Long-term adaptation study of bacterial isolates of plant growth-promoting bacteria in heat-stressed conditions Long-term adaptation study of bacterial isolates
Main Article Content
Abstract
In many bacterial species, there is still a lack of comprehensive research and characterization of the basic mechanisms behind bacterial adaptation. Furthermore, it's still unclear if prokaryotes can learn by association and adaptation. Since Plant Growth Promoting Bacteria (PGPB) are essential to the preservation of plant physiology and growth across a range of stress scenarios, PGPB can be utilized to analyze this adaptation of bacteria under stress. This study examines the initial findings on adaptive flexibility in PGPB under conditions of heat stress. The performance of the isolated PGPB receiving both periodic and non-periodic heat stress was compared to that of the control group. Characteristics such as ammonia and siderophore production, phosphate utilization, and amount of indole-3-acetic acid produced, as well as anti-oxidant activities like DPPH activity, hydroxyl radical scavenging activity, and hydrogen peroxide scavenging activity were analysed. Following heat stress treatment, it was clear from the isolated PGPB that those under periodic stress were able to outperform the PGPB exposed to non-periodic stress in comparison to the control. When compared to the other isolates in our investigation, the two novel strains of Paenibacillus alvei SJ6 and Paenibacillus alvei SJ8, among the four isolated PGPB have demonstrated the greatest capacity to respond to sporadic heat stress. Therefore, preliminary evidence for the existence of history-dependent adaptation has been examined in this work.
Article Details
References
Agbodjato N. A. L., Amogou, F., Baba-Moussa, A. Adjanohoun, Baba-Moussa, L. Characterization of plant growth-promoting rhizobacteria under heat stress conditions. Applied and Environmental Soil Science, 2015, 8(9): 901656. https://doi.org/10.1155/2015/901656
Aguilera-Torres C., Riveros G., Morales L.V., Sierra-Almeida A., Schoebitz M., Hasbún R. Relieving your stress: PGPB associated with Andean xerophytic plants are most abundant and active on the most extreme slopes. Frontiers in Microbiology, 2022, 13(1): 1062414. https://doi.org/10.3389/fmicb.2022.1062414
Al-Zahrani H.S., Alharby H.F., Fahad S. Antioxidative defense system, hormones, and metabolite accumulation in different plant parts of two contrasting rice cultivars as influenced by plant growth regulators under heat stress. Frontiers Plant Science, 2022, 13(5): 911846. https://doi.org/10.3389/fpls.2022.911846
Amaya-Gómez Carol V., Porcel Mario, Mesa-Garriga Leyanis, Gómez-Álvarez Martha I. A Framework for the Selection of Plant Growth-Promoting Rhizobacteria Based on Bacterial Competence Mechanisms. Applied Environmental Microbiology, 2020, 86(14): 00760-20. https://doi.org/10.1128/AEM.00760-20
Ammonia Nessler Test Method, Technical Information. Palintest. August 5, 2022. Accessed at: February 9, 2024. Available at: https://www.palintest.com/tech-info-sheet/ammonia-nessler-test-method-technical-information/
Anjum N.A., Gill S.S., Corpas F.J., Hasanuzzaman M., Fujita M., Pereira E., Ahmad I. Editorial: recent insights into the double role of hydrogen peroxide in plants. Frontiers in Plant Science, 2022, 13(1): 843274. https://doi.org/10.3389/fpls.2022.843274
Arora N.K., Verma M. Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech, 2017, 7(6): 381. https://doi.org/10.1007/s13205-017-0940-7
Barbaccia P., Gaglio R., Dazzi C. Plant growth-promoting activities of bacteria isolated from an anthropogenic soil located in Agrigento Province. Microorganisms, 2022 10(11): 2167. https://doi.org/10.3390/microorganisms10112167
Batool T., Ali S., Seleiman M.F., Naveed N.H., Ali A., Ahmed K., Abid M., Rizwan M., Shahid M.R. Plant growth-promoting rhizobacteria alleviate drought stress in potato in response to suppressive oxidative stress and antioxidant enzyme activities. Scientific Reports, 2020 10(1): 16975. https://doi.org/10.1038/s41598-020-73986-1
