ISSN 2074-9414 (Print),
ISSN 2313-1748 (Online)

Antagonistic Activity of Extremophilic Bacteria Against Phytopathogens in Agricultural Crops

Abstract
Wheat is a vital agricultural crop whose phytopathogens include fungi of the genera Fusarium and Alternaria. Synthetic pesticides, which are used to combat them, have a negative impact on the environment. Therefore, there is a need for developing safe and effective biopesticides. We aimed to create a consortium of extremophilic microorganisms isolated from natural sources to protect wheat from the diseases caused by Alternaria and Fusarium fungi.
Ten isolates of extremophilic microorganisms were tested for their antimicrobial activity against Escherichia coli and their antagonistic activity against phytopathogens. Based on the results, we developed microbial consortia and evaluated their effectiveness in protecting wheat from phytopathogens.
Five of the strains under study showed the highest activity, three of which were biocompatible, namely Leclercia sp., Sphingomonas paucimobilis, and Lactobacillus plantarum. Four consortia were created from these microorganisms, of which consortium B (with a 2:1:1 ratio of the strains, respectively) proved the most effective. In particular, it increased the area free from the phytopathogen by 4.2% compared to the average values of its individual microorganisms. Also, the consortium had a phytostimulating effect on wheat seedlings (germination of 73.2–99.6%) and protected the seeds infected with phytopathogens from morphometric changes.
The resulting consortium can be used as a biopesticide since it is highly effective in protecting wheat from Alternaria and Fusarium pathogens.
Keywords
Triticum aestivum L., agricultural productivity, phytopathogens, biopesticides, extremophilic bacteria, consortium of microorganisms, environmental safety
FUNDING
This study was part of the state assignment entitled “Basic research on the development of biopesticides from extremophilic and endophytic microorganisms to help agricultural crops overcome abiotic and biotic stress in Kemerovo Oblast – Kuzbass” (code FZSR-2023-0003).
REFERENCES
  1. Sabouri H, Kazerani B, Fallahi HA, Dehghan MA, Alegh SM, Dadras AR, et al. Association analysis of yellow rust, fusarium head blight, tan spot, powdery mildew, and brown rust horizontal resistance genes in wheat. Physiological and Molecular Plant Pathology. 2022;118. https://doi.org/10.1016/j.pmpp.2022.101808
  2. Drakopoulos D, Kägi A, Six J, Zorn A, Wettstein FE, Bucheli TD, et al. The agronomic and economic viability of innovative cropping systems to reduce Fusarium head blight and related mycotoxins in wheat. Agricultural Systems. 2021;192. https://doi.org/10.1016/j.agsy.2021.103198
  3. Shude SPN, Mbili NC, Yobo KS. Epiphytic yeasts as potential antagonists against Fusarium head blight of wheat (Triticum aestivum L.) caused by Fusarium graminearum sensu stricto. Journal of the Saudi Society of Agricultural Sciences. 2022;21(6):404–411. https://doi.org/10.1016/j.jssas.2021.11.001
  4. Zhang D, Chen G, Zhang H, Jin N, Gu C, Weng S, et al. Integration of spectroscopy and image for identifying fusarium damage in wheat kernels. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy. 2020;236. https://doi.org/10.1016/j.saa.2020.118344
  5. Martínez M, Biganzoli F, Arata A, Dinolfo MI, Rojas D, Cristos D, et al. Warm nights increase Fusarium Head Blight negative impact on barley and wheat grains. Agricultural and Forest Meteorology. 2022;318. https://doi.org/10.1016/j.agrformet.2022.108909
  6. Gagkaeva TYu, Gavrilova OP, Orina AS. First detection of Fusarium globosum in small grain cereals on Ural and Siberian territory. Plant Protection News. 2019;99(1):10–18. (In Russ.). https://doi.org/10.31993/2308-6459-2019-1(99)-10-18
  7. Asan-Ozusaglam M, Celik I. White pitahaya as a natural additive: potential usage in cosmetic industry. Foods and Raw Materials. 2023;11(1):57–63. https://doi.org/10.21603/2308-4057-2023-1-552
