Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Inhibition of Verticillium Wilt in Cotton through the Application of Pseudomonas aeruginosa ZL6 Derived from Fermentation Residue of Kitchen Waste

  • Qiuhong Niu (College of Life Science and Agricultural Engineering, Nanyang Normal University) ;
  • Shengwei Lei (College of Life Science and Agricultural Engineering, Nanyang Normal University) ;
  • Guo Zhang (College of Agriculture and Engineering, Nanyang Vocational College of Agriculture) ;
  • Guohan Wu (College of Life Science and Agricultural Engineering, Nanyang Normal University) ;
  • Zhuo Tian (College of Life Science and Agricultural Engineering, Nanyang Normal University) ;
  • Keyan Chen (College of Life Science and Agricultural Engineering, Nanyang Normal University) ;
  • Lin Zhang (College of Life Science and Agricultural Engineering, Nanyang Normal University)
  • Received : 2024.01.29
  • Accepted : 2024.03.25
  • Published : 2024.05.28
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Abstract

To isolate and analyze bacteria with Verticillium wilt-resistant properties from the fermentation residue of kitchen wastes, as well as explore their potential for new applications of the residue. A total of six bacterial strains exhibiting Verticillium wilt-resistant capabilities were isolated from the biogas residue of kitchen waste fermentation. Using a polyphasic approach, strain ZL6, which displayed the highest antagonistic activity against cotton Verticillium wilt, was identified as belonging to the Pseudomonas aeruginosa. Bioassay results demonstrated that this strain possessed robust antagonistic abilities, effectively inhibiting V. dahliae spore germination and mycelial growth. Furthermore, P. aeruginosa ZL6 exhibited high temperature resistance (42℃), nitrogen fixation, and phosphorus removal activities. Pot experiments revealed that P. aeruginosa ZL6 fermentation broth treatment achieved a 47.72% biological control effect compared to the control group. Through activity tracking and protein mass spectrometry identification, a neutral metalloproteinase (Nml) was hypothesized as the main virulence factor. The mutant strain ZL6ߡNml exhibited a significant reduction in its ability to inhibit cotton Verticillium wilt compared to the strain P. aeruginosa ZL6. While the inhibitory activities could be partially restored by a complementation of nml gene in the mutant strain ZL6CMߡNml. This research provides a theoretical foundation for the future development and application of biogas residue as biocontrol agents against Verticillium wilt and as biological preservatives for agricultural products. Additionally, this study presents a novel approach for mitigating the substantial amount of biogas residue generated from kitchen waste fermentation.

Keywords

Acknowledgement

This work was supported by the National Natural Science Foundation Program of China (3217010010), the Program for Outstanding Youth Science Fund Project of Henan Province (222300420014), Agricultural Biomass Green Conversion Technology University Scientific Innovation Team in Henan Province (24IRTSTHN036), by Special Fund for Doctor in Nanyang Normal University (2022ZX031), and by open subject from National Key Laboratory of cotton biological breeding and comprehensive utilization (CB2023A11).

