Abstract
Reductive soil disinfestation (RSD) is an effective bioremediation technique to restructure the soil microbial community and eliminate soilborne phytopathogens. Yet we still lack a comprehensive understanding of the keystone taxa involved and their roles in ecosystem functioning in degraded soils treated by RSD. In this study, the bacteriome network structure in RSD-treated soil and the subsequent cultivation process were explored. As a result, bacterial communities in RSD-treated soil developed more complex topologies and stable co-occurrence patterns. The richness and diversity of keystone taxa were higher in the RSD group (module hub: 0.57%; connector: 23.98%) than in the Control group (module hub: 0.16%; connector: 19.34%). The restoration of keystone taxa in RSD-treated soil was significantly (P < 0.01) correlated with soil pH, total organic carbon, and total nitrogen. Moreover, a strong negative correlation (r = −0.712; P < 0.01) was found between keystone taxa richness and Fusarium abundance. Our results suggest that keystone taxa involved in the RSD network structure are capable of maintaining a flexible generalist mode of metabolism, namely with respect to nitrogen fixation, methylotrophy, and methanotrophy. Furthermore, distinct network modules composed by numerous anti-pathogen agents were formed in RSD-treated soil; i.e., the genera Hydrogenispora, Azotobacter, Sphingomonas, and Clostridium_8 under the soil treatment stage, and the genera Anaerolinea and Pseudarthrobacter under the plant cultivation stage. The study provides novel insights into the association between fungistasis and keystone or sensitive taxa in RSD-treated soil, with significant implications for comprehending the mechanisms of RSD.
Key points
• RSD enhanced bacteriome network stability and restored keystone taxa.
• Keystone taxa richness was negatively correlated with Fusarium abundance.
• Distinct sensitive OTUs and modules were formed in RSD soil.
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References
Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576. https://doi.org/10.1038/s41579-018-0024-1
Banerjee S, Schlaeppi K, van der Heijden MG (2019) Reply to ‘Can we predict microbial keystones?’ Nat Rev Microbiol 17:194–194. https://doi.org/10.1038/s41579-018-0133-x
Bao SD (2008) Soil agro-chemistrical analysis. China Agriculture Press, Beijing
Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. ICWSM 3:361–362. https://doi.org/10.1609/icwsm.v3i1.13937
Benjamini Y, Krieger AM, Yekutieli D (2006) Adaptive linear step-up procedures that control the false discovery rate. Biometrika 93:491–507. https://doi.org/10.1093/biomet/93.3.491
Bonanomi G, Lorito M, Vinale F, Woo SL (2018) Organic amendments, beneficial microbes, and soil microbiota: toward a unified framework for disease suppression. Annu Rev Phytopathol 56:1–20. https://doi.org/10.1146/annurev-phyto-080615-100046
Cania B, Vestergaard G, Krauss M, Fliessbach A, Schloter M, Schulz S (2019) A long-term field experiment demonstrates the influence of tillage on the bacterial potential to produce soil structure-stabilizing agents such as exopolysaccharides and lipopolysaccharides. Environ Microbiome 14:1–14. https://doi.org/10.1186/s40793-019-0341-7
Chaudhry V, Rehman A, Mishra A, Chauhan PS, Nautiyal CS (2012) Changes in bacterial community structure of agricultural land due to long-term organic and chemical amendments. Microb Ecol 64:450–460. https://doi.org/10.1007/s00248-012-0025-y
