Kemerovo, Russian Federation
Kemerovo, Russian Federation
Novosibirsk, Russian Federation
Kemerovo, Russian Federation
Kemerovo, Russian Federation
Cereals are crucial to food security, but intensive agrochemical farming depletes soil ecosystems and increases environmental risks. In this regard, microbial biological control agents hold great promise. The bacterial genus Pantoea stimulates plant growth and suppresses phytopathogens. However, its practical application requires a molecular genetic assessment of its biosafety and metabolic potential. A genome-wide bioinformatic analysis of the biosynthesis of Pantoea pleuroti B-14756 secondary metabolites was conducted to assess its genetic and metabolic potential as a biocontrol agent for phytopathogens of cereal crops. The strain of P. pleuroti B-14756 was obtained from the National Bioresource Center at the Kurchatov Institute (Moscow, Russia). Genome-wide sequencing was performed on the MGIseq-2000 and Polyseq One platforms. The genome was assembled de novo, polished, and annotated using the following bioinformatics tools: Flye, Raven, Trycycler, Medaka, Polypolish, POLCA, BUSCO, Bakta, and antiSMASH. The sequencing and assembly yielded the P. pleuroti B-14756 genome with a size of 4,735,406 bp and a GC content of 53%. The genome annotation revealed 4,416 coding sequences, seven rRNA clusters, and 78 tRNAs. The antiSMASH analysis revealed nine clusters of secondary metabolite biosynthesis, including clusters associated with the synthesis of aerobactin, desferrioxamine E, and carotenoids. Aerobactin and desferrioxamine E demonstrate the ability to bind, chelate, and subsequently import iron ions, while carotenoids perform an antioxidant function, protecting the cell from reactive oxygen species under stressful conditions. P. pleuroti B-14756 was proved to possess biosynthetic clusters of secondary metabolites (including NRPS, RiPP, phosphonate, and terpene pathways). This finding confirms the pronounced antagonistic potential of the strain and its promising application in the biological control of phytopathogens.
Pantoea pleuroti, biological control, secondary metabolites, whole-genome sequencing, bioinformatics analysis, siderophores, antagonistic activity
1. Shah F, Wu W. Soil and crop management strategies to ensure higher crop productivity within sustainable environments. Sustainability. 2019;11(5):1485. https://doi.org/10.3390/su11051485
2. Prosekov AYu. Food security and globalization. Foods and Raw Materials. 2026;14(2):247–251. https://doi.org/10.21603/2308-4057-2026-2-679
3. Giraldo P, Benavente E, Manzano-Agugliaro F, Gimenez E. Worldwide research trends on wheat and barley: A bibliometric comparative analysis. Agronomy. 2019;9(7):352. https: //doi.org/10.3390/agronomy9070352
4. Shewry PR, Hey SJ. The contribution of wheat to human diet and health. Food and Energy Security. 2015;4(3):178–202. https://doi.org/10.1002/fes3.64
5. Fotina NV, Serazetdinova YuR, Kolpakova DE, Asyakina LK, Atuchin VV, et al. Enhancement of wheat growth by plant growth-stimulating bacteria during phytopathogenic inhibition. Biocatalysis and Agricultural Biotechnology. 2024;60:103294. https://doi.org/10.1016/j.bcab.2024.103294
6. Myers SS, Smith MR, Guth S, Golden CD, Vaitla B, et al. Climate change and global food systems: Potential impacts on food security and undernutrition. The Annual Review of Public Health. 2017;38:259–277. https://doi.org/10.1146/annurevpublhealth-031816-044356
