Biofertilizer induces soil disease suppression by activating pathogen suppressive protist taxa

1. Gardi, C., Jeffery, S. & Saltelli, A. An estimate of potential threats levels to soil biodiversity in EU. Glob. Change Biol. 19, 1538–1548 (2013).

   Google Scholar 

2. Wardle, D. A. et al. Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecol. Monogr. 69, 535–568 (1999).

   Google Scholar 

3. Dong, L., Xu, J., Feng, G., Li, X. & Chen, S. Soil bacterial and fungal community dynamics in relation to Panax notoginseng death rate in a continuous cropping system. Sci. Rep. 6, 31802 (2016).

   Google Scholar 

4. Huang, M. et al. Effects of fertilization methods on chemical properties, enzyme activity, and fungal community structure of black soil in Northeast China. Diversity 12, 476 (2020).

   Google Scholar 

5. Li, Y. et al. Effects of organic fertilizer application on crop yield and soil properties in rice-wheat rotation system: a meta-analysis. Yingyong Shengtai Xuebao 32, 3231–3239 (2021).

   Google Scholar 

6. Shi, Y., Zhao, X., Gao, X., Zhang, S. & Wu, P. The effects of long-term fertiliser applications on soil organic carbon and hydraulic properties of a loess soil in China. Land Degrad. Dev. 27, 60–67 (2016).

   Google Scholar 

7. Chen, Q., Zhang, X., Zhao, H. & Guan, J. Advance in research and application of some functional microbes in bio-organic fertilizer. Chin. J. Appl. Environ. Biol 16, 294–300 (2010).

   Google Scholar 

8. Liu, W., Cui, S. & Wu, L. Effects of Bio-organic Fertilizer on Soil Fertility, Yield, and Quality of Tea. J Soil Sci Plant Nutr. 23, 5109–5121 (2023).

   Google Scholar 

9. Noble, R. Risks and benefits of soil amendment with composts in relation to plant pathogens. Australas. Plant Pathol. 40, 157–167 (2011).

   Google Scholar 

10. Deng, X. et al. Bio-organic soil amendment promotes the suppression of Ralstonia solanacearum by inducing changes in the functionality and composition of rhizosphere bacterial communities. New Phytol. 235, 1558–1574 (2022).

    Google Scholar 

11. Liu, H. 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 423, 1–12 (2018).

    Google Scholar 

12. Tao, C. et al. Additive fungal interactions drive biocontrol of Fusarium wilt disease. New Phytol. 238, 1198–1214 (2023).

    Google Scholar 

13. Handelsman, J. & Stabb, E. V. Biocontrol of soilborne plant pathogens. Plant Cell 8, 1855–1869 (1996).

    Google Scholar 

14. Li, B. et al. Responses of beneficial Bacillus amyloliquefaciens SQR9 to different soilborne fungal pathogens through the alteration of antifungal compounds production. Front. Microbiol. 5, 636 (2014).

    Google Scholar 

15. Mavrodi, D. V., Yang, M., Mavrodi, O. V. & Wen, S. Management of Soilborne Plant Pathogens with Beneficial Root-Colonizing Pseudomonas. Advances in PGPR Research 147–164 (Cabi Publishing-C a B Int, CABI Publishing, Wallingford 0X10 8DE, OXON, UK, 2017).

16. Weller, D. Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97, 250–256 (2007).

    Google Scholar 

17. Bashan, Y., de-Bashan, L. E., Prabhu, S. R. & Hernandez, J.-P. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378, 1–33 (2014).

    Google Scholar 

18. Mawarda, P. C., Le Roux, X., Acosta, M. U., van Elsas, J. D. & Salles, J. F. The impact of protozoa addition on the survivability of Bacillus inoculants and soil microbiome dynamics. ISME Commun. 2, 1–9 (2022).

    Google Scholar 

19. Gao, Z., Karlsson, I., Geisen, S., Kowalchuk, G. & Jousset, A. Protists: puppet masters of the rhizosphere microbiome. Trends Plant Sci. 24, 165–176 (2019).

    Google Scholar 

20. Geisen, S. et al. Soil protists: a fertile frontier in soil biology research. FEMS Microbiol. Rev 42, 293–323 (2018).

