Abstract
Background and aims
Wild fruit forests are vital reservoirs of germplasm genetic and biodiversity. Unfortunately, wild fruit forests of Central Asia are in the decline due to fungal disease and insect pest outbreaks. A health soil microbial community may help ameliorate the degradation of wild trees by increasing their systematic resistance, stabilizing soil carbon pool, and maintaining the quality of the habitat environment. We evaluated soil bacterial and fungal community beneath the dominant tree species, Malus sieversii (Ledeb.) M. Roem, to identify potential interactions between wild fruit forest degradation events and soil microorganisms in the Tianshan Mountain, China.
Methods
Based on targeted metagenomics of the 16S rRNA and ITS (Internal Transcribed Spacer), we explored the bacterial and fungal microbial communities in soils beneath healthy and degraded M. sieversii trees (i.e., microbial biomass, species interactions, potential and niche breadth), and soil physicochemical properties.
Results
We found that the degradation of M. sieversii reduced the beta diversity of topsoil bacterial communities and fungal symbiotic groups. The decline in M. sieversii abundance loosened connections within bacterial and fungal co-occurrence networks. Community assembly identified higher migration rates in the topsoil around degraded M. sieversii for bacteria and for fungi, suggesting that dispersal restricted in degraded wild fruit forest soils. Ultimately, the demise of M. sieversii homogenized the soil bacteria resulting in a narrow niche-breadth, enhanced pathogenetic fungal species, and reduced beneficial symbiotic and saprotrophic fungal diversity.
Conclusions
Our results demonstrated that the degradation of M. sieversii leads to alterations in diversity, self-assembling and resource competitiveness of forest soil-dwelling microorganisms.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albanese D, Filosi M, Visintainer R, Riccadonna S, Jurman G, Furlanello C (2012) Minerva and minepy: a C engine for the MINE suite and its R, Python and MATLAB wrappers. Bioinformatics 29:407–408. https://doi.org/10.1093/bioinformatics/bts707
Arntzen MØ, Bengtsson O, Várnai A, Delogu F, Mathiesen G, Eijsink VGH (2020) Quantitative comparison of the biomass-degrading enzyme repertoires of five filamentous fungi. Sci Rep 10:20267. https://doi.org/10.1038/s41598-020-75217-z
Baldrian P, López-Mondéjar R, Kohout P (2023) Forest microbiome and global change. Nat Rev Microbiol 21:487–501. https://doi.org/10.1038/s41579-023-00876-4
Baselga A, Orme CDL (2012) Betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812. https://doi.org/10.1111/j.2041-210X.2012.00224.x
Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Proc Int AAAI Conf Web Soc Med 3:361–362. https://doi.org/10.1609/icwsm.v3i1.13937
Bastida F, Eldridge DJ, García C, Kenny Png G, Bardgett RD, Delgado-Baquerizo M (2021) Soil microbial diversity–biomass relationships are driven by soil carbon content across global biomes. ISME J 15:2081–2091. https://doi.org/10.1038/s41396-021-00906-0
Bhalla K, Qu X, Kretschmer M, Kronstad JW (2022) The phosphate language of fungi. Trends Microbiol 30:338–349. https://doi.org/10.1016/j.tim.2021.08.002
Bowd EJ, Banks SC, Bissett A, May TW, Lindenmayer DB (2022) Disturbance alters the forest soil microbiome. Mol Ecol 31:419–447. https://doi.org/10.1111/mec.16242
Buscardo E, Souza RC, Meir P, Geml J, Schmidt SK, da Costa ACL, Nagy L (2021) Effects of natural and experimental drought on soil fungi and biogeochemistry in an Amazon rain forest. Commun Earth Environ 2:55. https://doi.org/10.1038/s43247-021-00124-8
