{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T14:49:53Z","timestamp":1792594193940,"version":"4.5.0"},"reference-count":123,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2025,3,18]],"date-time":"2025-03-18T00:00:00Z","timestamp":1742256000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"National Science Centre, Poland","doi-asserted-by":"publisher","award":["DEC-2022\/06\/X\/NZ8\/01165"],"award-info":[{"award-number":["DEC-2022\/06\/X\/NZ8\/01165"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["CIMB"],"abstract":"<jats:p>Rhizobial bacteria perform a number of extremely important functions in the soil environment. In addition to fixing molecular nitrogen and transforming it into a form available to plants, they participate in the circulation of elements and the decomposition of complex compounds present in the soil, sometimes toxic to other organisms. This review article describes the molecular mechanisms occurring in the most diverse group of rhizobia, the genus Bradyrhizobium, allowing these bacteria to adapt to selected substances found in the soil. Firstly, the adaptation of bradyrhizobia to low and high concentrations of elements such as iron, phosphorus, sulfur, calcium and manganese was shown. Secondly, the processes activated in their cells in the presence of heavy metals such as lead, mercury and arsenic, as well as radionuclides, were described. Additionally, due to the potential use of Bradyrhziobium as biofertilizers, their response to pesticides commonly used in agriculture, such as glyphosate, sulfentrazone, chlorophenoxy herbicides, flumioxazine, imidazolinone, atrazine, and insecticides and fungicides, was also discussed. The paper shows the great genetic diversity of bradyrhizobia in terms of adapting to variable environmental conditions present in the soil.<\/jats:p>","DOI":"10.3390\/cimb47030205","type":"journal-article","created":{"date-parts":[[2025,3,18]],"date-time":"2025-03-18T11:02:31Z","timestamp":1742295751000},"page":"205","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Adaptations of the Genus Bradyrhizobium to Selected Elements, Heavy Metals and Pesticides Present in the Soil Environment"],"prefix":"10.3390","volume":"47","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7626-422X","authenticated-orcid":false,"given":"Joanna","family":"Banasiewicz","sequence":"first","affiliation":[{"name":"Department of Biochemistry and Microbiology, Institute of Biology, Warsaw University of Life Sciences (SGGW), Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aleksandra","family":"Gumowska","sequence":"additional","affiliation":[{"name":"Faculty of Biology and Biotechnology, Warsaw University of Life Sciences (SGGW), Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agata","family":"Ho\u0142ubek","sequence":"additional","affiliation":[{"name":"Faculty of Biology and Biotechnology, Warsaw University of Life Sciences (SGGW), Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3370-6910","authenticated-orcid":false,"given":"S\u0142awomir","family":"Orzechowski","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Microbiology, Institute of Biology, Warsaw University of Life Sciences (SGGW), Nowoursynowska 159, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,3,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e0053920","DOI":"10.1128\/JB.00539-20","article-title":"How Rhizobia Adapt to the Nodule Environment","volume":"203","author":"Ledermann","year":"2021","journal-title":"J. Bacteriol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/s44187-024-00167-8","article-title":"Rhizobium as a Biofertilizer for Non-Leguminous Plants","volume":"4","author":"Pereira","year":"2024","journal-title":"Discov. Food"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Fahde, S., Boughribil, S., Sijilmassi, B., and Amri, A. (2023). Rhizobia: A Promising Source of Plant Growth-Promoting Molecules and Their Non-Legume Interactions: Examining Applications and Mechanisms. Agriculture, 13.","DOI":"10.3390\/agriculture13071279"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"012027","DOI":"10.1088\/1755-1315\/1252\/1\/012027","article-title":"The Effect of Rhizobia Inoculum and Mineral Fertilizers on the Number of Root Nodes, Growth, and Yield of Groundnut","volume":"1252","author":"Mohammad","year":"2023","journal-title":"IOP Conf. Ser. Earth Environ. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"107338","DOI":"10.1016\/j.ympev.2021.107338","article-title":"Bradyrhizobium altum sp. nov., Bradyrhizobium oropedii sp. nov. and Bradyrhizobium acaciae sp. nov. from South Africa Show Locally Restricted and Pantropical nodA Phylogeographic Patterns","volume":"167","author":"Avontuur","year":"2022","journal-title":"Mol. Phylogenet. Evol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"95","DOI":"10.17221\/130\/2020-PPS","article-title":"The Multifaceted Plant-Beneficial Rhizobacteria toward Agricultural Sustainability","volume":"57","author":"Fasusi","year":"2021","journal-title":"Plant Protect. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Bitire, T.D., Abberton, M., Oyatomi, O., and Babalola, O.O. (2022). Effect of Bradyrhizobium japonicum Strains and Inorganic Nitrogen Fertilizer on the Growth and Yield of Bambara Groundnut (Vigna subterranea (L.) Verdc) Accessions. Front. Sustain. Food Syst., 6.","DOI":"10.3389\/fsufs.2022.913239"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Zhang, N., Jin, C.-Z., Zhuo, Y., Li, T., Jin, F.-J., Lee, H.-G., and Jin, L. (2023). Genetic Diversity into a Novel Free-Living Species of Bradyrhizobium from Contaminated Freshwater Sediment. Front. Microbiol., 14.","DOI":"10.3389\/fmicb.2023.1295854"},{"key":"ref_9","first-page":"001105","article-title":"Complex Evolutionary History of Photosynthesis in Bradyrhizobium","volume":"9","author":"Avontuur","year":"2023","journal-title":"Microb. Genom."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Gao, Y., \u00d8verlie Arntzen, M., Kjos, M., Bakken, L.R., and Frosteg\u00e5rd, \u00c5. (2023). Denitrification by Bradyrhizobia under Feast and Famine and the Role of the bc1 Complex in Securing Electrons for N2O Reduction. Appl. Environ. Microbiol., 89.","DOI":"10.1128\/aem.01745-22"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3057","DOI":"10.1128\/JB.01188-10","article-title":"Molecular and Biochemical Characterization of the 5-Nitroanthranilic Acid Degradation Pathway in Bradyrhizobium sp. Strain JS329","volume":"193","author":"Qu","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1107\/S2059798323004199","article-title":"Crystal Structure of the Monocupin Ring-Cleaving Dioxygenase 5-Nitrosalicylate 1,2-Dioxygenase from Bradyrhizobium sp.","volume":"79","author":"Eppinger","year":"2023","journal-title":"Acta Crystallogr. Sect. D"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1038\/nchembio.2191","article-title":"Enzymatic hydrolysis by transition-metal-dependent nucleophilic aromatic substitution","volume":"12","author":"Kalyoncu","year":"2016","journal-title":"Nat. Chem. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"121344","DOI":"10.1016\/j.jhazmat.2019.121344","article-title":"High-Efficiency Biodegradation of Chloramphenicol by Enriched Bacterial Consortia: Kinetics Study and Bacterial Community Characterization","volume":"384","author":"Zhang","year":"2019","journal-title":"J. Hazard. Mater."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1038\/nature06592","article-title":"An Earth-System Perspective of the Global Nitrogen Cycle","volume":"451","author":"Gruber","year":"2008","journal-title":"Nature"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1111\/mmi.15198","article-title":"The Divalent Metal Ion Exporter IhpABC Is Required to Maintain Iron Homeostasis under Low to Moderate Environmental Iron Conditions in the Bacterium Bradyrhizobium japonicum","volume":"121","author":"Zhang","year":"2024","journal-title":"Mol. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/S0968-0004(99)01359-6","article-title":"Bacterial Solutions to the Iron-Supply Problem","volume":"24","author":"Braun","year":"1999","journal-title":"Trends Biochem. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/abbi.1999.1518","article-title":"Iron and Oxidative Stress in Bacteria","volume":"373","author":"Ouati","year":"2000","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1111\/mmi.12709","article-title":"The Ins and Outs of Bacterial Iron Metabolism","volume":"93","author":"Frawley","year":"2014","journal-title":"Mol. