Effective Use of Microorganisms in Agriculture; Microbial Whole Genome Based Approaches

Abstract

The increasing population, urbanization, climate change, and the pressure on crop production threaten the long-term sustainability and functioning of ecosystems. In this context, the conservation of biodiversity and genetic resources forms the foundation of green sustainable agriculture strategies. Genomic-based research on plant-associated microorganisms has significantly expanded our knowledge of both plant pathogens and Plant Growth-Promoting Bacteria (PGPB). The expression of certain genes in microorganisms in natural environments can be suppressed when cultured under standard laboratory conditions due to the absence of natural triggers or stress signals. This study explores the opportunities provided by genomic approaches in understanding the diversity and functional significance of plant-associated microbiomes in sustainable agriculture. The full biosynthetic capacity of bacterial strains for primary and secondary metabolites, which are key indicators for both direct and indirect PGPB mechanisms, can be revealed through whole-genome sequencing analysis. The bacterial whole-genome approach can uncover determinants of various PGPB traits, including gene clusters involved in symbiotic nitrogen fixation, siderophore diversity, and genes associated with antimicrobial/heavy metal resistance. The use of genomic technologies will enable the modulation of beneficial plant-microorganism interactions, paving the way for the development of promising and environmentally friendly new applications for sustainable agriculture.

Keywords

• biodiversity
• microbial Genomes
• PGPB
• sustainable agriculture.

Tarımda Mikroorganizmaların Etkin Kullanımı; Mikrobiyal Tüm Genom Temelli Yaklaşımlar

Abstract

Artan nüfus, şehirleşme, iklim değişikliği ve mahsul üretimi üzerindeki baskı, ekosistemin uzun vadeli sürdürülebilirliğini ve işleyişini tehdit etmektedir. Bu bağlamda, biyoçeşitliliğin ve genetik kaynakların korunması, yeşil sürdürülebilir tarım stratejilerinin önemli bir iş planını oluşturmaktadır. Bitki ile ilişkili mikroorganizmalar üzerine yapılan genom tabanlı araştırmalar hem bitki patojenleri hem de bitki gelişimini destekleyici bakterilerin (PGPB) tarımda kullanımı konusundaki bilgi birikimimizi büyük ölçüde geliştirmiştir. Mikroorganizmaların doğal ortamlardaki bazı gen ifadeleri standart laboratuvar koşullarında kültüre edildiklerinde, doğal tetikleyicilerin veya stres sinyallerinin yokluğundan dolayı baskılanabilmektedir. Bu çalışmada, sürdürülebilir tarımda bitki ile ilişkili mikrobiyom çeşitliliğinin ve işlevsel öneminin anlaşılmasında genomik yaklaşımların sunduğu fırsatlar ele alınmıştır. Bakteriyel suşların primer ve sekonder metabolitler için tam biyosentetik kapasitesi, yani doğrudan ve dolaylı PGPB mekanizmaları için anahtar belirteçler, tüm genom dizisinin analizi ile ortaya çıkarılabilmektedir. Bakteriyel tüm genom yaklaşımı simbiyotik azot fiksasyonunda rol oynayan gen kümeleri, siderofor çeşitliliği, antimikrobiyal/ağır metal direnci ile ilişkili genler başta olmak üzere birçok PGPB özelliklerinin determinantlarını açığa çıkarabilmektedir. Genomik teknolojilerin kullanımı, faydalı bitki-mikroorganizma etkileşimlerinin modülasyonunu sağlayarak sürdürülebilir tarım için umut verici ve çevre dostu yeni uygulamaların geliştirilmesine olanak tanıyacaktır.