Carvalhais LC, Rincon-Florez VA, Brewer PB, Beveridge CA, Dennis PG, Schenk PM (2019) The ability of plants to produce strigolactones affects rhizosphere community composition of fungi but not bacteria. Rhizosphere 9:18–26. https://doi.org/10.1016/j.rhisph.2018.10.002
Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:art24. https://doi.org/10.1890/ES10-00117.1
Chen YN, Wang Q, Li WH, Ruan X (2007) Microbiotic crusts and their interrelations with environmental factors in the Gurbantonggut desert, western China. Environ Geol 52:691–700. https://doi.org/10.1007/s00254-006-0505-9
Chen W, Ren K, Isabwe A, Chen H, Liu M, Yang J (2019) Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome 7:138. https://doi.org/10.1186/s40168-019-0749-8
Chen QL, Hu HW, Yan ZZ, Li CY, Nguyen BAT, Sun AQ, Zhu YG, He JZ (2021) Deterministic selection dominates microbial community assembly in termite mounds. Soil Biol Biochem 152:108073. https://doi.org/10.1016/j.soilbio.2020.108073
Cornille A, Antolín F, Garcia E, Vernesi C, Fietta A, Brinkkemper O, Kirleis W, Schlumbaum A, Roldán-Ruiz I (2019) A multifaceted overview of apple tree domestication. Trends Plant Sci 24:770–782. https://doi.org/10.1016/j.tplants.2019.05.007
Cui X, Liu D, Liu A (2015) Research progress in integrated management of Agrilus mali. Plant Prot 41:16–23
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
Don A, Schumacher J, Freibauer A (2011) Impact of tropical land-use change on soil organic carbon stocks – a meta-analysis. Glob Chang Biol 17:1658–1670. https://doi.org/10.1111/j.1365-2486.2010.02336.x
Dove NC, Taş N, Hart SC (2022) Ecological and genomic responses of soil microbiomes to high-severity wildfire: linking community assembly to functional potential. ISME J 16:1853–1863. https://doi.org/10.1038/s41396-022-01232-9
Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366. https://doi.org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2
Durodola B, Blumenstein K, Akinbobola A, Kolehmainen A, Chano V, Gailing O, Terhonen E (2023) Beyond the surface: exploring the mycobiome of Norway spruce under drought stress and with Heterobasidion parviporum. BMC Microbiol 23:350. https://doi.org/10.1186/s12866-023-03099-y
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Ekblad A, Mikusinska A, Ågren GI, Menichetti L, Wallander H, Vilgalys R, Bahr A, Eriksson U (2016) Production and turnover of ectomycorrhizal extramatrical mycelial biomass and necromass under elevated CO2 and nitrogen fertilization. New Phytol 211:874–885. https://doi.org/10.1111/nph.13961
Fahey C, Koyama A, Antunes PM, Dunfield K, Flory L (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
Ferrenberg S, O'Neill SP, Knelman JE, Todd B, Duggan S, Bradley D, Robinson T, Schmidt SK, Townsend AR, Williams MW, Cleveland CC, Melbourne BA, Jiang L, Nemergut DR (2013) Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J 7:1102–1111. https://doi.org/10.1038/ismej.2013.11
Fukami T, Dickie IA, Paula Wilkie J, Paulus BC, Park D, Roberts A, Buchanan PK, Allen RB (2010) Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecol Lett 13:675–684. https://doi.org/10.1111/j.1461-0248.2010.01465.x
García-Angulo D, Hereş AM, Fernández-López M, Flores O, Sanz MJ, Rey A, Valladares F, Curiel Yuste J (2020) Holm oak decline and mortality exacerbates drought effects on soil biogeochemical cycling and soil microbial communities across a climatic gradient. Soil Biol Biochem 149:107921. https://doi.org/10.1016/j.soilbio.2020.107921
Gómez-Aparicio L, Domínguez-Begines J, Kardol P, Ávila JM, Ibáñez B, García LV (2017) Plant-soil feedbacks in declining forests: implications for species coexistence. Ecology 98:1908–1921. https://doi.org/10.1002/ecy.1864
