen on potato tubers causing yellow rot. J. Fungi. 2022;8:1160. doi: 10.3390/jof8111160. PubMed DOI PMC

Benoliel B., Poças-Fonseca M.J., Torres F.A.G., de Moraes L.M.P. Expression of a glucose-tolerant β-glucosidase from Humicola grisea var. thermoidea in Saccharomyces cerevisiae. Appl. Biochem. Biotechnol. 2010;160:2036–2044. doi: 10.1007/s12010-009-8732-7. PubMed DOI

Cintra L.C., Fernandes A.G., de Oliveira I.C.M., Siqueira S.J.L., Costa I.G.O., Colussi F., Jesuíno R.S.A., Ulhoa C.J., de Faria F.P. Characterization of a recombinant xylose tolerant β-xylosidase from Humicola grisea var. thermoidea and its use in sugarcane bagasse hydrolysis. Int. J. Biol. Macromol. 2017;105:262–271. doi: 10.1016/j.ijbiomac.2017.07.039. PubMed DOI

Datta R. Enzymatic degradation of cellulose in soil: A review. Heliyon. 2024;10:e24022. doi: 10.1016/j.heliyon.2024.e24022. PubMed DOI PMC

Liu Y., Jin X., Huang S., Liu Y., Kong Z., Wu L., Ge G. Co-Occurrence Patterns of Soil Fungal and Bacterial Communities in Subtropical Forest-Transforming Areas. Curr. Microbiol. 2024;81:64. doi: 10.1007/s00284-023-03608-2. PubMed DOI

Huang J., Gao K., Yang L., Lu Y. Successional action of Bacteroidota and Firmicutes in decomposing straw polymers in a paddy soil. Environ. Microbiome. 2023;18:76. doi: 10.1186/s40793-023-00533-6. PubMed DOI PMC

Zhang B., Wu X., Tai X., Sun L., Wu M., Zhang W., Chen X., Zhang G., Chen T., Liu G. Variation in actinobacterial community composition and potential function in different soil ecosystems belonging to the arid Heihe River Basin of Northwest China. Front. Microbiol. 2019;10:2209. doi: 10.3389/fmicb.2019.02209. PubMed DOI PMC

Zhu H.-Z., Jiang C.-Y., Liu S.-J. Microbial roles in cave biogeochemical cycling. Front. Microbiol. 2022;13:950005. doi: 10.3389/fmicb.2022.950005. PubMed DOI PMC

Singh B.K., Bardgett R.D., Smith P., Reay D.S. Microorganisms and climate change: Terrestrial feedbacks and mitigation options. Nat. Rev. Microbiol. 2010;8:779–790. doi: 10.1038/nrmicro2439. PubMed DOI

Zhou Z., Wang C., Luo Y. Effects of forest degradation on microbial communities and soil carbon cycling: A global meta-analysis. Glob. Ecol. Biogeogr. 2018;27:110–124. doi: 10.1111/geb.12663. DOI

Lange L., Pilgaard B., Herbst F.-A., Busk P.K., Gleason F., Pedersen A.G. Origin of fungal biomass degrading enzymes: Evolution, diversity and function of enzymes of early lineage fungi. Fungal Biol. Rev. 2019;33:82–97. doi: 10.1016/j.fbr.2018.09.001. DOI

Lisá L., Bajer A., Pacina J., McCool J.-P., Cílek V., Rohovec J., Matoušková Š., Kallistova A., Gottvald Z. Prehistoric dark soils/sediments of Central Sudan; case study from the Mesolithic landscape at the Sixth Nile Cataract. Catena. 2017;149:273–282. doi: 10.1016/j.catena.2016.09.023. DOI

Wentworth C.K. A scale of grade and class terms for clastic sediments. J. Geol. 1922;30:377–392. doi: 10.1086/622910. DOI

Mehlich A. Mehlich 3 soil test extractant: A modification of Mehlich 2 extractant. Commun. Soil Sci. Plant Anal. 1984;15:1409–1416. doi: 10.1080/00103628409367568. DOI

Zbíral J. Determination of plant-available micronutrients by the Mehlich 3 soil extractant-a proposal of critical values. Plant Soil Environ. 2016;62:527–531. doi: 10.17221/564/2016-PSE. DOI

Lê Cao K.-A., Boitard S., Besse P. Sparse PLS discriminant analysis: Biologically relevant feature selection and graphical displays for multiclass problems. BMC Bioinform. 2011;12:253. doi: 10.1186/1471-2105-12-253. PubMed DOI PMC

Chong J., Wishart D.S., Xia J. Using MetaboAnalyst 4.0 for comprehensive and integrative metabolomics data analysis. Curr. Protoc. Bioinform. 2019;68:e86. doi: 10.1002/cpbi.86. PubMed DOI

Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., Glöckner F.O. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41:e1. doi: 10.1093/nar/gks808. PubMed DOI PMC

White T.J., Bruns T., Lee S., Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc. A Guide Methods Appl. 1990;18:315–322.