References

  1. Ye Y, Ngo HH, Guo W, Liu Y, Chang SW, Nguyen DD, et al. 2018. A critical review on ammonium recovery from wastewater for sustainable wastewater management. Bioresour. Technol. 268: 749-758. https://doi.org/10.1016/j.biortech.2018.07.111
  2. Li D, Sun M, Xu J, Gong T, Ye M, Xiao Y, et al. 2022. Effect of biochar derived from biogas residue on methane production during dry anaerobic fermentation of kitchen waste. Waste Manag. 149: 70-78. https://doi.org/10.1016/j.wasman.2022.06.006
  3. Tursi A. 2019. A review on biomass: importance, chemistry, classification, and conversion. Biofuel Res. J. 6: 962-979. https://doi.org/10.18331/BRJ2019.6.2.3
  4. Cheong JC, Lee JTE, Lim JW, Song S, Tan JKN, Chiam ZY, et al. 2020. Closing the food waste loop: food waste anaerobic digestate as fertilizer for the cultivation of the leafy vegetable, xiao bai cai (Brassica rapa). Sci. Total Environ. 715: 136789.
  5. Zhao Y, Hu K, Yu J, Khan MTA, Cai Y, Zhao X, et al. 2023. Biogas residues improved microbial diversity and disease suppression function under extent indigenous soil microbial biomass. Life (Basel) 13: 774.
  6. Fu SF, Wang DH, Xie Z, Zou H, Zheng Y. 2022. Producing insect protein from food waste digestate via black soldier fly larvae cultivation: a promising choice for digestate disposal. Sci. Total Environ. 830: 154654.
  7. Owens J, Hao X, Thomas BW, Stoeckli J, Soden C, Acharya S, et al. 2021. Effects of 3-nitrooxypropanol manure fertilizer on soil health and hydraulic properties. J. Environ. Qual. 50: 1452-1463. https://doi.org/10.1002/jeq2.20276
  8. Gong Q, Yang Z, Wang X, Butt HI, Chen E, He S, et al. 2017. Salicylic acid-related cotton (Gossypium arboreum) ribosomal protein GaRPL18 contributes to resistance to Verticillium dahliae. BMC Plant Biol. 17: 59.
  9. Huang CL, Zhang ZF, Zhang XJ, Jiang L, Hua XD, Ye JL, et al. 2023. A novel intelligent system for dynamic observation of cotton Verticillium Wilt. Plant Phenomics 5: 0013.
  10. Deketelaere S, Tyvaert L, Franca SC, Hofte M. 2017. Desirable traits of a good biocontrol agent against Verticillium wilt. Front. Microbiol. 8: 1186.
  11. Dadd-Daigle P, Kirkby K, Roy Chowdhury P, Labbate M, Chapman TA. 2021. The Verticillium wilt problem in Australian cotton. Australasian Plant Pathol. 50: 129-135. https://doi.org/10.1007/s13313-020-00756-y
  12. Shaban M, Miao Y, Ullah A, Khan AQ, Menghwar H, Khan AH, et al. 2018. Physiological and molecular mechanism of defense in cotton against Verticillium dahliae. Plant Physiol. Biochem. 125: 193-204. https://doi.org/10.1016/j.plaphy.2018.02.011
  13. Tao X, Zhang H, Gao M, Li M, Zhao T, Guan X. 2020. Pseudomonas species isolated via high-throughput screening significantly protect cotton plants against Verticillium wilt. AMB Express 10: 193.
  14. Song R, Li J, Xie C, Jian W, Yang X. 2020. An overview of the molecular genetics of plant resistance to the Verticillium wilt pathogen Verticillium dahliae. Int. J. Mol. Sci. 21: 1120.
  15. Li S, Zhang N, Zhang Z, Luo J, Shen B, Zhang R, et al. 2013. Antagonist Bacillus subtilis HJ5 controls Verticillium wilt of cotton by root colonization and biofilm formation. Biol. Fertility Soils 49: 295-303. https://doi.org/10.1007/s00374-012-0718-x
  16. Jin L, Yang L, Li W, Xu D, Yang N, Li G, Wan P. 2021. Diversity and biocontrol potential of culturable endophytic fungi in cotton. Front. Microbiol. 12: 698930.
  17. Zhang Y, Yang N, Zhao L, Zhu H, Tang C. 2020a. Transcriptome analysis reveals the defense mechanism of cotton against Verticillium dahliae in the presence of the biocontrol fungus Chaetomium globosum CEF-082. BMC Plant Biol. 20: 89.
  18. Zhang L, Li W, Tao Y, Zhao S, Yao L, Cai Y, et al. 2019. Overexpression of the key virulence factor 1,3-1,4-β-d-glucanase in the endophytic bacterium Bacillus halotolerans Y6 to improve Verticillium resistance in cotton. J. Agric. Food Chem. 67: 6828-6836. https://doi.org/10.1021/acs.jafc.9b00728
  19. Zhang L, Tao Y, Zhao S, Yin X, Chen J, Wang M, et al. 2020b. A novel peroxiredoxin from the antagonistic endophytic bacterium Enterobacter sp. V1 contributes to cotton resistance against Verticillium dahliae. Plant Soil 454: 395-409. https://doi.org/10.1007/s11104-020-04661-7
  20. Wang B, Huang B, Chen J, Li W, Yang L, Yao L, et al. 2019. Whole-genome analysis of the colonization-resistant bacterium Phytobacter sp. SCO41T  isolated from Bacillus nematocida B16-fed adult Caenorhabditis elegans. Mol. Biol. Rep. 46: 1563-1575. https://doi.org/10.1007/s11033-018-04574-w
  21. Niu Q, Liu S, Yin M, Lei S, Rezzonico F, Zhang L. 2022. Phytobacter diazotrophicus from Intestine of Caenorhabditis elegans confers colonization-resistance against Bacillus nematocida using flagellin (FliC) as an inhibition factor. Pathogens 11: 82.
  22. Li N, Peng Q, Yao L, He Q, Qiu J, Cao H, et al. 2020. Roles of the gentisate 1,2-Dioxygenases DsmD and GtdA in the catabolism of the herbicide dicamba in Rhizorhabdus dicambivorans Ndbn-20. J. Agric. Food Chem. 68: 9287-9298. https://doi.org/10.1021/acs.jafc.0c01523
