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Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health

Abstract

Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life.

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Fig. 1: Effects and underlying drivers of organic and chemical fertilizer treatments on Fusarium wilt disease incidence and banana yield.
Fig. 2: Comparison of protistan and bacterial community composition and correlations of key protistan and bacterial OTU, predatory protists and Fusarium oxysporum density, and predatory protists and Bacillus/ bacteria.
Fig. 3: Microbial functional genes and their potential interactions with pathogen density.
Fig. 4: Pathogen suppression capability of predatory protists and their potential interactions with Bacillus and NRPS gene.
Fig. 5: Interactions between the pathogen, the bacterial isolates and the predator in the greenhouse experiment.
Fig. 6: Conceptual model.

Data availability

All raw 16 S rRNA, ITS and 18 S rRNA gene sequences are available at the NCBI Sequence Read Archive (SRA) under the accession number BioProject PRJNA737165. The raw data of metagenomics-derived gene catalogues are publicly available under the accession number BioProject PRJNA736854.

References

  1. Amundson R, Berhe AA, Hopmans JW, Olson C, Sztein AE, Sparks DL. Soil and human security in the 21st century. Science. 2015;348:1261071.

    PubMed  Article  CAS  Google Scholar 

  2. Borrelli P, Robinson DA, Fleischer LR, Lugato E, Ballabio C, Alewell C, et al. An assessment of the global impact of 21st century land use change on soil erosion. Nat Commun. 2017;8:2013.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  3. Carvalho FP. Pesticides, environment, and food safety. Food Energy Secur. 2017;6:48–60.

    Article  Google Scholar 

  4. Santos VB, Araújo ASF, Leite LFC, Nunes LAPL, Melo WJ. Soil microbial biomass and organic matter fractions during transition from conventional to organic farming systems. Geoderma. 2012;170:227–31.

    CAS  Article  Google Scholar 

  5. Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, et al. Forecasting agriculturally driven global environmental change. Science. 2001;292:281–4.

    CAS  PubMed  Article  Google Scholar 

  6. Tu C, Louws FJ, Creamer NG, Paul Mueller J, Brownie C, Fager K, et al. Responses of soil microbial biomass and N availability to transition strategies from conventional to organic farming systems. Agric Ecosyst Environ. 2006;113:206–15.

    Article  Google Scholar 

  7. Blundell R, Schmidt JE, Igwe A, Cheung AL, Vannette RL, Gaudin ACM, et al. Organic management promotes natural pest control through altered plant resistance to insects. Nat Plants. 2020;6:483–91.

    CAS  PubMed  Article  Google Scholar 

  8. Verbruggen E, Röling WFM, Gamper HA, Kowalchuk GA, Verhoef HA, van der Heijden MGA. Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. N. Phytol. 2010;186:968–79.

    CAS  Article  Google Scholar 

  9. Lupatini M, Korthals GW, de Hollander M, Janssens TKS, Kuramae EE. Soil microbiome is more heterogeneous in organic than in conventional farming system. Front Microbiol. 2017;7:2064.

    PubMed  PubMed Central  Article  Google Scholar 

  10. Cheng H, Zhang D, Ren L, Song Z, Li Q, Wu J, et al. Bio-activation of soil with beneficial microbes after soil fumigation reduces soil-borne pathogens and increases tomato yield. Environ Pollut. 2021;283:117160.

    CAS  PubMed  Article  Google Scholar 

  11. Shahi DK, Kachhap S, Kumar A, Agarwal BK. Organic agriculture for plant disease management. In: Singh KP, Jahagirdar S, Sarma BK. (eds). Emerging Trends in Plant Pathology. 2021. Springer, Singapore, pp 643–62.

  12. Francioli D, Schulz E, Lentendu G, Wubet T, Buscot F, Reitz T. Mineral vs organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Front Microbiol. 2016;7:1446.

    PubMed  PubMed Central  Article  Google Scholar 

  13. Sanchez-Barrios A, Sahib MR, DeBolt S. “I’ve got the magic in me”: the microbiome of conventional vs organic production systems. In: Singh DP, Singh HB, Prabha R. (eds). Plant-Microbe Interactions in Agro-Ecological Perspectives: Volume 1: Fundamental Mechanisms, Methods and Functions. 2017. Springer, Singapore, pp 85–95.