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Dutta, K., Shityakov, S., and Maruyama, F. (2023). DSF Inactivator RpfB Homologous FadD Upregulated in Bradyrhizobium japonicum under Iron Limiting Conditions. Sci. Rep., 13.","DOI":"10.1038\/s41598-023-35487-9"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1111\/evo.13230","article-title":"The Evolution of Siderophore Production as a Competitive Trait","volume":"71","author":"Niehus","year":"2017","journal-title":"Evolution"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1111\/mmi.15028","article-title":"The Bradyrhizobium japonicum fsrB Gene Is Essential for Utilization of Structurally Diverse Ferric Siderophores to Fulfill Its Nutritional Iron Requirement","volume":"119","author":"Ong","year":"2023","journal-title":"Mol. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1039\/C7MT00112F","article-title":"Ferrous Iron Efflux Systems in Bacteria","volume":"9","author":"Pi","year":"2017","journal-title":"Metallomics"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e00140-17","DOI":"10.1128\/IAI.00140-17","article-title":"The PerR-Regulated P1B-4-Type ATPase (PmtA) Acts as a Ferrous Iron Efflux Pump in Streptococcus pyogenes","volume":"85","author":"Turner","year":"2017","journal-title":"Infect. Immun."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1051\/parasite\/2019069","article-title":"P-Type Transport ATPases in Leishmania and Trypanosoma","volume":"26","author":"Meade","year":"2019","journal-title":"Parasite"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"12054","DOI":"10.1073\/pnas.1218274110","article-title":"Iron and citrate export by a major facilitator superfamily pump regulates metabolism and stress resistance in Salmonella typhimurium","volume":"110","author":"Frawley","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"7938","DOI":"10.1128\/AEM.02835-15","article-title":"A ferrous iron exporter mediates iron resistance in Shewanella oneidensis MR-1","volume":"81","author":"Bennett","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Alves de Souza, A., Michel, D., Arag\u00e3o, O.O., Castro, J., Ferreira, M., and Moreira, F. (Authorea, 2024). Symbiotic efficiency with Enterolobium contortisiliquum, adaptability, and functional genes of Bradyrhizobium strains isolated from soils with high Fe and Mn content, Authorea, preprint.","DOI":"10.22541\/au.173253107.77535964\/v1"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Sankari, S., and O\u2019Brian, M.R. (2016). Synthetic lethality of the bfr and mbfA genes reveals a functional relationship between iron storage and iron export in managing stress responses in Bradyrhizobium japonicum. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0157250"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1080\/15226514.2016.1207600","article-title":"Native rhizobia from Zn mining soil promote the growth of Leucaena leucocephala on contaminated soil","volume":"19","author":"Rangel","year":"2017","journal-title":"Int. J. Phytoremediat."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"32815","DOI":"10.1007\/s11356-019-06394-2","article-title":"Phytoextraction of Iron from Contaminated Soils by Inoculation of Iron-Tolerant Plant Growth-Promoting Bacteria in Brassica juncea L. Czern","volume":"26","author":"Jinal","year":"2019","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"102326","DOI":"10.1016\/j.eti.2022.102326","article-title":"Bacterial Inoculations Mitigate Different Forms of Iron (Fe) Stress and Enhance Nutrient Uptake in Rice Seedlings (Oryza sativa L.)","volume":"26","author":"Chandwani","year":"2022","journal-title":"Environ. Technol. Innov."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1007\/s11101-024-09976-2","article-title":"Role of Secondary Metabolites in Plant Defense Mechanisms: A Molecular and Biotechnological Insight","volume":"24","author":"Upadhyay","year":"2024","journal-title":"Phytochem. Rev."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e13607","DOI":"10.1111\/ppl.13607","article-title":"Nodulating white lupins take advantage of the reciprocal interplay between N and P nutritional responses","volume":"174","author":"Buoso","year":"2022","journal-title":"Physiol. Plant."