    Google Scholar 

21. Guo, S. et al. Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health. ISME J. 16, 1932–1943 (2022).

    Google Scholar 

22. Guo, S. et al. Protists as main indicators and determinants of plant performance. Microbiome 9, 64 (2021).

    Google Scholar 

23. Xiong, W. et al. Rhizosphere protists are key determinants of plant health. Microbiome 8, 27 (2020).

    Google Scholar 

24. Fan, B. et al. Bacillus velezensis FZB42 in 2018: the gram-positive model strain for plant growth promotion and biocontrol. Front. Microbiol. 9, 2491 (2018).

    Google Scholar 

25. McDaniel, R., Ebert-Khosla, S., Hopwood, D. A. & Khosla, C. Engineered biosynthesis of novel polyketides. Science 262, 1546–1550 (1993).

    Google Scholar 

26. Betina, V. Biological effects of the antibiotic brefeldin A (decumbin, cyanein, ascotoxin, synergisidin): a retrospective. Folia Microbiol. 37, 3–11 (1992).

    Google Scholar 

27. Ai, C. et al. Reduced dependence of rhizosphere microbiome on plant-derived carbon in 32-year long-term inorganic and organic fertilized soils. Soil Biol. Biochem. 80, 70–78 (2015).

    Google Scholar 

28. Ling, N. et al. Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biol. Biochem. 99, 137–149 (2016).

    Google Scholar 

29. Li, H.-Z. et al. Effects of soil protists on the antibiotic resistome under long term fertilization. Environ. Pollut. 307, 119516 (2022).

    Google Scholar 

30. Murase, J. et al. Impact of long-term fertilizer treatment on the microeukaryotic community structure of a rice field soil. Soil Biol. Biochem. 80, 237–243 (2015).

    Google Scholar 

31. Li, F. et al. Specific protistan consumers and parasites are responsive to inorganic fertilization in rhizosphere and bulk soils. J. Soils Sediments 21, 3801–3812 (2021).

    Google Scholar 

32. Ren, P. et al. Predatory protists play predominant roles in suppressing soil-borne fungal pathogens under organic fertilization regimes. Sci. Total Environ. 863, 160986 (2023).

    Google Scholar 

33. Zhao, Z.-B. et al. Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome 7, 33 (2019).

    Google Scholar 

34. Jeyanthi, V. & Kanimozhi, S. Plant growth promoting rhizobacteria (PGPR) – prospective and mechanisms: a review. J. Pure Appl. Microbiol. 12, 733–749 (2018).

    Google Scholar 

35. Philippot, L. et al. Loss in microbial diversity affects nitrogen cycling in soil. ISME J. 7, 1609–1619 (2013).

    Google Scholar 

36. Trap, J., Bonkowski, M., Plassard, C., Villenave, C. & Blanchart, E. Ecological importance of soil bacterivores for ecosystem functions. Plant Soil 398, 1–24 (2016).

    Google Scholar 

37. Bonkowski, M. Protozoa and plant growth: the microbial loop in soil revisited. New Phytol. 162, 617–631 (2004).

    Google Scholar 

38. Dumack, K. et al. What drives the assembly of plant-associated protist microbiomes? Investigating the effects of crop species, soil type and bacterial microbiomes. Protist 173, 125913 (2022).

    Google Scholar 

39. Li, W. & Stevens, M. H. H. Community temporal variability increases with fluctuating resource availability. Sci. Rep. 7, 45280 (2017).

    Google Scholar 

40. Kiesewalter, H. T. et al. Genomic and chemical diversity of Bacillus subtilis secondary metabolites against plant pathogenic fungi. mSystems 6, e00770-20 (2021).

    Google Scholar 

41. Yin, Q.-J. et al. Species-specificity of the secondary biosynthetic potential in Bacillus. Front. Microbiol. 14, 1271418 (2023).

    Google Scholar 

42. Liu, C. et al. Protist predation promotes antimicrobial resistance spread through antagonistic microbiome interactions. ISME J 18, 1 (2024).

    Google Scholar 

43. Jousset, A., Lara, E., Wall, L. G. & Valverde, C. Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl. Environ. Microbiol. 72, 7083–7090 (2006).

    Google Scholar 

44. Cornforth, D. M. & Foster, K. R. Competition sensing: the social side of bacterial stress responses. Nat. Rev. Microbiol. 11, 285–293 (2013).

    Google Scholar 

45. Sukhanova, E., Zimens, E., Kaluzhnaya, O., Parfenova, V. & Belykh, O. Epilithic biofilms in lake baikal: screening and diversity of PKS and NRPS genes in the genomes of heterotrophic bacteria. Pol. J. Microbiol. 67, 501–516 (2018).