  14. Chowdhury SP, Babin D, Sandmann M, Jacquiod S, Sommermann L, Sørensen SJ, et al. Effect of long-term organic and mineral fertilization strategies on rhizosphere microbiota assemblage and performance of lettuce. Environ Microbiol. 2019;21:2426–39.

    Article  CAS  Google Scholar 

  15. Weller DM. Pseudomonas biocontrol agents of soilborne pathogens: Looking back over 30 years. Phytopathology 2007;97:250–6.

    PubMed  Article  Google Scholar 

  16. Tao C, Li R, Xiong W, Shen Z, Liu S, Wang B, et al. Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 2020;8:137.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  17. Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM. Phenazine antibiotics produced by fluorescent Pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J. 2009;3:977–91.

    CAS  PubMed  Article  Google Scholar 

  18. Yuan J, Zhao M, Li R, Huang Q, Rensing C, Shen Q. Lipopeptides produced by B. amyloliquefaciens NJN-6 altered the soil fungal community and non-ribosomal peptides genes harboring microbial community. Appl Soil Ecol. 2017;117–8:96–105.

    Article  Google Scholar 

  19. Kiesewalter HT, Lozano-Andrade CN, Strube ML, Kovács ÁT. Secondary metabolites of Bacillus subtilis impact the assembly of soil-derived semisynthetic bacterial communities. Beilstein J Org Chem. 2020;16:2983–98.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. Banerjee S, Schlaeppi K, van der Heijden MGA. Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol. 2018;16:567–76.

    CAS  PubMed  Article  Google Scholar 

  21. Zhang Z, Han X, Yan J, Zou W, Wang E, Lu X, et al. Keystone microbiomes revealed by 14 years of field restoration of the degraded agricultural soil under distinct vegetation scenarios. Front Microbiol. 2020;11:1915.

    PubMed  PubMed Central  Article  Google Scholar 

  22. Shang X, Cai X, Zhou Y, Han X, Zhang C-S, Ilyas N, et al. Pseudomonas inoculation stimulates endophytic Azospira population and induces systemic resistance to bacterial wilt. Front Plant Sci. 2021;12:1964.

    Article  Google Scholar 

  23. Tyc O, Song C, Dickschat JS, Vos M, Garbeva P. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol. 2017;25:280–92.

    CAS  PubMed  Article  Google Scholar 

  24. Cornforth DM, Foster KR. Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol. 2013;11:285–93.

    CAS  PubMed  Article  Google Scholar 

  25. Berg G, Mahnert A, Moissl-Eichinger C. Beneficial effects of plant-associated microbes on indoor microbiomes and human health? Front Microbiol. 2014;5:15.

    PubMed  PubMed Central  Google Scholar 

  26. Straight PD, Willey JM, Kolter R. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J Bacteriol. 2006;188:4918–25.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. González O, Ortíz-Castro R, Díaz-Pérez C, Díaz-Pérez AL, Magaña-Dueñas V, López-Bucio J, et al. Non-ribosomal peptide synthases from Pseudomonas aeruginosa play a role in cyclodipeptide biosynthesis, quorum-sensing regulation, and root development in a plant host. Micro Ecol. 2017;73:616–29.

    Article  CAS  Google Scholar 

  28. Zhao M, Yuan J, Zhang R, Dong M, Deng X, Zhu C, et al. Microflora that harbor the NRPS gene are responsible for Fusarium wilt disease-suppressive soil. Appl Soil Ecol. 2018;132:83–90.

    Article  Google Scholar 

  29. Caulier S, Nannan C, Gillis A, Licciardi F, Bragard C, Mahillon J. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front Microbiol. 2019;10:302.

    PubMed  PubMed Central  Article  Google Scholar 

  30. Tambadou F, Lanneluc I, Sablé S, Klein GL, Doghri I, Sopéna V, et al. Novel nonribosomal peptide synthetase (NRPS) genes sequenced from intertidal mudflat bacteria. FEMS Microbiol Lett. 2014;357:123–30.

    CAS  PubMed  Google Scholar 

  31. Prieto C. Characterization of nonribosomal peptide synthetases with NRPSsp. In: Evans BS. (ed). Nonribosomal Peptide and Polyketide Biosynthesis: Methods and Protocols. 2016. Springer, New York, NY, pp 273–8.