7. Said M. An overview of impact of agrochemicals on human health and natural environment. Scientific Research Communications. 2023;3(2). https://doi.org/10.52460/src.2023.009
8. Serazetdinova YuR, Chekushkina DYu, Borodina EE, Kolpakova DE, Minina VI, et al. Synergistic interaction between Azotobacter and Pseudomonas bacteria in a growth-stimulating consortium. Foods and Raw Materials. 2025;13(2):376–393. https://doi.org/10.21603/2308-4057-2025-2-651
9. Carvalho FP. Pesticides, environment, and food safety. Food and Energy Security. 2017;6(2):48–60 https://doi.org/10.1002/fes3.108
10. Gomiero T. Soil degradation, land scarcity and food security: Reviewing a complex challenge. Sustainability. 2016;8(3):281. https://doi.org/10.3390/su8030281
11. Faskhutdinova ER, Fotina NV, Neverova OA, Golubtsova YuV, Mudgal G, et al. Extremophilic bacteria as biofertilizer for agricultural wheat. Foods and Raw Materials. 2024;12(2):348 –360. https://doi.org/https://doi.org/10.21603/2308-4057-2024-2-613
12. Țopa D-C, Căpșună S, Calistru A-E, Ailincăi C. Sustainable practices for enhancing soil health and crop quality in modern agriculture: A review. Agriculture. 2025;15(9):998. h ttps://doi.org/10.3390/agriculture15090998
13. Elnahal ASM, El-Saadony MT, Saad AM, Desoky EM, El-Tahan AM, et al. The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: A review. European Journal of Plant Pathology. 2022;162:759–792. https://doi.org/10.1007/s10658-021-02393-7
14. Asyakina LK, Mudgal G, Tikhonov SL, Larichev TA, Fotina NV, et al. Study of the potential of natural microbiota of spring soft wheat to increase yield. Achievements of Science and Technology of Agriculture. 2023;37(11):12–17. (In Russ.) https://doi.org/10.53859/02352451_202 3_37_11_12
15. Asyakina LK, Isachkova OA, Kolpakova DE, Borodina EE, Boger VYu, et al. The effect of a microbial consortium on spring barley growth and development in The Kemerovo Region, Kuzbass. 2024;16(1):101–112. (In Russ.) https://doi.org/10.31367/2079-8725-2024-90-1-104-112
16. Faskhutdinova ER, Bogacheva NN, Borodina EE, Pozdnyakova AV, Luzyanin SL. Effect of endophytic microorganisms on growth rate of crops. Food Processing: Techniques and Technology. 2024;54(4):820–836. (In Russ.) https://doi.org/10.21603/2074- 9414-2024-4-2548
17. Serazetdinova YuR, Borodina EE, Fotina NV, Naik A, Mudgal G, et al. Rhizobia as complex biofertilizers for wheat: Biological nitrogen fixation and plant growth promotion. Foods and Raw Materials. 2026;14(1):214–227. https://doi.org/10.21603/2308-4057-2026-1-669
18. Serazetdinova YuR, Kolpakova DE, Borodina EE, Asyakina LK, Prosekov AYu, et al. Sinorhizobium and sustainable farming: Genomic approaches. Foods and Raw Materials. 2027;15(1):238–256. https://doi.org/10.21603/2308-4057-2027-1-705
19. Duchateau S, Crouzet J, Dorey S, Aziz A. The plant-associated Pantoea spp. as biocontrol agents: Mechanisms and diversity of bacteria-produced metabolites as a prospective tool for plant protection. Biological Control. 2024;188:105441.https://doi.org/10.1016/j.biocontrol.2024.105441
20. Serazetdinova YuR, Kolpakova DE, Borodina EE, Pleshivtsev II, Gordienko AV, et al. Biological control of cereal crop diseases using bacteria of the genus Pantoea. Biosfera. 2025;17(3):153–174. (In Russ.) https://doi.org/10.24855/biosfera.v17i3.1006