    Google Scholar 

46. Aleti, G., Sessitsch, A. & Brader, G. Genome mining: Prediction of lipopeptides and polyketides from Bacillus and related Firmicutes. Comput. Struct. Biotechnol. J. 13, 192–203 (2015).

    Google Scholar 

47. Tomaseto, A. A., Alpiste, M. C., de Castro Nassar, A. F. & Lanza Destefano, S. A. Antibacterial activity of phytopathogenic Streptomyces strains against bacteria associated to clinical diseases. Arq. Inst. Biol. Sao Paulo 87, e0142020 (2020).

    Google Scholar 

48. Olishevska, S., Nickzad, A. & Deziel, E. Bacillus and Paenibacillus secreted polyketides and peptides involved in controlling human and plant pathogens. Appl. Microbiol. Biotechnol. 103, 1189–1215 (2019).

    Google Scholar 

49. Jousset, A. & Bonkowski, M. The model predator Acanthamoeba castellanii induces the production of 2,4, DAPG by the biocontrol strain Pseudomonas fluorescens Q2-87. Soil Biol. Biochem. 42, 1647–1649 (2010).

    Google Scholar 

50. Chakraborty, S. & Warcup, J. H. Populations of mycophagous and other amoebae in take-all suppressive and non-suppressive soils. Soil Biol. Biochem. 16, 197–199 (1984).

    Google Scholar 

51. Loznik, B. & Oosterkamp, P. J. Fertilizer Comprising Bacteria and Protozoa (2015).

52. Komaki, H., Hosoyama, A., Ichikawa, N. & Igarashi, Y. Draft genome sequence of marine-derived Bacillus subtilis TP-B0611, a producer of Bacilosarcins and Amicoumacins. Genome Announc 4, e01134–16 (2016).

    Google Scholar 

53. Guo, S. et al. Predatory protists reduce bacteria wilt disease incidence in tomato plants. Nat. Commun. 15, 829 (2024).

    Google Scholar 

54. Shi, Y. et al. Copper stress shapes the dynamic behavior of amoebae and their associated bacteria. ISME J. 18, wrae100 (2024).

    Google Scholar 

55. Shu, L., Zhang, B., Queller, D. C. & Strassmann, J. E. Burkholderia bacteria use chemotaxis to find social amoeba Dictyostelium discoideum hosts. ISME J. 12, 1977–1993 (2018).

    Google Scholar 

56. Thomas, V., Herrera-Rimann, K., Blanc, D. S. & Greub, G. Biodiversity of amoebae and amoeba-resisting bacteria in a hospital water network. Appl. Environ. Microbiol. 72, 2428–2438 (2006).

    Google Scholar 

57. Gao, Z. Soil Protists: From Traits To Ecological Functions https://doi.org/10.33540/391.(2020).

58. Koji, M., Ryozo, I., Mutsunori, H. & Kazuhiro, T. Quantification of Bacillus species in a wastewater treatment system by the molecular analyses. Biotechnol. Bioprocess Eng. 9, 482–489 (2004).

    Google Scholar 

59. Tao, C., Li, R. & Xiong, W. Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 8, 137 (2020).

    Google Scholar 

60. Schönfeld, J., Heuer, H., Van Elsas, J. D. & Smalla, K. Specific and sensitive detection of Ralstonia solanacearum in soil on the basis of PCR amplification of fliC fragments. Appl. Environ. Microbiol. 69, 7248–7256 (2003).

    Google Scholar 

61. Schirmer, A. et al. Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl. Environ. Microbiol. 71, 4840–4849 (2005).

    Google Scholar 

62. 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. Microb. Ecol. 49, 10–24 (2005).

    Google Scholar 

63. Zhao, M. et al. Microflora that harbor the NRPS gene are responsible for Fusarium wilt disease-suppressive soil. Appl. Soil Ecol. 132, 83–90 (2018).

    Google Scholar 

64. Xiong, W. et al. A global overview of the trophic structure within microbiomes across ecosystems. Environ. Int. 151, 106438 (2021).

    Google Scholar 

65. Bass, D. 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. 18, 1604–1619 (2016).

    Google Scholar 

66. Guillou, 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. 41, D597–D604 (2013).

    Google Scholar 

67. Li, R. et al. Tomato bacterial wilt disease outbreaks are accompanied by an increase in soil antibiotic resistance. Environ. Int. 190, 108896 (2024).

    Google Scholar 

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