  8. Wegulo SN, Baenziger PS, Nopsa JH, Bockus WW, Hallen-Adams H. Management of Fusarium head blight of wheat and barley. Crop Protection. 2015;73:100–107. https://doi.org/10.1016/j.cropro.2015.02.025
  9. da Cruz Cabral L, Delgado J, Patriarca A, Rodríguez A. Differential response to synthetic and natural antifungals by Alternaria tenuissima in wheat simulating media: Growth, mycotoxin production and expression of a gene related to cell wall integrity. International Journal of Food Microbiology. 2019;292:48–55. https://doi.org/10.1016/j.ijfoodmicro.2018.12.005
  10. Somma S, Amatulli MT, Masiello M, Moretti A, Logrieco AF. Alternaria species associated to wheat black point identified through a multilocus sequence approach. International Journal of Food Microbiology. 2019;293:34–43. https://doi.org/10.1016/j.ijfoodmicro.2019.01.001
  11. Guler GO, Cakmak YS, Dagli Z, Aktumsek A, Ozparlak H. Organochlorine pesticide residues in wheat from Konya region, Turkey. Food and Chemical Toxicology. 2010;48(5):1218–1221. https://doi.org/10.1016/j.fct.2010.02.013
  12. Syed-Ab-Rahman SF, Singh E, Pieterse CMJ, Schenk PM. Emerging microbial biocontrol strategies for plant pathogens. Plant Science. 2018;262:102–111. https://doi.org/10.1016/j.plantsci.2017.11.012
  13. Choe SG, Maeng HR, Pak SJ, U SN. Production of Bacillus thuringiensis biopesticide using penicillin fermentation waste matter and application in agriculture. Journal of Natural Pesticide Research. 2022;2. https://doi.org/10.1016/j.napere.2022.100012
  14. Ajayi FF, Ogori AF, Orede VO, Peter E. Synergistic effect of Balanites aegyptiaca essential oil and storage materials on cowpea seeds. Foods and Raw Materials. 2022;10(2):353–364. https://doi.org/10.21603/2308-4057-2022-2-545
  15. Lu C, Yang Z, Liu J, Liao Q, Ling W, Waigi MG, et al. Chlorpyrifos inhibits nitrogen fixation in rice-vegetated soil containing Pseudomonas stutzeri A1501. Chemosphere. 2020;256. https://doi.org/10.1016/j.chemosphere.2020.127098
  16. Walder F, Schmid MW, Riedo J, Valzano-Held AY, Banerjee S, Büchi L, et al. Soil microbiome signatures are associated with pesticide residues in arable landscapes. Soil Biology and Biochemistry. 2022;174. https://doi.org/10.1016/j.soilbio.2022.108830
  17. Tao Y, Jia C, Jing J, Zhang J, Yu P, He M, et al. Occurrence and dietary risk assessment of 37 pesticides in wheat fields in the suburbs of Beijing, China. Food Chemistry. 2021;350. https://doi.org/10.1016/j.foodchem.2021.129245
  18. Mrid RB, Benmrid B, Hafsa J, Boukcim H, Sobeh M, Yasri A. Secondary metabolites as biostimulant and bioprotectant agents: A review. Science of the Total Environment. 2021;777. https://doi.org/10.1016/j.scitotenv.2021.146204
  19. Nysanth NS, Divya S, Nair CB, Anju AB, Praveena R, Anith KN. Biological control of foot rot (Phytophthora capsici Leonian) disease in black pepper (Piper nigrum L.) with rhizospheric microorganisms. Rhizosphere. 2022;23. https://doi.org/10.1016/j.rhisph.2022.100578
  20. Santos AP, Muratore LN, Solé-Gil A, Farías ME, Ferrando A, Blázquez MA, et al. Extremophilic bacteria restrict the growth of Macrophomina phaseolina by combined secretion of polyamines and lytic enzymes. Biotechnology Reports. 2021;32. https://doi.org/10.1016/j.btre.2021.e00674
  21. Giudice AL, Fani R. Antimicrobial potential of cold-adapted bacteria and fungi from Polar Regions. In: Rampelotto PH, editor. Biotechnology of extremophiles: Advances and challenges. Cham: Springer; 2016. pp. 83–115. https://doi.org/10.1007/978-3-319-13521-2_3
  22. Liu K, Ding H, Yu Y, Chen B. A cold-adapted chitinase-producing bacterium from Antarctica and its potential in biocontrol of plant pathogenic fungi. Marine Drugs. 2019;17(12). https://doi.org/10.3390/md17120695
  23. Milentyeva IS, Fotina NV, Zharko MYu, Proskuryakova LA. Microbial treatment and oxidative stress in agricultural plants. Food Processing: Techniques and Technology. 2022;52(4):750–761. (In Russ.). https://doi.org/10.21603/2074-9414-2022-4-2403