21. Ercole TG, Liviero R, Terra LA, Zocolo GJ, Klepa MS, et al. Integrated genome mining and phytohormone profiling of six plant growth-promoting elite bacterial strains. Archives of Microbiology. 2026;208(3):152. https://doi.org/10.1007/s00203-025-04712-6
22. Walterson AM, Stavrinides J. Pantoea: Insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiology Reviews. 2015;39(6):968–984. https://doi.org/10.1093/femsre/fuv027
23. Timofeeva AM, Galyamova MR, Sedykh SE. Plant growth-promoting soil bacteria: Nitrogen fixation, phosphate solubilization, siderophore production, and other biological activities. Plants. 2023;12(24):4074. https://doi.org/10.3390/plants12244074
24. Suleimanova AD, Sokolnikova LV, Egorova EA, Berkutova ES, Pudova DS, et al. Antifungal activity of siderophore isolated from Pantoea brenneri against Fusarium oxysporum. Russian Journal of Plant Physiology. 2023;70(8):199. https://doi.org/10.1134/s1021443723602744
25. Şimşek Ö, Isak MA, Dönmez D, Şekerci AD, İzgü T, et al. Advanced biotechnological interventions in mitigating drought stress in plants. Plants. 2024;13(5):717. https://doi.org/10.3390/plants13050717
26. Valbuena-Rodríguez JL, Fonseca IR, Buitrago-Yomayusa C, Puentes-S A, Benavides ME. Isolation and characterization of Pantoea ananatis and P. agglomerans in quinoa: P. ananatis as a potential fungal biocontroller and plant growth promoter. International Microbiology. 2025;28(6):1149–1161. https://doi.org/10.1007/s10123-024-00608-5
27. Boro M, Sannyasi S, Chettri D, Verma AK. Microorganisms in biological control strategies to manage microbial plant pathogens: A review. Archives of Microbiology. 2022;204(1 1):666. https://doi.org/10.1007/s00203-022-03279-w
28. Mechan Llontop ME, Hurley K, Tian L, Bernal Galeano VA, Wildschutte H, et al. Exploring rain as source of biological control agents for fire blight on apple. Frontiers in Microbiology. 2020;11:199. https://doi.org/10.3389/fmicb.2020.00199
29. Itkina DL, Suleimanova AD, Sharipova MR. Isolation, purification, and identification of the secretion compound Pantoea brenneri AS3 with fungicidal activity. Applied Biochemistry and Microbiology. 2022;58:456–462. https://doi.org/10.1134/S000368382204007X
30. Melini F, Luziatelli F, Bonini P, Ficca AG, Melini V, et al. Optimization of the growth conditions through response surface methodology and metabolomics for maximizing the auxin production by Pantoea agglomerans C1. Frontiers in Microbiology. 2023;14:1022248. https://doi.org/10.3389/fmicb.2023.1022248
31. Xu S, Liu YX, Cernava T, Wang H, Zhou Y, et al. Fusarium fruiting body microbiome member Pantoea agglomerans inhibits fungal pathogenesis by targeting lipid rafts. Nature Microbiology. 2022;7(6):831–843. https://doi.org/10.1038/s41564-022-01131-x
32. Quartana C, Faddetta T, Anello L, Di Bernardo M, Petralia R, et al. Activity of bacterial seed endophytes of landrace durum wheat for control of Fusarium foot rot. Phytopathologia Mediterranea. 2022;61(1):95–106. https://doi.org/10.36253/phyto-12993
33. Dutkiewicz J, Mackiewicz B, Lemieszek MK, Golec M, Milanowski J. Pantoea agglomerans: A mysterious bacterium of evil and good. Part IV. Beneficial effects. Annals of Agricultural and Environmental Medicine. 2016;23(2):206–222. https://doi.org/10.5604/12321966.1203879