Chu H, Gao G, Ma Y, Fan K, Delgado-Baquerizo M (2020) Soil microbial biogeography in a changing world: recent advances and future perspectives. Msystems 5:e00803-e819. https://doi.org/10.1128/mSystems.00803-19
Clauset A, Newman ME, Moore C (2004) Finding community structure in very large networks. Phys Rev E 70:066111. https://doi.org/10.1103/PhysRevE.70.066111
Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJournal Complex Syst 1695:1–9. https://igraph.org
Dary M, Chamber-Pérez M, Palomares A, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330. https://doi.org/10.1016/j.jhazmat.2009.12.035
Delgado-Baquerizo M, Reith F, Dennis PG, Hamonts K, Powell JR, Young A, Singh BK, Bissett A (2018) Ecological drivers of soil microbial diversity and soil biological networks in the Southern Hemisphere. Ecology 99:583–596. https://doi.org/10.1002/ecy.2137
Delgado-Baquerizo M, Guerra CA, Cano-Díaz C, Egidi E, Wang J, Eisenhauer N, Singh BK, Maestre FT (2020) The proportion of soil-borne pathogens increases with warming at the global scale. Nat Clim Change 10:550–554. https://doi.org/10.1038/s41558-020-0759-3
Dickie IA, Cooper JA, Bufford JL, Hulme PE, Bates ST (2017) Loss of functional diversity and network modularity in introduced plant–fungal symbioses. Aob Plants 9:plw084. https://doi.org/10.1093/aobpla/plw084
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC (2016a) SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences. bioRxiv. https://doi.org/10.1101/074161
Edgar RC (2016b) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv. https://doi.org/10.1101/081257
Fan K, Weisenhorn P, Gilbert JA, Chu H (2018) Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biol Biochem 125:251–260. https://doi.org/10.1016/j.soilbio.2018.07.022
Gu Y, Banerjee S, Dini-Andreote F, Xu Y, Shen Q, Jousset A, Wei Z (2022) Small changes in rhizosphere microbiome composition predict disease outcomes earlier than pathogen density variations. ISME J 16:2448–2456. https://doi.org/10.1038/s41396-022-01290-z
Guimera R, Nunes Amaral LA (2005) Functional cartography of complex metabolic networks. Nature 433:895–900. https://doi.org/10.1038/nature03288
Guo J, Liu W, Zhu C, Luo G, Kong Y, Ling N, Wang M, Dai J, Shen Q, Guo S (2018) Bacterial rather than fungal community composition is associated with microbial activities and nutrient-use efficiencies in a paddy soil with short-term organic amendments. Plant Soil 424:335–349. https://doi.org/10.1007/s11104-017-3547-8
Han J, Luo Y, Yang L, Liu X, Wu L, Xu J (2014) Acidification and salinization of soils with different initial pH under greenhouse vegetable cultivation. J Soils Sed 14:1683–1692. https://doi.org/10.1007/s11368-014-0922-4
Hartman K, van der Heijden MGA, Wittwer RA, Banerjee S, Walser JC, Schlaeppi K (2018) Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming. Microbiome 6:14. https://doi.org/10.1186/s40168-017-0389-9
Houghton KM (2013) The physiological characterisation of a novel Thermomicrobia strain WKT50.2, and a review of the characteristics of the class Thermomicrobia. Doctoral, University of Waikato
Huang X, Bie Z, Huang Y (2010) Identification of autotoxins in rhizosphere soils under the continuous cropping of cowpea. Allelopathy J 25:383–392
Huang X, Zhao J, Zhou X, Han Y, Zhang J, Cai Z (2019a) How green alternatives to chemical pesticides are environmentally friendly and more efficient. Eur J Soil Sci 70:518–529. https://doi.org/10.1111/ejss.12755
Huang X, Zhao J, Zhou X, Zhang J, Cai Z (2019b) Differential responses of soil bacterial community and functional diversity to reductive soil disinfestation and chemical soil disinfestation. Geoderma 348:124–134. https://doi.org/10.1016/j.geoderma.2019.04.027