  32. Yuan J, Ruan Y, Wang B, Zhang J, Waseem R, Huang Q, et al. Plant growth-promoting rhizobacteria strain Bacillus amyloliquefaciens NJN-6-enriched bio-organic fertilizer suppressed Fusarium wilt and promoted the growth of banana plants. J Agric Food Chem. 2013;61:3774–80.

    CAS  PubMed  Article  Google Scholar 

  33. Yuan J, Li B, Zhang N, Waseem R, Shen Q, Huang Q. Production of bacillomycin- and macrolactin-type antibiotics by Bacillus amyloliquefaciens NJN-6 for suppressing soilborne plant pathogens. J Agric Food Chem. 2012;60:2976–81.

    CAS  PubMed  Article  Google Scholar 

  34. Xiong W, Song Y, Yang K, Gu Y, Wei Z, Kowalchuk GA, et al. Rhizosphere protists are key determinants of plant health. Microbiome. 2020;8:27.

    PubMed  PubMed Central  Article  Google Scholar 

  35. Thakur MP, Geisen S. Trophic regulations of the soil microbiome. Trends Microbiol. 2019;27:771–80.

    CAS  PubMed  Article  Google Scholar 

  36. Müller MS, Scheu S, Jousset A. Protozoa drive the dynamics of culturable biocontrol bacterial communities. PLOS ONE. 2013;8:e66200.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  37. Geisen S, Mitchell EAD, Adl S, Bonkowski M, Dunthorn M, Ekelund F, et al. Soil protists: A fertile frontier in soil biology research. FEMS Microbiol Rev. 2018;42:293–323.

    CAS  PubMed  Article  Google Scholar 

  38. Gao Z, Karlsson I, Geisen S, Kowalchuk G, Jousset A. Protists: puppet masters of the rhizosphere microbiome. Trends Plant Sci. 2019;24:165–76.

    CAS  PubMed  Article  Google Scholar 

  39. Jousset A, Lara E, Wall LG, Valverde C. Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl Environ Microbiol. 2006;72:7083–90.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Liu H, Xiong W, Zhang R, Hang X, Wang D, Li R, et al. Continuous application of different organic additives can suppress tomato disease by inducing the healthy rhizospheric microbiota through alterations to the bulk soil microflora. Plant Soil. 2018;423:229–40.

    CAS  Article  Google Scholar 

  41. Chen D, Wang X, Zhang W, Zhou Z, Ding C, Liao Y, et al. Persistent organic fertilization reinforces soil-borne disease suppressiveness of rhizosphere bacterial community. Plant Soil. 2020;452:313–28.

    CAS  Article  Google Scholar 

  42. Müller JP, Hauzy C, Hulot FD. Ingredients for protist coexistence: Competition, endosymbiosis and a pinch of biochemical interactions. J Anim Ecol. 2012;81:222–32.

    PubMed  Article  Google Scholar 

  43. Guo S, Xiong W, Hang X, Gao Z, Jiao Z, Liu H, et al. Protists as main indicators and determinants of plant performance. Microbiome. 2021;9:64.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. Ren F, Sun N, Xu M, Zhang X, Wu L, Xu M. Changes in soil microbial biomass with manure application in cropping systems: a meta-analysis. Soil Tillage Res. 2019;194:104291.

    Article  Google Scholar 

  45. Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.

    CAS  PubMed  Article  Google Scholar 

  46. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y. The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil. 2009;321:341–61.

    CAS  Article  Google Scholar 

  47. Compant S, Cambon MC, Vacher C, Mitter B, Samad A, Sessitsch A. The plant endosphere world – bacterial life within plants. Environ Microbiol. 2021;23:1812–29.

    PubMed  Article  Google Scholar 

  48. Oliverio AM, Geisen S, Delgado-Baquerizo M, Maestre FT, Turner BL, Fierer N. The global-scale distributions of soil protists and their contributions to belowground systems. Sci Adv. 2020;6:eaax8787.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. Dumack K, Fiore-Donno AM, Bass D, Bonkowski M. Making sense of environmental sequencing data: ecologically important functional traits of the protistan groups Cercozoa and Endomyxa (Rhizaria). Mol Ecol Resour. 2020;20:398–403.