Keywords

• biyoçeşitlilik
• mikrobiyal genomlar
• PGPB
• sürdürülebilir tarım

References

1. Ohyama, T. (2017). The role of legume-Rhizobium symbiosis in sustainable agriculture. Legume nitrogen fixation in soils with low phosphorus availability: Adaptation and Regulatory Implication 1-20.
2. Karaca, M., Ince, A.G. (2019). Conservation of biodiversity and genetic resources for sustainable agriculture. Innovations in Sustainable Agriculture 363-410.
3. Binyamin, R., Nadeem, S. M., Akhtar, S., Khan, M.Y., Anjum, R. (2019). Beneficial and pathogenic plant-microbe interactions: A review. Soil & Environment 38(2).
4. Hallmann, J. (2001). Plant interactions with endophytic bacteria.
5. Pontes, J.G.D.M., Fernandes, L.S., dos Santos, R.V., Tasic, L., Fill, T.P. (2020). Virulence factors in the phytopathogen-host interactions: an overview. Journal of Agricultural and Food Chemistry 68(29), 7555-7570.
6. Li, E., de Jonge, R., Liu, C., Jiang, H., Friman, V. P., Pieterse, C. M., ... & Jousset, A. (2021). Rapid evolution of bacterial mutualism in the plant rhizosphere. Nature Communications 12(1), 3829.
7. Ren, X.M., Guo, S.J., Tian, W., Chen, Y., Han, H., Chen, E., ... & Chen, Z.J. (2019). Effects of plant growth-promoting bacteria (PGPB) inoculation on the growth, antioxidant activity, Cu uptake, and bacterial community structure of rape (Brassica napus L.) grown in Cu-contaminated agricultural soil. Frontiers in Microbiology 10, 1455.
8. Fukami, J., Cerezini, P., Hungria, M. (2018). Azospirillum: benefits that go far beyond biological nitrogen fixation. Amb Express 8(1), 73.