Kennedy AC, Smith KL (1995) Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170:75–86. https://doi.org/10.1007/BF02183056
Langfelder P, Horvath S (2012) Fast R functions for robust correlations and hierarchical clustering. J Stat Softw 46:i11
Lee CG, Kunitomo E, Iida T, Nakaho K, Ohkuma M (2020) Soil prokaryotes are associated with decreasing Fusarium oxysporum density during anaerobic soil disinfestation in the tomato field. Appl Soil Ecol 155:103632. https://doi.org/10.1016/j.apsoil.2020.103632
Li X, Zhang M, Zhang Q, Tan F, Gong Z, Xie Y, Tao Y, Chen J (2022) Insights into pyrroloquinoline quinone (PQQ) effects on soil nutrients and pathogens from pepper monocropping soil under anaerobic and aerobic conditions. Microbiol Spectr 10:e00933-e1022. https://doi.org/10.1128/spectrum.00933-22
Liu L, Long S, Deng B, Kuang J, Wen K, Li T, Bai Z, Shao Q (2022) Effects of plastic shed cultivation system on the properties of red paddy soil and its management by reductive soil disinfestation. Horticulturae 8:279. https://doi.org/10.3390/horticulturae8040279
Louca S, Parfrey LW, Doebeli M (2016) Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272–1277
Ma Z, Xie Y, Zhu L, Cheng L, Xiao X, Zhou C, Wang J (2017) Which of soil microbes is in positive correlation to yields of maize (Zea mays L.)? Plant Soil Environ 63:574–580
Meng T, Ren G, Wang G, Ma Y (2019) Impacts on soil microbial characteristics and their restorability with different soil disinfestation approaches in intensively cropped greenhouse soils. Appl Microbiol Biotechnol 103:6369–6383. https://doi.org/10.1007/s00253-019-09964-z
Momma N, Kobara Y, Momma M (2011) Fe2+ and Mn2+, potential agents to induce suppression of Fusarium oxysporum for biological soil disinfestation. J Gen Plant Pathol 77:331–335. https://doi.org/10.1007/s10327-011-0336-8
Momma N, Kobara Y, Uematsu S, Kita N, Shinmura A (2013) Development of biological soil disinfestations in Japan. Appl Microbiol Biotechnol 97:3801–3809. https://doi.org/10.1007/s00253-013-4826-9
Morriën E, Hannula SE, Snoek LB, Helmsing NR, Zweers H, De Hollander M, Soto RL, Bouffaud M-L, Buée M, Dimmers W (2017) Soil networks become more connected and take up more carbon as nature restoration progresses. Nat Commun 8:1–10. https://doi.org/10.1038/ncomms14349
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. PNAS 104:19891–19896. https://doi.org/10.1073/pnas.0706375104
Peng G, Wu J (2016) Optimal network topology for structural robustness based on natural connectivity. Physica A 443:212–220. https://doi.org/10.1016/j.physa.2015.09.023
Poret-Peterson AT, Sayed N, Glyzewski N, Forbes H, Gonzalez-Orta ET, Kluepfel DA (2020) Temporal responses of microbial communities to anaerobic soil disinfestation. Microb Ecol 80:191–201. https://doi.org/10.1007/s00248-019-01477-6
Prasad S, Malav LC, Choudhary J, Kannojiya S, Kundu M, Kumar S, Yadav AN (2021) Soil microbiomes for healthy nutrient recycling. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer Singapore, Singapore, pp 1–21
Priyashantha AKH, Attanayake RN (2021) Can anaerobic soil disinfestation (ASD) be a game changer in tropical agriculture? Pathogens 10:133. https://doi.org/10.3390/pathogens10020133
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
Rosskopf EN, Serrano-Pérez P, Hong J, Shrestha U, Rodríguez-Molina MdC, Martin K, Kokalis-Burelle N, Shennan C, Muramoto J, Butler D (2015) Anaerobic soil disinfestation and soilborne pest management. In: Meghvansi MK, Varma A (eds) Organic amendments and soil suppressiveness in plant disease management. Springer International Publishing, Cham, pp 277–305