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Brownlie, W.J., Alexander, P., Cordell, D., Maslin, M., Metson, G.S., Sutton, M.A., and Spears, B.M. (2024). National phosphorus planning for food and environmental security. Curr. Opin. Biotechnol., 90.","DOI":"10.1016\/j.copbio.2024.103226"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"White, P.J., and Hammond, J.P. (2008). Phosphorus in the Global Environment. Ecophysiology of Plant-Phosphorus Interactions, Springer.","DOI":"10.1007\/978-1-4020-8435-5"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.plantsci.2016.12.010","article-title":"Adaptive strategies for nitrogen metabolism in phosphate deficient legume nodules","volume":"256","author":"Valentine","year":"2017","journal-title":"Plant Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"4546","DOI":"10.1038\/s41467-020-18326-7","article-title":"Global phosphorus shortage will be aggravated by soil erosion","volume":"11","author":"Alewell","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1038\/s41467-019-14197-9","article-title":"High-quality genome sequence of white lupin provides insight into soil exploration and seed quality","volume":"11","author":"Hufnagel","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/BF02374724","article-title":"The acquisition of phosphorus by Lupinus albus L. I. Some characteristics of the soil\/root interface","volume":"67","author":"Gardner","year":"1982","journal-title":"Plant Soil"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Pueyo, J.J., Qui\u00f1ones, M.A., Coba de la Pe\u00f1a, T., Fedorova, E.E., and Lucas, M.M. (2021). Nitrogen and phosphorus interplay in lupin root nodules and cluster roots. Front. Plant Sci., 12.","DOI":"10.3389\/fpls.2021.644218"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1046\/j.1365-3040.1999.00441.x","article-title":"Acid phosphatase activity in phosphorus-deficient white lupin roots","volume":"22","author":"Gilbert","year":"2002","journal-title":"Plant Cell Environ."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1046\/j.1469-8137.2003.00695.x","article-title":"Phosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource","volume":"157","author":"Vance","year":"2003","journal-title":"New Phytol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1971","DOI":"10.1016\/j.soilbio.2008.02.017","article-title":"Flavonoids of white lupin roots participate in phosphorus mobilization from soil","volume":"40","author":"Tomasi","year":"2008","journal-title":"Soil Biol. Biochem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1023\/A:1022314613217","article-title":"Structure, ecology and physiology of root clusters\u2014A review","volume":"248","author":"Lamont","year":"2003","journal-title":"Plant Soil"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"115311","DOI":"10.1016\/j.geoderma.2021.115311","article-title":"Phosphorus deficiency in soils with red color: Insights from the interactions between minerals and microorganisms","volume":"404","author":"Su","year":"2021","journal-title":"Geoderma"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1111\/1365-2745.13630","article-title":"Root functional traits explain root exudation rate and composition across a range of grassland species","volume":"110","author":"Williams","year":"2022","journal-title":"J. Ecol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1093\/aob\/mcl154","article-title":"Nitrogen fixation by white lupin under phosphorus deficiency","volume":"98","author":"Schulze","year":"2006","journal-title":"Ann. Bot."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"4023","DOI":"10.1093\/jxb\/ert306","article-title":"The evolution of autotrophy in relation to phosphorus requirement","volume":"64","author":"Raven","year":"2013","journal-title":"J. Exp. Bot."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1128\/JB.188.3.1089-1102.2006","article-title":"Regulation and properties of PstSCAB, a high-affinity, high-velocity phosphate transport system of Sinorhizobium meliloti","volume":"188","author":"Yuan","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_51","first-page":"315","article-title":"Effect of phosphorus nutrition on the nodulation, nitrogen fixation and nutrient-use efficiency of Bradyrhizobiumjaponicun soybean (Glycine max L. Merr.) symbiosis","volume":"3","author":"iTsvetkova","year":"2003","journal-title":"Bulg. J. Plant Physiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1007\/BF00336124","article-title":"Sulfonate S: A major form of forest soil organic sulfur","volume":"10","author":"Autry","year":"1990","journal-title":"Biol. Fertil. Soils"},{"key":"ref_53","unstructured":"Aftab, T., and Hakeem, K.R. (2023). Chapter Two\u2014Plant Nutrition and Soil Fertility: Physiological and Molecular Avenues for Crop Improvement. Sustainable Plant Nutrition, Academic Press."