Gómez-Aparicio L, Domínguez-Begines J, Villa-Sanabria E, García LV, Muñoz-Pajares AJ (2022) Tree decline and mortality following pathogen invasion alters the diversity, composition and network structure of the soil microbiome. Soil Biol Biochem 166:108560. https://doi.org/10.1016/j.soilbio.2022.108560
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
He G, Peng T, Guo Y, Wen S, Ji L, Luo Z (2022) Forest succession improves the complexity of soil microbial interaction and ecological stochasticity of community assembly: evidence from Phoebe bournei-dominated forests in subtropical regions. Front Microbiol 13:1021258. https://doi.org/10.3389/fmicb.2022.1021258
Hernandez DJ, David AS, Menges ES, Searcy CA, Afkhami ME (2021) Environmental stress destabilizes microbial networks. ISME J 15:1722–1734. https://doi.org/10.1038/s41396-020-00882-x
Hou L, Wang H, Chen Q, Su JQ, Gad M, Li J, Mulla SI, Yu CP, Hu A (2021a) Fecal pollution mediates the dominance of stochastic assembly of antibiotic resistome in an urban lagoon (Yundang lagoon), China. J Haz Mat 417:126083. https://doi.org/10.1016/j.jhazmat.2021.126083
Hou S, Wolinska KW, Hacquard S (2021b) Microbiota-root-shoot-environment axis and stress tolerance in plants. Curr Opin Plant Biol 62:102028. https://doi.org/10.1016/j.pbi.2021.102028
Hu A, Choi M, Tanentzap AJ, Liu J, Jang KS, Lennon JT, Liu Y, Soininen J, Lu X, Zhang Y, Shen J, Wang J (2022) Ecological networks of dissolved organic matter and microorganisms under global change. Nat Commun 13:3600. https://doi.org/10.1038/s41467-022-31251-1
Huang R, Crowther TW, Sui Y, Sun B, Liang Y (2021) High stability and metabolic capacity of bacterial community promote the rapid reduction of easily decomposing carbon in soil. Commun Biol 4:1376. https://doi.org/10.1038/s42003-021-02907-3
Jiao S, Chu H, Zhang B, Wei X, Chen W, Wei G (2022) Linking soil fungi to bacterial community assembly in arid ecosystems. iMeta 1:e2. https://doi.org/10.1002/imt2.2
Jucker T, Coomes DA (2012) Comment on “plant species richness and ecosystem multifunctionality in global drylands”. Science 337:155. https://doi.org/10.1126/science.1220620
Langenheder S, Lindström ES (2019) Factors influencing aquatic and terrestrial bacterial community assembly. Environ Microbiol Rep 11:306–315. https://doi.org/10.1111/1758-2229.12731
Lazcano C, Boyd E, Holmes G, Hewavitharana S, Pasulka A, Ivors K (2021) The rhizosphere microbiome plays a role in the resistance to soil-borne pathogens and nutrient uptake of strawberry cultivars under field conditions. Sci Rep 11:3188. https://doi.org/10.1038/s41598-021-82768-2
Li J, Rui J, Yao M, Zhang S, Yan X, Wang Y, Yan Z, Li X (2015) Substrate type and free ammonia determine bacterial community structure in full-scale mesophilic anaerobic digesters treating cattle or swine manure. Front Microbiol 6:1337. https://doi.org/10.3389/fmicb.2015.01337
Liang M, Shi L, Burslem DFRP, Johnson D, Fang M, Zhang X, Yu S (2021) Soil fungal networks moderate density-dependent survival and growth of seedlings. New Phytol 230:2061–2071. https://doi.org/10.1111/nph.17237
Liu A, Zhang X, Wen J, Yue C, Alimu Jiao S, Zhang J, Kereman (2014) Preliminary research on the composite damage of Agrilus mali Matsumura and Valsa mali Miyabe et Yamada in wild apple trees in Tianshan Mountain. Xinjiang Agric Sci 51:2240–2244
Liu L, Zhu K, Krause SMB, Li S, Wang X, Zhang Z, Shen M, Yang Q, Lian J, Wang X, Ye W, Zhang J (2021) Changes in assembly processes of soil microbial communities during secondary succession in two subtropical forests. Soil Biol Biochem 154:108144. https://doi.org/10.1016/j.soilbio.2021.108144