  23. Li DG, Liu CM, Luo R, Sadakane K, Lam TW. 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31: 1674-1676. https://doi.org/10.1093/bioinformatics/btv033
  24. Li R, Li Y, Kristiansen K, Wang J. 2008. SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713-714. https://doi.org/10.1093/bioinformatics/btn025
  25. Noguchi H, Park J, Takagi T. 2006. MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res. 34: 5623-5630. https://doi.org/10.1093/nar/gkl723
  26. Arthurson V. 2009. Closing the global energy and nutrient cycles through application of biogas residue to agricultural land-potential benefits and drawbacks. Energies 2: 226-242. https://doi.org/10.3390/en20200226
  27. Tang GL, Xu KF, Wang C, Sun ZJ, Huang J, Liu GQ. 2008. Biohydrogen production by anaerobic fermentation from manure wastewater. Huanjing kexue. 29: 1621-1625
  28. Adediran JA, Baets ND, Mnkeni PNS, Kiekens L, Muyima NYO, Thys A. 2003. Organic waste materials for soil fertility improvement in the border region of the eastern cape, South Africa. Biol. Agric. Hortic. 20: 283-300 https://doi.org/10.1080/01448765.2003.9754974
  29. Odlare M, Pell M, Svensson K. 2008. Changes in soil chemical and microbiological properties during 4 years of application of various organic residues. Waste Manage. 28: 1246-1253. https://doi.org/10.1016/j.wasman.2007.06.005
  30. Wei F, Zhang Y, Shi Y, Feng H, Zhao L, Feng Z, et al. 2019a. Evaluation of the biocontrol potential of endophytic fungus Fusarium solani CEF559 against Verticillium dahliae in cotton plant. BioMed Res. Int. 2019: 3187943.
  31. Wei F, Fan R, Dong H, Shang W, Xu X, Zhu H, et al. 2015. Threshold microsclerotial inoculum for cotton Verticillium Wilt determined through wet-sieving and real-time quantitative PCR. Phytopathology 105: 220-229. https://doi.org/10.1094/PHYTO-05-14-0139-R
  32. Wei F, Zhao L, Xu X, Feng H, Shi Y, Deakin G, et al. 2019b. Cultivar-Dependent variation of the cotton rhizosphere and endosphere microbiome under field conditions. Front. Plant Sci. 10: 1659.
  33. Egamberdieva D. 2016. Bacillus spp.: A Potential Plant Growth Stimulator and Biocontrol Agent Under Hostile Environmental Conditions. Bacilli and Agrobiotechnol. pp. 91-111.
  34. Sullivan RF, Holtman MA, Zylstra GJ, White JF, Jr., Kobayashi DY. 2003. Taxonomic positioning of two biological control agents for plant diseases as Lysobacter enzymogenes based on phylogenetic analysis of 16S rDNA, fatty acid composition and phenotypic characteristics. J. Appl. Microbiol. 94: 1079-1086. https://doi.org/10.1046/j.1365-2672.2003.01932.x
  35. Niu G, Chater KF, Tian Y, Zhang J, Tan H. 2016. Specialized metabolites regulating antibiotic biosynthesis in Streptomyces spp. FEMS Microbiol. Rev. 40: 554-573. https://doi.org/10.1093/femsre/fuw012
  36. Prieto P, Navarro-Raya C, Valverde-Corredor A, Amyotte SG, Dobinson KF, Mercado-Blanco J. 2009. Colonization process of olive tissues by Verticillium dahliae and its in planta interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microb. Biotechnol. 2: 499-511. https://doi.org/10.1111/j.1751-7915.2009.00105.x
  37. de Kievit TR, Iglewski BH. 2000. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68: 4839-4849. https://doi.org/10.1128/IAI.68.9.4839-4849.2000
  38. Soares A, Alexandre K, Etienne M. 2020. Tolerance and persistence of Pseudomonas aeruginosa in biofilms exposed to antibiotics: molecular mechanisms, antibiotic strategies and therapeutic perspectives. Front. Microbiol. 11: 2057.
  39. Wang X, Zhou X, Cai Z, Guo L, Chen X, Chen X, et al. 2021. A biocontrol strain of Pseudomonas aeruginosa CQ-40 promote growth and control Botrytis cinerea in tomato. Pathogens 10: 22.
  40. Harting R, Nagel A, Nesemann K, Hofer AM, Bastakis E, Kusch H, et al.2021. Pseudomonas strains induce transcriptional and morphological changes and reduce root colonization of Verticillium spp. J. Front. Microbiol. 12: 652468.
  41. Gambello MJ, Iglewski BH. 1991. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J. Bacteriol. 173: 3000-3009. https://doi.org/10.1128/jb.173.9.3000-3009.1991
  42. Everett MJ, Davies DT, Leiris S, Sprynski N, Llanos A, Castandet JM, et al. 2023. Chemical optimization of selective Pseudomonas aeruginosa LasB elastase inhibitors and their impact on LasB-mediated activation of IL-1β in cellular and animal infection models. ACS Infect. Dis. 9: 270-282.
  43. Fujimoto A, Augusto F, Fill TP, Moretto RK, Kupper KC. 2022. Biocontrol of Phyllosticta citricarpa by Bacillus spp.: biological and chemical aspects of the microbial interaction. World J. Microbiol. Biotechnol. 38: 53.
  44. Ernst G, Muller A, Gohler, H, Emmerling C. 2008. C and N turnover of fermented residues from biogas plants in soil in the presence of three different earthworm species (Lumbricus terrestris, Aporrectodea longa, Aporrectodea caliginosa). Soil Biol. Biochem. 40: 1413-1420.  https://doi.org/10.1016/j.soilbio.2007.12.026