Bullivant A., Lozano-Huntelman N., Tabibian K. Evolution under thermal stress affects Escherichia coli’s resistance to antibiotics. BioRxiv, 2024, March 03, 2024: 582334. https://doi.org/10.1101/2024.02.27.582334
Chan T.H., Ariyawansa H.A., Rho H. Thermotolerant plant growth-promoting bacteria enhance growth and nutrient uptake of lettuce under heat stress conditions by altering stomatal movement and chlorophyll fluorescence. Physiology and Molecular Biology in Plants, 2024, 30(6): 969-984. https://doi.org/10.1007/s12298-024-01392-4
Dholakiya R.N., Kumar R., Mishra A., Mody K.H., Jha B. Antibacterial and antioxidant activities of novel Actinobacteria strain isolated from Gulf of Khambhat, Gujarat. Frontiers in Microbiology, 2017 8(12): 2420. https://doi.org/10.3389/fmicb.2017.02420
Dutta J., Thakur D. Evaluation of multifarious plant growth promoting traits, antagonistic potential and phylogenetic affiliation of rhizobacteria associated with commercial tea plants grown in Darjeeling, India. PLoS One, 2017, 12(8): e0182302. https://doi.org/10.1371/journal.pone.0182302
Etesami H., Glick B.R. Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience. Microbiology Research. 2024, 281(4): 127602. https://doi.org/10.1016/j.micres.2024.127602
B. R. Glick, Plant growth-promoting bacteria: mechanisms and applications. Scientifica, 2012, 2012(10): 963401. https://doi.org/10.6064/2012/963401
Gohil R.B., Raval V.H., Panchal R.R., Rajput K.N. Plant growth-promoting activity of Bacillus sp. PG-8 isolated from fermented panchagavya and its effect on the growth of Arachis hypogea. Frontiers in Agronomy, 2022 4(3): 805454. https://doi.org/10.3389/fagro.2022.805454
Gray W.M., Ostin A., Sandberg G., Romano C.P., Estelle M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proceedings of the National Academy of Science USA, 1998, 95(12): 7197-7202. https://doi.org/10.1073/pnas.95.12.7197
Hakim, S., Naqqash, T., Nawaz, M. S., Laraib, I., Siddique, M. J., Zia, R., Mehmood, A. Rhizosphere engineering with plant growth-promoting microorganisms for agriculture and ecological sustainability. Frontiers in Sustainable Food Systems, 2021, 5(2): 617157. https://doi.org/10.3389/fsufs.2021.617157
Hasanuzzaman M., Nahar K., Alam M.M., Roychowdhury R., Fujita M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. International Journal of Molecular Science, 2013, 14(5): 9643-9684. https://doi.org/10.3390/ijms14059643
Hasanuzzaman M., Nahar K., Fujit M. Extreme Temperature Responses, Oxidative Stress and Antioxidant Defense in Plants. In: Abiotic Stress - Plant Responses and Applications in Agriculture,
(K.Vahdati and C. Leslie Eds.). IntechOpen. 2013, рр. 169-205, Print ISBN: 978-953-51-1024-8, eBook ISBN: 978-953-51-4254-6, https://doi.org/10.5772/54833
Hossain M.A., Bhattacharjee S., Armin S.M., Qian P., Xin W., Li H.Y., Burritt D.J., Fujita M., Tran L-SP. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Frontiers in Plant Science, 2015; 6(6): 420. https://doi.org/10.3389/fpls.2015.00420
Johnson, J. S., Spakowicz, D. J., Hong, B. Y., Petersen, L. M., Demkowicz, P., Chen, L., Leopold, S. R., Hanson, B. M., Agresta, H. O., Gerstein, M., Sodergren, E. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nature Communications, 2019, 10(11): 5029. https://doi.org/10.1038/s41467-019-13036-1
Kapadia, C., Patel, N., Rana, A., Vaidya, H., Alfarraj, S., Ansari, M. J., Jha, B. Evaluation of plant growth-promoting and salinity-ameliorating potential of halophilic bacteria isolated from saline soil. Frontiers in Plant Science, 2022, 13(8): 946217. https://doi.org/10.3389/fpls.2022.946217
Karthik L., Kumar G., Bhaskara Rao K.V. Antioxidant activity of a newly discovered lineage of marine actinobacteria. Asian Pacific Journal of Tropical Medicine, 2013; 6(4): 325-332. https://doi.org/10.1016/S1995-7645(13)60055-1