Lladó S, López-Mondéjar R, Baldrian P (2017) Forest soil bacteria: diversity, involvement in ecosystem processes, and response to global change. Microbiol Mol Biol Rev 81:e00063–e00016. https://doi.org/10.1128/mmbr.00063-16
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
Maillard F, Kohler A, Morin E, Hossann C, Miyauchi S, Ziegler-Devin I, Gérant D, Angeli N, Lipzen A, Keymanesh K, Johnson J, Barry K, Grigoriev IV, Martin FM, Buée M (2023) Functional genomics gives new insights into the ectomycorrhizal degradation of chitin. New Phytol 238:845–858. https://doi.org/10.1111/nph.18773
Neilson JW, Califf K, Cardona C, Copeland A, van Treuren W, Josephson KL, Knight R, Gilbert JA, Quade J, Caporaso JG, Maier RM (2017) Significant impacts of increasing aridity on the arid soil microbiome. mSystems 2:e00195–e00116. https://doi.org/10.1128/mSystems.00195-16
Nelson AR, Narrowe AB, Rhoades CC, Fegel TS, Daly RA, Roth HK, Chu RK, Amundson KK, Young RB, Steindorff AS, Mondo SJ, Grigoriev IV, Salamov A, Borch T, Wilkins MJ (2022) Wildfire-dependent changes in soil microbiome diversity and function. Nat Microbiol 7:1419–1430. https://doi.org/10.1038/s41564-022-01203-y
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. https://doi.org/10.1016/j.funeco.2015.06.006
Ning D, Deng Y, Tiedje JM, Zhou J (2019) A general framework for quantitatively assessing ecological stochasticity. Proc Natl Acad Sci U S A 116:16892–16898. https://doi.org/10.1073/pnas.1904623116
Palakurty SX, Stinchcombe JR, Afkhami ME (2018) Cooperation and coexpression: how coexpression networks shift in response to multiple mutualists. Mol Ecol 27:1860–1873. https://doi.org/10.1111/mec.14550
Peralta G, Perry GLW, Vázquez DP, Dehling DM, Tylianakis JM (2020) Strength of niche processes for species interactions is lower for generalists and exotic species. J Anim Ecol 89:2145–2155. https://doi.org/10.1111/1365-2656.13274
Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220:1059–1075. https://doi.org/10.1111/nph.15119
Ratzke C, Barrere J, Gore J (2020) Strength of species interactions determines biodiversity and stability in microbial communities. Nat Ecol Evol 4:376–383. https://doi.org/10.1038/s41559-020-1099-4
Ross DJ (1992) Influence of sieve mesh size on estimates of microbial carbon and nitrogen by fumigation-extraction procedures in soils under pasture. Soil Biol Biochem 24:343–350. https://doi.org/10.1016/0038-0717(92)90194-3
Runte G, Smith A, Moeller H, Bogar L (2021) Spheres of influence: host tree proximity and soil chemistry shape rRNA, but not DNA, communities of symbiotic and free-living soil fungi in a mixed hardwood-conifer forest. Front Ecol Evol 9:641732. https://doi.org/10.3389/fevo.2021.641732
Santillan E, Seshan H, Constancias F, Drautz-Moses DI, Wuertz S (2019) Frequency of disturbance alters diversity, function, and underlying assembly mechanisms of complex bacterial communities. NPJ Biofilms Microbiomes 5:8. https://doi.org/10.1038/s41522-019-0079-4
Shan Q, Ling H, Zhao H, Li M, Wang Z, Zhang G (2021) Do extreme climate events cause the degradation of Malus sieversii forests in China? Front Plant Sci 12:608211. https://doi.org/10.3389/fpls.2021.608211
Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079. https://doi.org/10.1038/ismej.2013.93
Štursová M, Šnajdr J, Cajthaml T, Bárta J, Šantrůčková H, Baldrian P (2014) When the forest dies: the response of forest soil fungi to a bark beetle-induced tree dieback. ISME J 8:1920–1931. https://doi.org/10.1038/ismej.2014.37
Tian J, Dungait JAJ, Lu X, Yang Y, Hartley IP, Zhang W, Mo J, Yu G, Zhou J, Kuzyakov Y (2019) Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil. Glob Chang Biol 25:3267–3281. https://doi.org/10.1111/gcb.14750