34. López SMY, Pastorino GN, Balatti PA. Volatile organic compounds profile synthesized and released by endophytes of tomato (Solanum lycopersici L.) and their antagonistic role. Archives of Microbiology. 2021;203:1383–1397. https://doi.org/10.1007/s00203-020-02136-y
35. Safara S, Harighi B, Bahramnejad B, Ahmadi S. Antibacterial activity of endophytic bacteria against sugar beet root rot agent by volatile organic compound production and induction of systemic resistance. Frontiers in Microbiology. 2022;13:921762. https://doi.org/10.3389/fmicb.2022.921762
36. Lahlali R, Aksissou W, Lyousfi N, Ezrari S, Blenzar A, et al. Biocontrol activity and putative mechanism of Bacillus amyloliquefaciens (SF14 and SP10), Alcaligenes faecalis ACBC1, and Pantoea agglomerans ACBP1 against brown rot disease of fruit. Microbial Pathogenesis. 2020;139:103914. https://doi.org/10.1016/j.micpath.2019.103914
37. Enya J, Shinohara H, Yoshida S, Tsukiboshi T, Negishi H, et al. Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents. Microbial Ecology. 2007;53:524–436. https://doi.org/10.1007/s00248-006-9085-1
38. Simeya N, Numata S, Nakjima M, Haseba A, Hibi T, et al. Biological control of rice blast by the epiphytic bacterium Erwinia ananas transformed with a chitinolytic enzyme gene from an antagonistic bacterium, Serratia marcescens strain B2. Journal of General Plant Pathology. 2003;69:276–282. https://doi.org/10.1007/s10327-003-0043-1
39. Stromberg KD, Kinkel LL, Leonard KJ. Quantifying the effect of bacterial antagonists on the relationship between phyllosphere population sizes of Xanthomonas translucens pv. translucens and subsequent bacterial leaf streak severity on wheat seedlings. Biological Control. 2004;29(1):58–65. https://doi.org/10.1016/S1049-9644(03)00126-9
40. Tian Y, Lei W, Zhang J, Shen Y, Lu J, et al. Mechanism of Pantoea ananatis in the biocontrol of rice bacterial leaf blight. Frontiers in Microbiology. 2026;17:1722838. https://doi.org/10.3389/fmicb.2026.1722838
41. Sun W, Liu Q, Chen H, Xie X, Zhang Z, et al. Rice phyllospheric Pantoea spp. suppress blast and bacterial blight diseases. Environ Microbiome. 2025;20(1):137. https://doi.org/10.1186/s40793-025-00799-y
42. Borodina EE, Gordienko AV, Pleshivtsev II, Fotina NV, Fedorova AM, et al. New Pantoea strain as antistress agent and growth stimulator in grain growing. Food Processing: Techniques and Technology. 2025;55(4):710–722. (In Russ.) https://doi.org/10.21603/2074-9414-2025-4-2606
43. Naumova NB, Baturina OA, Lokteva AS, Pleshakova VI, Lescheva NA, et al. The effect of dextranal on the gut bacteriobiome of calves. Siberian Journal of Life Sciences and Agriculture. 2023;15(6):197–221. (In Russ.) https://doi.org/10.12731/2658-6649-2023-15-6-956
44. Andreeva IS, Totmenina OD, Kabanov AS, Antonets ME, Bodnev SA, et al. Assessment of the pathogenic potential of microorganisms in atmospheric aerosols of Novosibirsk and its suburbs. Public Health and Life Environment. 2024;32(4):27–36. (In Russ.) https://doi.org/10.3 5627/2219-5238/2024-32-4-27-36
45. Kolmogorov M, Yuan J, Lin Y, Pevzner P. Assembly of long error-prone reads using repeat graphs. Nature Biotechnology. 2019;37:540–546. https://doi.org/10.1038/s41587-019-0072-8
46. Wick RR, Holt KE. Benchmarking of long-read assemblers for prokaryote whole genome sequencing. F1000Research. 2019;8:2138. https://doi.org/10.12688/f1000research.21782.4
47. Wick RR, Judd LM, Cerdeira LT, Hawkey J, Méric G, et al. Trycycler: Consensus long-read assemblies for bacterial genomes. Genome Biology. 2021;22:266. https://doi.org/10.1186/s13059-021-02483-z