9. Nazir, N., Kamili, A.N., Shah, D. (2018). Mechanism of plant growth promoting rhizobacteria (PGPR) in enhancing plant growth-A review. Int. J. Manag. Technol. Eng, 8, 709-721.
10. Lardi, M., Pessi, G. (2018). Functional genomics approaches to studying symbioses between legumes and nitrogen-fixing rhizobia. High-Throughput 7(2), 15.
11. Wang, Z., Lu, K., Liu, X., Zhu, Y., Liu, C. (2023). Comparative functional genome analysis reveals the habitat adaptation and biocontrol characteristics of plant growth-promoting bacteria in NCBI databases. Microbiology Spectrum 11(3), e05007-22.
12. Duflos, R., Vailleau, F., Roux, F. (2024). Toward ecologically relevant genetics of interactions between host plants and plant growth‐promoting bacteria. Advanced Genetics 2300210.
13. Koonin, E.V., Makarova, K.S., Wolf, Y.I. (2021). Evolution of microbial genomics: conceptual shifts over a quarter century. Trends in Microbiology 29(7), 582-592.
14. Gao, F. (2019). Recent developments of software and database in microbial genomics and functional genomics. Briefings in Bioinformatics 20(2), 732-734.
15. Parret, A.H., Temmerman, K., De Mot, R. (2005). Novel lectin-like bacteriocins of biocontrol strain Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology 71(9), 5197-5207.
16. Kumar, V., Eid, E.M., Al-Bakre, D.A., Abdallah, S.M., Širić, I., Andabaka, Ž., ... & Choi, K.S. (2022). Combined use of sewage sludge and plant growth-promoting rhizobia improves germination, biochemical response and yield of ridge gourd (Luffa acutangula (L.) Roxb.) under field conditions. Agriculture 12(2), 173.
17. Koumoutsi, A., Chen, X.H., Henne, A., Liesegang, H., Hitzeroth, G., Franke, P., ... & Borriss, R. (2004). Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42.
18. Paterson, J., Jahanshah, G., Li, Y., Wang, Q., Mehnaz, S., Gross, H. (2017). The contribution of genome mining strategies to the understanding of active principles of PGPR strains. FEMS Microbiology Ecology, 93(3), fiw249.
19. Wang, R., Huo, B., Chen, L., Li, K., Yi, G., Wang, E., ... & Sui, X. (2023). Rhizobia modulate the peanut rhizobacterial community and soil metabolites depending on nitrogen availability. Biology and Fertility of Soils 1-14.
20. Janda, J.M. (2021). Taxonomic classification of bacteria. In Practical Handbook of Microbiology pp.161-166. CRC Press.
21. Christensen, H., Olsen, J.E. (2023). Sequence-Based Classification and Identification. In Introduction to Bioinformatics in Microbiology pp.131-151. Cham: Springer International Publishing.
22. Ribeiro, R.A., Martins, T.B., Ormeno-Orrillo, E., Marcon Delamuta, J.R., Rogel, M.A., Martínez-Romero, E., Hungria, M. (2015). Rhizobium ecuadorense sp. nov., an indigenous N2-fixing symbiont of the Ecuadoriancommon bean (Phaseolus vulgaris L.) genetic pool. International Journal of Systematic and Evolutionary Microbiology, 65(Pt_9), 3162-3169.
23. Le Quéré, A., Tak, N., Gehlot, H.S., Lavire, C., Meyer, T., Chapulliot, D., ... & Munive, J.A. (2017). Genomic characterization of Ensifer aridi, a proposed new species of nitrogen-fixing rhizobium recovered from Asian, African and American deserts. BMC Genomics 18(1), 1-24.
24. Le Quéré, A., Tak, N., Gehlot, H.S., Lavire, C., Meyer, T., Chapulliot, D., ... & Munive, J.A. (2017). Genomic characterization of Ensifer aridi, a proposed new species of nitrogen-fixing rhizobium recovered from Asian, African and American deserts. BMC genomics, 18(1), 1-24.
25. Ashrafi, S., Kuzmanović, N., Patz, S., Lohwasser, U., Bunk, B., Spröer, C., ... & Thünen, T. (2022). Two new Rhizobiales species isolated from root nodules of common sainfoin (Onobrychis viciifolia) show different plant colonization strategies. Microbiology Spectrum, 10(5), e01099-22.
26. Eren Eroğlu, A. E., Eroğlu, V., Yaşa, İ. (2024). Genomic insights into the symbiotic and plant growth-promoting traits of “Candidatus Phyllobacterium onerii” sp. nov. isolated from endemic Astragalus flavescens. Microorganisms, 12(2), 336.
27. Kumar, A., Dubey, A. (2020). Rhizosphere microbiome: Engineering bacterial competitiveness for enhancing crop production. Journal of Advanced Research 24, 337-352.
28. Petrillo, C., Castaldi, S., Lanzilli, M., Selci, M., Cordone, A., Giovannelli, D., Isticato, R. (2021). Genomic and physiological characterization of Bacilli isolated from salt-pans with plant growth promoting features. Frontiers in Microbiology 12, 715678.
29. Snak, A., Vendruscolo, E.C.G., Santos, M.F.D., Fiorini, A., Mesa, D. (2021). Genome sequencing and analysis of plant growth-promoting attributes from Leclercia adecarboxylata. Genetics and Molecular Biology, 44, e20200130.