    PubMed  Article  Google Scholar 

  50. Romdhane S, Spor A, Banerjee S, Breuil M-C, Bru D, Chabbi A, et al. Land-use intensification differentially affects bacterial, fungal and protist communities and decreases microbiome network complexity. Environ Microbiome. 2022;17:1.

    PubMed  PubMed Central  Article  Google Scholar 

  51. Jousset A, Rochat L, Péchy-Tarr M, Keel C, Scheu S, Bonkowski M. Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters. ISME J. 2009;3:666–74.

    CAS  PubMed  Article  Google Scholar 

  52. Yu GY, Sinclair JB, Hartman GL, Bertagnolli BL. Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem. 2002;34:955–63.

    CAS  Article  Google Scholar 

  53. Romero D, de Vicente A, Rakotoaly RH, Dufour SE, Veening J-W, Arrebola E, et al. The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Microbe Interact. 2007;20:430–40.

    CAS  PubMed  Article  Google Scholar 

  54. Xu Z, Mandic-Mulec I, Zhang H, Liu Y, Sun X, Feng H, et al. Antibiotic bacillomycin D affects iron acquisition and biofilm formation in Bacillus velezensis through a Btr-mediated FeuABC-dependent pathway. Cell Rep. 2019;29:1192–1202.e5.

    CAS  PubMed  Article  Google Scholar 

  55. Huang J, Wei Z, Tan S, Mei X, Shen Q, Xu Y. Suppression of bacterial wilt of tomato by bioorganic fertilizer made from the antibacterial compound producing strain Bacillus amyloliquefaciens HR62. J Agric Food Chem. 2014;62:10708–16.

    CAS  PubMed  Article  Google Scholar 

  56. Wang B, Shen Z, Zhang F, Raza W, Yuan J, Huang R, et al. Bacillus amyloliquefaciens strain W19 can promote growth and yield and suppress Fusarium wilt in banana under greenhouse and field conditions. Pedosphere. 2016;26:733–44.

    CAS  Article  Google Scholar 

  57. Shen Z, Ruan Y, Chao X, Zhang J, Li R, Shen Q. Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fertil Soils. 2015;51:553–62.

    CAS  Article  Google Scholar 

  58. Jeger MJ, Eden-Green S, Thresh JM, Johanson A, Waller JM, Brown AE. Banana diseases. In: Gowen S. (ed). Bananas and Plantains. 1995. Springer Netherlands, Dordrecht, pp 317–81.

  59. Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci. 2015;112:E911–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Fierer N, Jackson JA, Vilgalys R, Jackson RB. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol. 2005;71:4117–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. Jiménez-Fernández D, Montes-Borrego M, Navas-Cortés JA, Jiménez-Díaz RM, Landa BB. Identification and quantification of Fusarium oxysporum in planta and soil by means of an improved specific and quantitative PCR assay. Appl Soil Ecol. 2010;46:372–82.

    Article  Google Scholar 

  62. Mori K, Iriye R, Hirata M, Takamizawa K. Quantification of Bacillus species in a wastewater treatment system by the molecular analyses. Biotechnol Bioprocess Eng. 2004;9:482–9.

    CAS  Article  Google Scholar 

  63. Ayuso-Sacido A, Genilloud O. New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Micro Ecol. 2005;49:10–24.

    CAS  Article  Google Scholar 

  64. Fu L, Penton CR, Ruan Y, Shen Z, Xue C, Li R, et al. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol Biochem. 2017;104:39–48.

    CAS  Article  Google Scholar 

  65. Claesson MJ, O’Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H, et al. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLOS ONE. 2009;4:e6669.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  66. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ. (eds). PCR Protocols. 1990. Academic Press, San Diego, pp 315–22.

  67. Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113–8.

    CAS  PubMed  Article  Google Scholar 

  68. Bass D, Silberman JD, Brown MW, Pearce RA, Tice AK, Jousset A, et al. Coprophilic amoebae and flagellates, including Guttulinopsis, Rosculus and Helkesimastix, characterise a divergent and diverse rhizarian radiation and contribute to a large diversity of faecal-associated protists. Environ Microbiol. 2016;18:1604–19.

    CAS  PubMed  Article  Google Scholar 

  69. Geisen S, Vaulot D, Mahé F, Lara E, Vargas C de, Bass D. A user guide to environmental protistology: primers, metabarcoding, sequencing, and analyses. BioRxiv 2019;850610:1–34.