48. Wick RR, Holt KE. Polypolish: Short-read polishing of long-read bacterial genome. PLOS Computational Biology. 2022;18(1):e1009802. https://doi.org/10.1371/journal.pcbi.1009802
49. Zimin AV, Salzberg SL. The genome polishing tool POLCA makes fast and accurate corrections in genome assemblies. PLOS Computational Biology. 2020;16(6):e1007981. https://doi.org/10.1371/journal.pcbi.1007981
50. Marcel M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17(1):10. https://doi.org/10.14806/ej.17.1.200
51. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology. 2012;19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
52. Manni M, Berkeley MR, Seppey M, Zdobnov EM. BUSCO: Assessing genomic data quality and beyond. Current Protocols. 2021;1:e323. https://doi.org/10.1002/cpz1.323
53. Schwengers O, Jelonek L, Dieckmann MA, Beyvers S, Blom J, et al. Bakta: Rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microbial Genomics. 2021;7(11):000685. https://doi.org/10.1099/mgen.0.000685
54. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: A toolkit to classify genomes with the genome taxonomy database. Bioinformatics. 2019;36:1925–1927. https://doi.org/10.1093/bioinformatics/btz848
55. Blin K, Shaw S, Vader L, Szenei J, Reitz ZL, et al. antiSMASH 8.0: Extended gene cluster detection capabilities and analyses of chemistry, enzymology, and regulation. Nucleic Acids Research. 2025;53:32–38. https://doi.org/10.1093/nar/gkaf334
56. Konopka K, Bindereif A, Neilands JB. Aerobactin-mediated utilization of transferrin iron. Biochemistry. 1982;21(25):6503–6508. https://doi.org/10.1021/bi00268a028
57. Seel W, Baust D, Sons D, Albers M, Etzbach L, et al. Carotenoids are used as regulators for membrane fluidity by Staphylococcus xylosus. Scientific Reports. 2020;10(1):330. https://doi.org/10.1038/s41598-019-57006-5
58. Bozhüyük KAJ, Fleischhacker F, Linck A, Wesche F, Tietze A, et al. De novo design and engineering of nonribosomal peptide synthetases. Nature Chemistry. 2018;10:275–281. https://doi.org/10.1038/nchem.2890
59. Miller BR, Gulick AM. Structural biology of nonribosomal peptide synthetases. Methods in Molecular Biology. 2016;1401:3–29. https://doi.org/10.1007/978-1-4939-3375-4_1
60. Singh M, Chaudhary S, Sareen D. Non-ribosomal peptide synthetases: Identifying the cryptic gene clusters and decoding the natural product. Journal of Biosciences. 2017;42:175–187. https://doi.org/10.1007/s12038-017-9663-z
61. Ranjan A, Rajput VD, Prazdnova EV, Gurnani M, Bhardwaj P, et al. Nature’s antimicrobial arsenal: Non-ribosomal peptides from PGPB for plant pathogen biocontrol. Fermentation. 2023;9(7):597. https://doi.org/10.3390/fermentation9070597
62. Jin M, Fischbach MA, Clardy J. A biosynthetic gene cluster for the acetyl-CoA aarboxylase inhibitor andrimid. Journal of the American Chemical Society. 2006;128:10660–10661. https://doi.org/10.1021/ja063194c
63. Shariati VJ, Malboobi MA, Tabrizi Z, Tavakol E, Owlia P, et al. Comprehensive genomic analysis of a plant growthpromoting rhizobacterium Pantoea agglomerans strain P5. Scientific Reports. 2017;7:15610. https://doi.org/10.1038/s41598-017-15820-9
64. Travin DY, Watson ZL, Metelev M, Ward FR, Osterman IA, et al. Structure of ribosome-bound azole-modified peptide phazolicin rationalizes its species-specific mode of bacterial translation inhibition. Nature Communications. 2019;10(1):4563. https://doi.org/10.1038/s41467-019-12589-5