30. Flores, A., Diaz-Zamora, J.T., Orozco-Mosqueda, M.D.C., Chávez, A., de Los Santos-Villalobos, S., Valencia-Cantero, E., Santoyo, G. (2020). Bridging genomics and field research: draft genome sequence of Bacillus thuringiensis CR71, an endophytic bacterium that promotes plant growth and fruit yield in Cucumis sativus L. 3 Biotech, 10, 1-7.
31. Guerrieri, M.C., Fiorini, A., Fanfoni, E., Tabaglio, V., Cocconcelli, P.S., Trevisan, M., Puglisi, E. (2021). Integrated genomic and greenhouse assessment of a novel plant growth-promoting rhizobacterium for tomato plant. Frontiers in Plant Science 12, 660620.
32. Lu, S., Feng, L., Zhou, D., Jia, M., Liu, Z., Hou, Z., ... & Yu, J. (2022). Complete genome sequence of Bacillus subtilis CNBG-PGPR-1 for studying the promotion of plant growth. Molecular Plant-Microbe Interactions 35(12), 1115-1119.
33. Rehman, M., Jyoti, S.Y., Regon, P., Kakati, S., Mishra, P.K., Tanti, B. Comparative Genomics Analyses of some selected Pseudomonas strains having Biocontrol, Plant Growth Promoting and Bioremediation activities using Bioinformatic Tools.
34. Subramaniam, G., Thakur, V., Saxena, R.K., Vadlamudi, S., Purohit, S., Kumar, V., ... & Varshney, R.K. (2020). Complete genome sequence of sixteen plant growth promoting Streptomyces strains. Scientific Reports 10(1), 10294.
35. Adeleke, B.S., Ayangbenro, A.S., Babalola, O.O. (2021). Genomic analysis of endophytic Bacillus cereus T4S and its plant growth-promoting traits. Plants 10(9), 1776.
36. Jiang, L., Seo, J., Peng, Y., Jeon, D., Park, S.J., Kim, C.Y., ... & Lee, J. (2023). Genome insights into the plant growth-promoting bacterium Saccharibacillus brassicae ATSA2T. AMB Express 13(1), 9.
37. Li, R., Feng, Y., Chen, H., Zhang, C., Huang, Y., Chen, L., ... & Zhou, X. (2020). Whole-genome sequencing of Bradyrhizobium diazoefficiens 113-2 and comparative genomic analysis provide molecular insights into species specificity and host specificity. Frontiers in Microbiology 11, 576800.
38. Jin, C.Z., Wu, X.W., Zhuo, Y., Yang, Y., Li, T., Jin, F.J., ... & Jin, L. (2022). Genomic insights into a free-living, nitrogen-fixing but non nodulating novel species of Bradyrhizobium sediminis from freshwater sediment: Three isolates with the smallest genome within the genus Bradyrhizobium. Systematic and Applied Microbiology 45(5), 126353.
39. Hooykaas, M.J., Hooykaas, P.J. (2021). Complete genomic sequence and phylogenomics analysis of Agrobacterium strain AB2/73: a new Rhizobium species with a unique mega-Ti plasmid. BMC Microbiology 21, 1-17.
40. Chen, X., Huang, H., Zhang, S., Zhang, Y., Jiang, J., Qiu, Y., ... & Wang, A. (2021). Bacillus velezensis WZ-37, a new broad-spectrum biocontrol strain, promotes the growth of tomato seedlings. Agriculture 11(7), 581.
41. Xu, Z., Xie, J., Zhang, H., Wang, D., Shen, Q., Zhang, R. (2019). Enhanced control of plant wilt disease by a xylose-inducible degQ gene engineered into Bacillus velezensis strain SQR9XYQ. Phytopathology 109(1), 36-43.
42. Liu, G., Kong, Y., Fan, Y., Geng, C., Peng, D., Sun, M. (2017). Whole-genome sequencing of Bacillus velezensis LS69, a strain with a broad inhibitory spectrum against pathogenic bacteria. Journal of Biotechnology 249, 20-24.
43. Kaur, S., Dwibedi, V., Sahu, P.K., Kocher, G.S. (Eds.). (2023). Metabolomics, Proteomes and Gene Editing Approaches in Biofertilizer Industry. Springer.
44. Nascimento, F.X., Hernández, A.G., Glick, B.R., Rossi, M.J. (2020). Plant growth-promoting activities and genomic analysis of the stress-resistant Bacillus megaterium STB1, a bacterium of agricultural and biotechnological interest. Biotechnology Reports, 25, e00406.
45. Ali, R. (2021). Role of recombinant DNA technology in biofertilizer production. Microbiota and Biofertilizers: A Sustainable Continuum for Plant and Soil Health, 143-163.
46. Fernández-Llamosas, H., Ibero, J., Thijs, S., Imperato, V., Vangronsveld, J., Díaz, E., Carmona, M. (2020). Enhancing the rice seedlings growth promotion abilities of Azoarcus sp. CIB by heterologous expression of ACC deaminase to improve performance of plants exposed to cadmium stress. Microorganisms 8(9), 1453.
47. Setten, L., Soto, G., Mozzicafreddo, M., Fox, A. R., Lisi, C., Cuccioloni, M., ... & Ayub, N.D. (2013). Engineering Pseudomonas protegens Pf-5 for nitrogen fixation and its application to improve plant growth under nitrogen-deficient conditions. Plos one, 8(5), e63666.
48. Tatemichi, Y., Nakahara, T., Ueda, M., Kuroda, K. (2021). Construction of recombinant Escherichia coli producing nitrogenase-related proteins from Azotobacter vinelandii. Bioscience, Biotechnology, and Biochemistry 85(10), 2209-2216.
49. Jordan, H.R., Tomberlin, J.K. (2017). Abiotic and biotic factors regulating inter-kingdom engagement between insects and microbe activity on vertebrate remains. Insects 54(8). https://doi.org/10.3390/insects8020054.