Bolyen E., Rideout J.R., Dillon M.R., Bokulich N.A., Abnet C.C., Al-Ghalith G.A., Alexander H., Alm E.J., Arumugam M., Asnicar F. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019;37:852–857. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC

Magoč T., Salzberg S.L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27:2957–2963. doi: 10.1093/bioinformatics/btr507. PubMed DOI PMC

Chen S., Zhou Y., Chen Y., Gu J. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–i890. doi: 10.1093/bioinformatics/bty560. PubMed DOI PMC

Rognes T., Flouri T., Nichols B., Quince C., Mahé F. VSEARCH: A versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. doi: 10.7717/peerj.2584. PubMed DOI PMC

Callahan B.J., McMurdie P.J., Rosen M.J., Han A.W., Johnson A.J.A., Holmes S.P. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Li M., Shao D., Zhou J., Gu J., Qin J., Chen W., Wei W. Signatures within esophageal microbiota with progression of esophageal squamous cell carcinoma. Chin. J. Cancer Res. 2020;32:755. doi: 10.21147/j.issn.1000-9604.2020.06.09. PubMed DOI PMC

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glöckner F.O. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–D596. doi: 10.1093/nar/gks1219. PubMed DOI PMC

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. The UNITE database for molecular identification of fungi: Handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 2019;47:D259–D264. doi: 10.1093/nar/gky1022. PubMed DOI PMC

Bokulich N.A., Kaehler B.D., Rideout J.R., Dillon M., Bolyen E., Knight R., Huttley G.A., Gregory Caporaso J. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018;6:90. doi: 10.1186/s40168-018-0470-z. PubMed DOI PMC

Magurran A.E. Ecological Diversity and Its Measurement. Springer Science & Business Media; Berlin/Heidelberg, Germany: 2013.

Chao A., Lee S.-M., Chen T.-C. A generalized Good’s nonparametric coverage estimator. Chin. J. Math. 1988;16:189–199.

Team R.C. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2013.

Lozupone C.A., Hamady M., Kelley S.T., Knight R. Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities. Appl. Environ. Microbiol. 2007;73:1576–1585. doi: 10.1128/AEM.01996-06. PubMed DOI PMC

Lozupone C., Lladser M.E., Knights D., Stombaugh J., Knight R. UniFrac: An effective distance metric for microbial community comparison. ISME J. 2011;5:169–172. doi: 10.1038/ismej.2010.133. PubMed DOI PMC

Minchin P.R. Theory and Models in Vegetation Science, Proceedings of the Symposium, Uppsala, Sweden, 8–13 July 1985. Springer; Dordrecht, The Netherlands: 1987. An evaluation of the relative robustness of techniques for ecological ordination; pp. 89–107.

Clarke K.R. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 1993;18:117–143. doi: 10.1111/j.1442-9993.1993.tb00438.x. DOI

Stat M., Pochon X., Franklin E.C., Bruno J.F., Casey K.S., Selig E.R., Gates R.D. The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: Correlations with host and the history of ocean thermal stress. Ecol. Evol. 2013;3:1317–1329. doi: 10.1002/ece3.556. PubMed DOI PMC

Chapman M., Underwood A. Ecological patterns in multivariate assemblages: Information and interpretation of negative values in ANOSIM tests. Mar. Ecol. Prog. Ser. 1999;180:257–265. doi: 10.3354/meps180257. DOI

D’Argenio V., Casaburi G., Precone V., Salvatore F. Comparative metagenomic analysis of human gut microbiome composition using two different bioinformatic pipelines. BioMed Res. Int. 2014;2014:325340. doi: 10.1155/2014/325340. PubMed DOI PMC

Paulson J.N., Pop M., Bravo H.C. Metastats: An improved statistical method for analysis of metagenomic data. Genome Biol. 2011;12:P17. doi: 10.1186/1465-6906-12-S1-P17. DOI

Segata N., Izard J., Waldron L., Gevers D., Miropolsky L., Garrett W.S., Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60. doi: 10.1186/gb-2011-12-6-r60. PubMed DOI PMC

Douglas G.M., Maffei V.J., Zaneveld J.R., Yurgel S.N., Brown J.R., Taylor C.M., Huttenhower C., Langille M.G. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 2020;38:685–688. doi: 10.1038/s41587-020-0548-6. PubMed DOI PMC

Kanehisa M., Goto S., Sato Y., Furumichi M., Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012;40:D109–D114. doi: 10.1093/nar/gkr988. PubMed DOI PMC

Nguyen N.H., Song Z., Bates S.T., Branco S., Tedersoo L., Menke J., Schilling J.S., Kennedy P.G. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 2016;20:241–248. doi: 10.1016/j.funeco.2015.06.006. DOI

Guseva K., Darcy S., Simon E., Alteio L.V., Montesinos-Navarro A., Kaiser C. From diversity to complexity: Microbial networks in soils. Soil Biol. Biochem. 2022;169:108604. doi: 10.1016/j.soilbio.2022.108604. PubMed DOI PMC

Csardi G., Nepusz T. The igraph software. Complex Syst. 2006;1695:862049.

Clauset A., Newman M.E., Moore C. Finding community structure in very large networks. Phys. Rev. E—Stat. Nonlinear Soft Matter Phys. 2004;70:066111. doi: 10.1103/PhysRevE.70.066111. PubMed DOI

Iyer S., Killingback T., Sundaram B., Wang Z. Attack robustness and centrality of complex networks. PLoS ONE. 2013;8:e59613. doi: 10.1371/journal.pone.0059613. PubMed DOI PMC

Shang Y. Unveiling robustness and heterogeneity through percolation triggered by random-link breakdown. Phys. Rev. E. 2014;90:032820. doi: 10.1103/PhysRevE.90.032820. PubMed DOI

Watts D.J., Strogatz S.H. Collective dynamics of ‘small-world’networks. Nature. 1998;393:440–442. doi: 10.1038/30918. PubMed DOI