Rosskopf E, Di Gioia F, Hong JC, Pisani C, Kokalis-Burelle N (2020) Organic amendments for pathogen and nematode control. Annu Rev Phytopathol 58:277–311. https://doi.org/10.1146/annurev-phyto-080516-035608
Shen W, Hu M, Qian D, Xue H, Gao N, Lin X (2021) Microbial deterioration and restoration in greenhouse-based intensive vegetable production systems. Plant Soil 463:1–18. https://doi.org/10.1007/s11104-021-04933-w
Shi Y, Fan K, Li Y, Yang T, He J, Chu H (2019) Archaea enhance the robustness of microbial co-occurrence networks in Tibetan Plateau soils. Soil Sci Soc Am J 83:1093–1099. https://doi.org/10.2136/sssaj2018.11.0426
Shi Y, Xu M, Zhao Y, Cheng L, Chu H (2022) Soil pH determines the spatial distribution, assembly processes, and co-existence networks of microeukaryotic community in wheat fields of the North China Plain. Front Microbiol 13:2276. https://doi.org/10.3389/fmicb.2022.911116
Shirane S, Momma N, Usami T, Suzuki C, Hori T, Aoyagi T, Amachi S (2023) Fungicidal activity of caproate produced by Clostridium sp strain E801, a bacterium isolated from cocopeat medium subjected to anaerobic soil disinfestation. Agronomy 13:747. https://doi.org/10.3390/agronomy13030747
Song Z, Massart S, Yan D, Cheng H, Eck M, Berhal C, Ouyang C, Li Y, Wang Q, Cao A (2020) Composted chicken manure for anaerobic soil disinfestation increased the strawberry yield and shifted the soil microbial communities. Sustainability-Basel 12:6313. https://doi.org/10.3390/su12166313
Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, Chow C-ET, Sachdeva R, Jones AC, Schwalbach MS (2011) Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J 5:1414–1425. https://doi.org/10.1038/ismej.2011.24
Strauss SL, Greenhut RF, McClean AE, Kluepfel DA (2017) Effect of anaerobic soil disinfestation on the bacterial community and key soilborne phytopathogenic agents under walnut tree-crop nursery conditions. Plant Soil 415:493–506. https://doi.org/10.1007/s11104-016-3126-4
Swilling KJ, Shrestha U, Ownley BH, Gwinn KD, Butler DM (2022) Volatile fatty acid concentration, soil pH and soil texture during anaerobic soil conditions affect viability of Athelia (Sclerotium) rolfsii sclerotia. Eur J Plant Pathol 162:149–161. https://doi.org/10.1007/s10658-021-02392-8
Tao Y, Zhang Q, Long S, Li X, Chen J, Li X (2022) Shifts of lipid metabolites help decode immobilization of soil cadmium under reductive soil disinfestation. Sci Total Environ 829:154592. https://doi.org/10.1016/j.scitotenv.2022.154592
Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. PNAS 108:20260–20264. https://doi.org/10.1073/pnas.1116437108
Toju H, Peay KG, Yamamichi M, Narisawa K, Hiruma K, Naito K, Fukuda S, Ushio M, Nakaoka S, Onoda Y (2018) Core microbiomes for sustainable agroecosystems. Nat Plants 4:247–257. https://doi.org/10.1038/s41477-018-0139-4
Ueki A, Kaku N, Ueki K (2018) Role of anaerobic bacteria in biological soil disinfestation for elimination of soil-borne plant pathogens in agriculture. Appl Microbiol Biotechnol 102:6309–6318. https://doi.org/10.1007/s00253-018-9119-x
Ueki A, Takehara T, Ishioka G, Kaku N, Ueki K (2020) β-1,3-Glucanase production as an anti-fungal enzyme by phylogenetically different strains of the genus Clostridium isolated from anoxic soil that underwent biological disinfestation. Appl Microbiol Biotechnol 104:5563–5578. https://doi.org/10.1007/s00253-020-10626-8