Veach AM, Stegen JC, Brown SP, Dodds WK, Jumpponen A (2016) Spatial and successional dynamics of microbial biofilm communities in a grassland stream ecosystem. Mol Ecol 25:4674–4688. https://doi.org/10.1111/mec.13784
Wang Y, Liu Z, Hao X, Wang Z, Wang Z, Liu S, Tao C, Wang D, Wang B, Shen Z, Shen Q, Li R (2023) Biodiversity of the beneficial soil-borne fungi steered by Trichoderma-amended biofertilizers stimulates plant production. NPJ Biofilms Microbiomes 9:46. https://doi.org/10.1038/s41522-023-00416-1
Wu MH, Chen SY, Chen JW, Xue K, Chen SL, Wang XM, Chen T, Kang SC, Rui JP, Thies JE, Bardgett RD, Wang YF (2021) Reduced microbial stability in the active layer is associated with carbon loss under alpine permafrost degradation. Proc Natl Acad Sci U S A 118:e2025321118. https://doi.org/10.1073/pnas.2025321118
Yang Y, Ye C, Zhang W, Zhu X, Li H, Yang D, Ahmed W, Zhao Z (2023) Elucidating the impact of biochar with different carbon/nitrogen ratios on soil biochemical properties and rhizosphere bacterial communities of flue-cured tobacco plants. Front Plant Sci 14:1250669. https://doi.org/10.3389/fpls.2023.1250669
Zhang X, Johnston ER, Liu W, Li L, Han X (2016) Environmental changes affect the assembly of soil bacterial community primarily by mediating stochastic processes. Glob Chang Biol 22:198–207. https://doi.org/10.1111/gcb.13080
Zhang Y, Zhang D, Li W, Li Y, Zhang C, Guan K, Pan B (2020) Characteristics and utilization of plant diversity and resources in Central Asia. Reg Sustain 1:1–10. https://doi.org/10.1016/j.regsus.2020.08.001
Zhou Z, Wang C, Luo Y (2018) Effects of forest degradation on microbial communities and soil carbon cycling: a global meta-analysis. Glob Ecol Biogeogr 27:110–124. https://doi.org/10.1111/geb.12663
Žifčáková L, Vetrovsky T, Howe A, Baldrian P (2015) Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol 18:288–301. https://doi.org/10.1111/1462-2920.13026
Zipfel C, Oldroyd GED (2017) Plant signalling in symbiosis and immunity. Nature 543:328–336. https://doi.org/10.1038/nature22009
Acknowledgements
We give our sincere gratitude to the editors and the two anonymous reviewers for their constructive comments and suggestions on improving this manuscript. We are also grateful to Prof. Zachary T. Aanderud and Prof. Tong Li for their editing the manuscript for word usage, readability, logic and structure. Our work was supported by the Xinjiang Tianshan Youth Talent Top Project (2022TSYCCX0007), the Third Xinjiang Scientific Expedition Program (2021xjkk0500), the Key Fund Projects of the Natural Science Foundation of Xinjiang (2022D01D083) and the National Natural Science Foundation of China (U2003214).
Author information
Authors and Affiliations
Contributions
XR and YZ designed research; NW, BY, XZ and ZA participated in sampling and discussion; BZ and YL contributed to the acquisition of environmental data; XR performed data analysis and wrote the paper.
The authors declare no conflict of interest.
Corresponding author
Ethics declarations
Competing interests
We declare that we have no known competing financial interests or personal relationships that could influence the work reported in this paper.
Additional information
Responsible Editor: Guiyao Zhou.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 2316 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
Rong, X., Wu, N., Yin, B. et al. Degradation of wild fruit forests created less diverse and diffuse bacterial communities decreased bacterial diversity, enhanced fungal pathogens and altered microbial assembly in the Tianshan Mountain, China. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06545-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-024-06545-6