Kumar, N., Kumar, A., Jeena, N., Singh, R., & Singh, H. Factors influencing soil ecosystem and agricultural productivity at higher altitudes. In: Microbiological Advancements for Higher Altitude Agro-Ecosystems & Sustainability (R. Goel, R. Soni, D.C. Suyal Eds.), Springer Singapore, 2020, pp. 55-70. Hardcover ISBN: 978-981-15-1901-7; Softcover ISBN: 978-981-15-1904-8; eBook ISBN: 978-981-15-1902-4; Series ISSN: 2523-8442; Series E-ISSN: 2523-8450; Edition 1. https://doi.org/10.1007/978-981-15-5089-2_4
Kumari S., Kumar P., Kiran S., Kumari S., Singh A. Optimization of siderophore production by Bacillus subtilis DR2 and its effect on growth promotion of Coriandrum sativum. Russian Agriculture Scientific, 2022, 48(6): 467-475. https://doi.org/10.3103/S1068367422060091
Li, S., Zhao, Y., Zhang, L., Zhang, X., Huang, L., Li, D., Niu, C., Yang, Z., Wang, Q. Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chemistry, 2012, 135(3): 1914-1919. https://doi.org/10.1016/j.foodchem.2012.06.037
Maury, G.L., Rodríguez, D.M., Hendrix, S., Rodríguez, H., González, R., Aragón, C. Antioxidants in plants: a valorization potential emphasizing the need for the conservation of plant biodiversity in Cuba. Antioxidants, 2020, 9(11): 1048. https://doi.org/10.3390/antiox9111048
Mitra, D., Díaz-Rodríguez, A. M., Parra-Cota, F.I., Khoshru, B., Rahman, M.H., Mahmud, N. Amelioration of thermal stress in crops by plant growth-promoting rhizobacteria. Physiological and Molecular Plant Pathology, 2021, 115(8): 101679. https://doi.org/10.1016/j.pmpp.2021.101679
Pajuelo-Domínguez, E., Arjona, S., Rodríguez-Llorente, I.D., Cubo, T., Ruiz-Lozano, J.M., Mateos-Naranjo, E. Coastal ecosystems as sources of biofertilizers in agriculture: From genomics to application in an urban orchard. Frontiers in Marine Science, 2021,.8(8): 685076. https://doi.org/10.3389/fmars.2021.685076
Powers E.M., Latt T.G. Simplified 48-hour IMVic test: an agar plate method. Applied Environmental Microbiology, 1977, 34(3): 274-279. https://doi.org/10.1128/aem.34.3.274-279.1977
Rajawat, M.V.S., Singh, R., Singh, D., Patel, P., Sahay, H., Gaur, R.K. Spatial distribution and identification of bacteria in stressed environments capable of weathering potassium aluminosilicate mineral. Brazilian Journal of Microbiology, 2020, 51(2): 751-764. https://doi.org/10.1007/s42770-019-00183-1
Rapparini F., Tam Y.Y., Cohen J.D., Slovin J.P. Indole-3-acetic acid metabolism in Lemna gibba undergoes dynamic changes in response to growth temperature. Plant Physiology, 2002,128(4): 1410-1416. https://doi.org/10.1104/pp.010931
Rehan M., Al-Turki A., Abdelmageed A.H.A., Abdelhameid N.M., Omar A.F. Performance of plant-growth-promoting rhizobacteria (PGPR) isolated from sandy soil on growth of tomato (Solanum lycopersicum L.). Plants, 2023, 12(8): 1588. https://doi.org/10.3390/plants12081588
Richards S.L., Wilkins K.A., Swarbreck S.M., Anderson A.A., Habib N., Smith A.G. The hydroxyl radical in plants: From seed to seed. Journal of Experimental Botany, 2015, 66(3): 681-694. https://doi.org/10.1093/jxb/eru373
Sarkar J., Chakraborty B., Chakraborty U. Plant growth-promoting rhizobacteria protect wheat plants against temperature stress through antioxidant signaling and reducing chloroplast and membrane injury. Journal of Plant Growth Regulation, 2018 37(4): 1396-1412. https://doi.org/10.1007/s00344-018-9829-4
Sarkar J., Chakraborty U., Chakraborty B. High-temperature resilience in Bacillus safensis - primed wheat plants: A study of dynamic response associated with modulation of antioxidant machinery, differential expression of HSPs and osmolyte biosynthesis. Environmental and Experimental Botany, 2021, 182(2): 104315. https://doi.org/10.1016/j.envexpbot.2020.104315
Schoebitz M., Ceballos C., Ciamp L. Effect of immobilized phosphate solubilizing bacteria on wheat growth and phosphate uptake. Journal of Soil Science and Plant Nutrition, 2013, 13(1): 1-10. https://doi.org/10.4067/S071895162013000100001