Ueki A, Tonouchi A, Kaku N, Ueki K (2023) Anaeromicropila herbilytica gen. nov., sp. nov., a plant polysaccharide-decomposing anaerobic bacterium isolated from anoxic soil subjected to reductive soil disinfestation, and reclassification of Clostridium populeti as Anaeromicropila populeti comb. nov. Int J Syst Evol Microbiol 73:005695. https://doi.org/10.1099/ijsem.0.005695
Wei Z (2019) Initial soil microbiome composition and functioning predetermine future plant health. Sci Adv 5(1):eaaw0759. https://doi.org/10.1126/sciadv.aaw0759
Yan Y, Wu R, Li S, Su Z, Shao Q, Cai Z, Huang X, Liu L (2022) Reductive soil disinfestation enhances microbial network complexity and function in intensively cropped greenhouse soil. Horticulturae 8:476. https://doi.org/10.3390/horticulturae8060476
Yang W, Jeelani N, Zhu Z, Luo Y, Cheng X, An S (2019) Alterations in soil bacterial community in relation to Spartina alterniflora Loisel. invasion chronosequence in the eastern Chinese coastal wetlands. Appl Soil Ecol 135:38–43. https://doi.org/10.1016/j.apsoil.2018.11.009
Zhang D, Ji X, Meng Z, Qi W, Qiao K (2019) Effects of fumigation with 1, 3-dichloropropene on soil enzyme activities and microbial communities in continuous-cropping soil. Ecotoxicol Environ Saf 169:730–736. https://doi.org/10.1016/j.ecoenv.2018.11.071
Zhang H, Zheng X, Wang X, Xiang W, Xiao M, Wei L, Zhang Y, Song K, Zhao Z, Lv W (2022) Effect of fertilization regimes on continuous cropping growth constraints in watermelon is associated with abundance of key ecological clusters in the rhizosphere. Agr Ecosyst Environ 339:108135. https://doi.org/10.1016/j.agee.2022.108135
Zhao J, Zhou X, Jiang A, Fan J, Lan T, Zhang J, Cai Z (2018) Distinct impacts of reductive soil disinfestation and chemical soil disinfestation on soil fungal communities and memberships. Appl Microbiol Biotechnol 102:7623–7634. https://doi.org/10.1007/s00253-018-9107-1
Zhao J, Liu S, Zhou X, Xia Q, Liu X, Zhang S, Zhang J, Cai Z, Huang X (2020) Reductive soil disinfestation incorporated with organic residue combination significantly improves soil microbial activity and functional diversity than sole residue incorporation. Appl Microbiol Biotechnol 104:7573–7588. https://doi.org/10.1007/s00253-020-10778-7
Zhu W, Wang W, Hong C, Ding J, Zhu F, Hong L, Yao Y (2022) Influence of reductive soil disinfestation on the chemical and microbial characteristics of a greenhouse soil infested with Fusarium oxysporum. Physiol Mol Plant Pathol 118:101805. https://doi.org/10.1016/j.pmpp.2022.101805
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This work was financially supported by the Natural Science Foundation of Zhejiang Province (LQ21D010002), the Science and Technology Program of Zhejiang Province (2020C02030), the Department of Agriculture and Rural Development of Zhejiang Province (2022SNJF024), and the Zhejiang Provincial Silkworm and Bee Resources Utilization and Innovation Research Key Laboratory (2020E10025).
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ZW and YY conceived and designed the research. ZW, HC, and LX conducted experiments. ZF and HL performed analyses. DJ and ZW contributed new reagents or analytical tools. ZW wrote the manuscript. All authors read and approved the manuscript.
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Zhu, W., Lu, X., Hong, C. et al. Pathogen resistance in soils associated with bacteriome network reconstruction through reductive soil disinfestation. Appl Microbiol Biotechnol 107, 5829–5842 (2023). https://doi.org/10.1007/s00253-023-12676-0
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DOI: https://doi.org/10.1007/s00253-023-12676-0