  24. Voitenkova EV, Matveeva ZN, Makarova MA, Egorova SA, Zabrovskaia AV, Suzhaeva LV, et al. Difficulties in identification of Comamonas kerstersii strains isolated from intestinal microbiota of residents of Republic of Guinea and Russian Federation. Russian Journal of Infection and Immunity. 2018;8(2):164–168. https://doi.org/10.15789/2220-7619-2018-2-163-168
  25. Khalil T, Oklab MK, Al-Qahtanic WH, Alia F, Zahrad M, Shakeela Q, et al. Tracing probiotic producing bacterial species from gut of buffalo (Bubalus bubalis), South-East-Asia. Brazilian Journal of Biology. 2022;84. https://doi.org/10.1590/1519-6984.259094
  26. Sornakili A, Thankappan S, Sridharan AP, Nithya P, Uthandi S. Antagonistic fungal endophytes and their metabolite-mediated interactions against phytopathogens in rice. Physiological and Molecular Plant Pathology. 2020;112. https://doi.org/10.1016/j.pmpp.2020.101525
  27. Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, et al. Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: A review. Ecotoxicology and Environmental Safety. 2016;126:111–121. https://doi.org/10.1016/j.ecoenv.2015.12.023
  28. Goswami M, Deka S. Isolation of a novel rhizobacteria having multiple plant growth promoting traits and antifungal activity against certain phytopathogens. Microbiological Research. 2020;240. https://doi.org/10.1016/j.micres.2020.126516
  29. Gorbunov MYu, Mrachkovskaya AN. The use of growth stimulants to increase the commercial yield of petunia seedlings. Trends in the Development of Science and Education. 2018;(35–4):60–62. (In Russ.). https://doi.org/10.18411/lj-28-02-2018-70
  30. Asyakina LK, Dyshlyuk LS, Prosekov AYu. Reclamation of post-technological landscapes: International experience. Food Processing: Techniques and Technology. 2021;51(4):805–818. (In Russ.). https://doi.org/10.21603/2074-9414-2021-4-805-818
  31. Panebianco S, Lombardo MF, Anzalone A, Musumarra A, Pellegriti MG, Catara V, et al. Epiphytic and endophytic microorganisms associated to different cultivar of tomato fruits in greenhouse environment and characterization of beneficial bacterial strains for the control of post-harvest tomato pathogens. International Journal of Food Microbiology. 2022;379. https://doi.org/10.1016/j.ijfoodmicro.2022.109861
  32. Xie Z, Li M, Wang D, Wang F, Shen H, Sun G, et al. Biocontrol efficacy of Bacillus siamensis LZ88 against brown spot disease of tobacco caused by Alternaria alternate. Biological Control. 2021;154. https://doi.org/10.1016/j.biocontrol.2020.104508
  33. Gupta S, Didwania N, Singh D. Biological control of mustard blight caused by Alternaria brassicae using plant growth promoting bacteria. Current Plant Biology. 2020;23. https://doi.org/10.1016/j.cpb.2020.100166
  34. Jankiewicz U, Brzezinska MS, Saks E. Identification and characterization of a chitinase of Stenotrophomonas maltophilia, a bacterium that is antagonistic towards fungal phytopathogens. Journal of Bioscience and Bioengineering. 2012;113(1):30–35. https://doi.org/10.1016/j.jbiosc.2011.08.023
  35. Chavéz-Díaz IF, Cruz-Cárdenas CI, Sandoval-Cancino G, Calvillo-Aguilar FF, Ruíz-Ramírez S, Blanco-Camarillo M, et al. Seedling growth promotion and potential biocontrol against phytopathogenic Fusarium by native rhizospheric Pseudomonas spp. strains from Amarillo Zamorano maize landrace. Rhizosphere. 2022;24. https://doi.org/10.1016/j.rhisph.2022.100601
  36. Baffoni L, Gaggia F, Dalanaj N, Prodi A, Nipoti P, Pisi A, et al. Microbial inoculants for the biocontrol of Fusarium spp. in durum wheat. BMC Microbiology. 2015;15. https://doi.org/10.1186/s12866-015-0573-7
  37. Wang L-Y, Xie Y-S, Cui Y-Y, Xu J, He W, Chen H-G, et al. Conjunctively screening of biocontrol agents (BCAs) against fusarium root rot and fusarium head blight caused by Fusarium graminearum. Microbiological Research. 2015;177:34–42. https://doi.org/10.1016/j.micres.2015.05.005
How to quote?
Asyakina LK, Serazetdinova YuR, Frolova AS, Fotina NV, Neverova OA, Petrov AN. Antagonistic Activity of Extremophilic Bacteria Against Phytopathogens in Agricultural Crops. Food Processing: Techniques and Technology. 2023;53(3):565–575. https://doi.org/10.21603/2074-9414-2023-3-2457 
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