65. Li C, Zha W, Li W, Wang J, You A. Advances in the biosynthesis of terpenoids and their ecological functions in plant resistance. International Journal of Molecular Sciences. 2023;24(14):11561. https://doi.org/10.3390/ijms241411561
66. Loreto F, Dicke M, Schnitzler J, Turlings T. Plant volatiles and the environment. Plant Cell & Environment. 2014;37:1905–1908. https://doi.org/10.1111/pce.12369
67. Bible AN, Fletcher SJ, Pelletier DA, Schadt CW, Jawdy SS, et al. A carotenoid-deficient mutant in Pantoea sp. YR343, a bacteria isolated from the rhizosphere of Populus deltoides, is defective in root colonization. Frontiers in Microbiology. 2016;7:491. https://doi.org/10.3389/fmicb.2016.00491
68. Kumar SV, Abraham PE, Hurs GB, Chourey K, Bible AN, et al. A carotenoid-deficient mutant of the plant-associated microbe Pantoea sp. YR343 displays an altered membrane proteome. Scientific Reports. 2020;10(1):14985. https://doi.org/10.1038/s41598-020-71672-w
69. Choi O, Kang B, Lee Y, Lee Y, Kim J. Pantoea ananatis carotenoid production confers toxoflavin tolerance and is regulated by Hfq‐controlled quorum sensing. MicrobiologyOpen . 2021;10(1):e1143. https://doi.org/10.1002/mbo3.1143
70. Brilli F, Loreto F, Baccelli I. Exploiting plant volatile organic compounds (VOCs) in agriculture to improve sustainable defense strategies and productivity of crops. Frontiers in Plant Science. 2019;10:264. https://doi.org/10.3389/fpls.2019.00264
71. Montejano-Ramírez V, Ávila-Oviedo JL, Campos-Mendoza FJ, Valencia-Cantero E. Microbial volatile organic compounds: Insights into plant defense. Plants. 2024;13(15):2013. https://doi.org/10.3390/plants13152013
72. Wilson BR, Bogdan AR, Miyazawa M, Hashimoto K, Tsuji Y. Siderophores in iron metabolism: From mechanism to therapy potential. Trends in Molecular Medicine. 2016;22(12):1077–1090. https://doi.org/10.1016/j.molmed.2016.10.005
73. Timofeeva AM, Galyamova MR, Sedykh SE. Bacterial siderophores: Classification, biosynthesis, perspectives of use in agriculture. Plants. 2022;11:3065. https://doi.org/10.3390/plants11223065
74. Choi O, Cho J, Kang B, Lee Y, Kim J. Negatively regulated Aerobactin and Desferrioxamine E by fur in Pantoea ananatis are required for full siderophore production and antibacterial activity, but not for virulence. Applied and Environmental Microbiology. 2022;88:e02405–21. https://doi.org/10.1128/aem.02405-21
75. Smits THM, Rezzonico F, Kamber T, Blom J, Goesmann A, et al. Metabolic versatility and antibacterial metabolite biosynthesis are distinguishing genomic features of the fire blight antagonist Pantoea vagans C9-1. PLOS ONE. 2011;6(7):e22247. https://doi.org/10.1371/journal.pone.0022247
76. Sandmann G. Antioxidant protection from UV- and light-stress related to carotenoid structures. Antioxidants. 2019;8:219. https://doi.org/10.3390/antiox8070219
77. Chia GWN, Seviour T, Kjelleberg S, Hinks J. Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization. Environmental Science: Nano. 2021;8:328 –341. https://doi.org/10.1039/D0EN00983K
78. López GD, Álvarez-Rivera G, Carazzone C, Ibáñez E, Leidy C, et al. Bacterial carotenoids: Extraction, characterization, and applications. Critical Reviews in Analytical Chemistry. 2023;53(6):1239–1262. https://doi.org/10.1080/10408347.2021.2016366