  70. Xiong W, Jousset A, Li R, Delgado-Baquerizo M, Bahram M, Logares R, et al. A global overview of the trophic structure within microbiomes across ecosystems. Environ Int. 2021;151:106438.

    PubMed  Article  Google Scholar 

  71. Xiong W, Li R, Ren Y, Liu C, Zhao Q, Wu H, et al. Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem. 2017;107:198–207.

    CAS  Article  Google Scholar 

  72. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): A catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2013;41:D597–D604.

    CAS  PubMed  Article  Google Scholar 

  75. Xiong W, Li R, Guo S, Karlsson I, Jiao Z, Xun W, et al. Microbial amendments alter protist communities within the soil microbiome. Soil Biol Biochem. 2019;135:379–82.

    CAS  Article  Google Scholar 

  76. Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2016;44:D286–93.

    CAS  PubMed  Article  Google Scholar 

  77. Revelle W, Revelle MW. Package ‘psych’. Compr R Arch Netw. 2015;337:338.

    Google Scholar 

  78. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.

    Google Scholar 

  79. Bargabus RL, Zidack NK, Sherwood JE, Jacobsen BJ. Characterisation of systemic resistance in sugar beet elicited by a non-pathogenic, phyllosphere-colonizing Bacillus mycoides, biological control agent. Physiol Mol Plant Pathol. 2002;61:289–98.

    CAS  Article  Google Scholar 

  80. Bais HP, Fall R, Vivanco JM. Biocontrol of Bacillus subtilis against infection of arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 2004;134:307–19.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  81. Cazorla FM, Romero D, Pérez-García A, Lugtenberg BJJ, Vicente Ade, Bloemberg G. Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol. 2007;103:1950–9.

    CAS  PubMed  Article  Google Scholar 

  82. Aneja KR. Experiments in microbiology, plant pathology and biotechnology. 2007. New Age International, New Delhi.

  83. Mela F, Fritsche K, de Boer W, van Veen JA, de Graaff LH, van den Berg M, et al. Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J. 2011;5:1494–504.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. Gao Z. Soil protists: From traits to ecological functions. 2020. Utrecht University.

  85. Anderson MJ. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online. 2017. American Cancer Society, pp 1–15.

  86. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, et al. Package ‘vegan’. Community Ecol Package Version. 2013;2:1–295.

    Google Scholar 

  87. Breiman L. Random forests. Mach Learn. 2001;45:5–32.

    Article  Google Scholar 

  88. Liaw A, Wiener M. Classification and regression by randomForest. R N. 2002;23:18–22.

    Google Scholar 

  89. Archer E. rfPermute: Estimate permutation p-values for random forest importance metrics. R Package Version 20 2016.

  90. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.

    PubMed  PubMed Central  Article  Google Scholar 

  91. Oguntunde PG, Fosu M, Ajayi AE, van de Giesen N. Effects of charcoal production on maize yield, chemical properties and texture of soil. Biol Fertil Soils. 2004;39:295–9.

    CAS  Article  Google Scholar 

  92. Mcdonald JH. Handbook of biological statistics. 2009. Baltimore: sparky house publishing, Baltimore.

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Acknowledgements

This study was funded by the National Natural Science Foundation of China (42090065, 31972509, 41867006 and 32102475), the Fundamental Research Funds for the Central Universities (KYXK202009), the China Postdoctoral Science Foundation (2021TQ0156 and 2021M691613), the 111 project (B12009), and the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD). Stefan Geisen was supported by an NWO-VENI grant from the Netherlands Organisation for Scientific Research (016.Veni.181.078).

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SG, CT, AJ, WX, ZX, ZG, RL, QS, GAK and SG developed the ideas and designed the experimental plans. SG, CT, ZW, ZS, BW, SL, RL and YR performed the experiments. SG, CT, WX, RL and SG analyzed the data. SG, CT, AJ, RL, QS, GAK and SG participated in the completion of the manuscript.

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Correspondence to Rong Li or Qirong Shen.

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Guo, S., Tao, C., Jousset, A. et al. Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health. ISME J 16, 1932–1943 (2022). https://doi.org/10.1038/s41396-022-01244-5

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