Shapiro J.A. Bacteria are small but not stupid: cognition, natural genetic engineering and socio-bacteriology. Studies in History and Philosophy of Biological and Biomedical Sciences, 2007, 38(4): 807-819. https://doi.org/10.1016/j.shpsc.2007.09.010
Sharma K., Sharma M., Thakur N., Patel D., Reddy S., Singh P. Enhancement of environmental microplastics (MPs) degradation via bacteria under stress conditions: key enzymes, pathways, and mechanisms. World Journal of Microbiology and Biotechnology, 2025, 41(9): 318. https://doi.org/10.1007/s11274-025-04123-7
Shehata T.E., Marr A.G. Effect of temperature on the size of Escherichia coli cells. Journal of Bacteriology, 1975, 124(2): 857-862. https://doi.org/10.1128/jb.124.2.857-862.1975
Sheppard S.K., Guttman D.S., Fitzgerald J.R. Population genomics of bacterial host adaptation. Nature Reviews Genetics, 2018, 19(9): 549-565. https://doi.org/10.1038/s41576-018-0032-z
Shi, Y., Cui, X., Gu, S., Yan, X., Li, R., Xia, S., Chen, H., Ge, J. Antioxidative and probiotic activities of lactic acid bacteria isolated from traditional artisanal milk cheese from Northeast China. Probiotics and Antimicrobial Proteins, 2019, 11(4): 1086-1099. https://doi.org/10.1007/s12602-018-9459-7
Siddiqui M.H., Alamri S.A., Al-Khaishany M.Y.Y., Al-Qutami M.A., Ali H.M., Khan M.N. Sodium nitroprusside and indole acetic acid improve the tolerance of tomato plants to heat stress by protecting against DNA damage. Journal of Plant Interactions, 2017, 12(1): 177-186. https://doi.org/10.1080/17429145.2017.1319507
Sousa A.M., Machado I., Nicolau A., Pereira M.O. Improvements on colony morphology identification towards bacterial profiling. Journal of Microbiology Methods, 2013, 95(3): 327-335. https://doi.org/10.1016/j.mimet.2013.09.016
Swetha J., Sayantan D. Isolation and characterization of plant growth-promoting bacteria (PGPB) from the rhizosphere of Spinacia oleracea L. Research Journal of Biotechnology, 2023, 18(4): 150-158. https://doi.org/10.25303/rjb.2023.18.4.150
Timofeeva A.M., Galyamova M.R., Sedykh S.E. Bacterial siderophores: Classification, biosynthesis, perspectives of use in agriculture. Plants, 2022, 11(22): 3065. https://doi.org/10.3390/plants11223065
Yadav A.N., Sachan S.G., Verma P., Saxena A.K. Prospecting cold deserts of north western Himalayas for microbial diversity and plant growth promoting attributes. Journal of Biosciences and Bioengineering, 2015, 119(6): 683-693. https://doi.org/10.1016/j.jbiosc.2014.11.002
Young K.D. Bacterial morphology: why have different shapes? Current Opinion in Microbiology, 2007, 10(6): 596-600. https://doi.org/10.1016/j.mib.2007.09.009
Zandi P., Schnug E. Reactive oxygen species, antioxidant responses and implications from a microbial modulation perspective. Biology, 2022, 11(2): 155. https://doi.org/10.3390/biology11020155
Zhang C., Kong Y., Xiang Q., Ma Y., Guo Q. Bacterial memory in antibiotic resistance evolution and nanotechnology in evolutionary biology. iScience, 2023, 26(8): 107433. https://doi.org/10.1016/j.isci.2023.107433
Zhang X., Yang Z., Wang L., Yue Y., Wang L., Yang X. The effects of plant growth-promoting rhizobacteria on plants under temperature stress: A meta-analysis. Rhizosphere. 2023, 28(12): 100788. https://doi.org/10.1016/j.rhisph.2023.100788

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Open access articles are distributed under the terms and conditions of the Creative Commons Attribution-Share Alike 4.0 International License (CC BY-SA 4.0) license:
https://creativecommons.org/licenses/by-sa/4.0![]()
If you have any questions about the permitted uses of a specific article, please contact us.
Permissions Department of the Academic Publishing House of the UFT Plovdiv
Plovdiv 4002, 26 Maritsa Blvd., Bulgaria
E-mail: editor.in.chief@ijfsab.com
Tel.: +359 (32) 603-802
Fax: +359 32/ 644 102