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1146\/annurev-earth-082517-010018","article-title":"Role of Soil Erosion in Biogeochemical Cycling of Essential Elements: Carbon, Nitrogen, and Phosphorus","volume":"46","author":"Berhe","year":"2018","journal-title":"Annu. Rev. Earth Planet. Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"123454","DOI":"10.1016\/j.jhazmat.2020.123454","article-title":"Distinction Between Cr and Other Heavy-Metal-Resistant Bacteria Involved in C\/N Cycling in Contaminated Soils of Copper Producing Sites","volume":"402","author":"Zhang","year":"2020","journal-title":"J. Hazard. Mater."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1007\/BF00035065","article-title":"Enhanced Competitiveness of a Bradyrhizobium japonicum Mutant Strain Improved for Nodulation and Nitrogen Fixation","volume":"186","author":"Kuykendall","year":"1996","journal-title":"Plant Soil"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1007\/BF02374616","article-title":"Dual Inoculation with Rhizobium sp. and Glomus fasciculatum Enhances Nodulation, Yield, and Nitrogen Fixation in Chickpea (Cicer arietinum Linn.)","volume":"95","author":"Rao","year":"1986","journal-title":"Plant Soil"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1007\/s42770-024-01585-7","article-title":"Sulfur Fertilization and Inoculation of Soybean with Azospirillum brasilense and Bradyrhizobium spp. Can Improve Grain Yield and Quality","volume":"56","author":"Deak","year":"2024","journal-title":"Braz. J. Microbiol."},{"key":"ref_59","first-page":"280","article-title":"Effect of Sulfur and Bradyrhizobium Inoculation on Nodulation and Yield of Soybean (Glycine max L.) on Nitisols of Southwestern Ethiopia","volume":"10","author":"Habetamu","year":"2021","journal-title":"Agric. For. Fish."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Becana, M., Wienkoop, S., and Matamoros, M.A. (2018). Sulfur Transport and Metabolism in Legume Root Nodules. Front. Plant Sci., 9.","DOI":"10.3389\/fpls.2018.01434"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1094\/MPMI-08-10-0184","article-title":"Expression and Functional Roles of Bradyrhizobium japonicum Genes Involved in the Utilization of Inorganic and Organic Sulfur Compounds in Free-Living and Symbiotic Conditions","volume":"24","author":"Sugawara","year":"2011","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"e01552-19","DOI":"10.1128\/AEM.01552-19","article-title":"An Alkane Sulfonate Monooxygenase Is Required for Symbiotic Nitrogen Fixation by Bradyrhizobium diazoefficiens (syn. Bradyrhizobium japonicum) USDA110T","volume":"85","author":"Speck","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_63","first-page":"75","article-title":"Elemental Sulphur Application Effects on Nutrient Availability and Sweet Maize (Zea mays L.) Response in a High pH Soil of Malaysia","volume":"18","author":"Karimizarchi","year":"2014","journal-title":"Malays. J. Soil Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/978-1-4020-3548-7_5","article-title":"Fine-Tuning of Symbiotic Genes in Rhizobia: Flavonoid Signal Transduction Cascade","volume":"7","author":"Kobayashi","year":"2008","journal-title":"Nitrogen Fixat. Orig. Appl. Res. Prog."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Yuan, P., Luo, F., Gleason, C., and Poovaiah, B.W. (2022). Calcium\/Calmodulin-Mediated Microbial Symbiotic Interactions in Plants. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.984909"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1146\/annurev-cellbio-120219-035210","article-title":"Calcium Signaling Mechanisms Across Kingdoms","volume":"37","author":"Luan","year":"2021","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1016\/S0176-1617(11)81791-8","article-title":"Role of Ca2+ in Bradyrhizobium japonicum Strain 273 Attachment Ability and Accumulation on Soybean Root Surface","volume":"145","author":"Kadreva","year":"1995","journal-title":"J. Plant Physiol."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Liu, X., Zhang, K., Liu, Y., Zou, D., Wang, D., and Xie, Z. (2020). Effects of Calcium and Signal Sensing Systems on Azorhizobium caulinodans Biofilm Formation and Host Colonization. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.563367"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1016\/j.jcis.2021.03.072","article-title":"Covalently Bonded Hopanoid-Lipid A from Bradyrhizobium: The Role of Unusual Molecular Structure and Calcium Ions in Regulating the Lipid Bilayers Organization","volume":"594","author":"Vitiello","year":"2021","journal-title":"J. Colloid Interface Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e0044221","DOI":"10.1128\/jb.00442-21","article-title":"Hopanoids Confer Robustness to Physicochemical Variability in the Niche of the Plant Symbiont Bradyrhizobium diazoefficiens","volume":"204","author":"Tookmanian","year":"2022","journal-title":"J. Bacteriol."},{"key":"ref_71","first-page":"101","article-title":"Senescence of legume nodules","volume":"45","author":"Andreeva","year":"1998","journal-title":"Rus. J. Plant Physiol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Zhou, S., Zhang, C., Huang, Y., Chen, H., Yuan, S., and Zhou, X. (2021). Characteristics and Research Progress of Legume Nodule Senescence. Plants, 10.","DOI":"10.3390\/plants10061103"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1007\/s12017-009-8101-2","article-title":"Manganese flux across the blood-brain barrier","volume":"11","author":"Yokel","year":"2009","journal-title":"Neuromol. Med."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.enceco.2023.01.001","article-title":"Ecotoxicological consequences of manganese mining pollutants and their biological remediation","volume":"5","author":"Dey","year":"2023","journal-title":"Environ. Chem. Ecotoxicol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"5402","DOI":"10.1073\/pnas.1100410108","article-title":"Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese","volume":"108","author":"Sobota","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1038\/s41565-020-0707-4","article-title":"Differentially charged nanoplastics demonstrate distinct accumulation in Arabidopsis thaliana","volume":"15","author":"Sun","year":"2020","journal-title":"Nat. Nanotechnol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1111\/j.1365-2958.2012.08057.x","article-title":"Manganese is required for oxidative metabolism in unstressed Bradyrhizobium japonicum cells","volume":"84","author":"Hohle","year":"2012","journal-title":"Mol. Microbiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1111\/j.1365-2958.2009.06650.x","article-title":"The mntH gene encodes the major Mn(2+) transporter in Bradyrhizobium japonicum and is regulated by manganese via the Fur protein","volume":"72","author":"Hohle","year":"2009","journal-title":"Mol. Microbiol."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Pisarek, I., and Grata, K. (2023). The Influence of Sewage Sludge and Fly Ash Fertilization on the Total Number of Bacteria (TNB) and Bradyrhizobium Species in Soybean Agroecosystem. Agriculture, 13.","DOI":"10.3390\/agriculture13010201"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1081\/PLN-120027552","article-title":"Manganese toxicity in mycorrhizal and phosphorus-fertilized soybean plants","volume":"27","author":"Nogueira","year":"2007","journal-title":"J. Plant Nutr."},{"key":"ref_81","first-page":"353","article-title":"Manganese toxicity in plants","volume":"21","author":"Cox","year":"2008","journal-title":"J. Plant Nutr."},{"key":"ref_82","first-page":"167","article-title":"The effect of copper on bacteria of the genus Azospirillum in the rhizosphere of maize and wheat seedlings","volume":"10","author":"Sawicka","year":"2010","journal-title":"Water-Environ. Rural. Areas"},{"key":"ref_83","first-page":"7","article-title":"The effect of seeds treatment with a micronutrient fertilizer on chlorophyll content in leaves and yield of soya","volume":"36","year":"2019","journal-title":"Fragm. Agron."},{"key":"ref_84","first-page":"17","article-title":"Effect of selected micronutrient seed fertilizers on the viability of Bradyrhizobium japonicum","volume":"61","year":"2021","journal-title":"Prog. Plant Prot."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1007\/s42770-021-00420-7","article-title":"Bradyrhizobium sp. sv. retamae nodulates Retama monosperma grown in a lead and zinc mine tailings in Eastern Morocco","volume":"52","author":"Lamin","year":"2021","journal-title":"Braz. J. Microbiol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s10532-012-9555-8","article-title":"Impact of mercury on denitrification and denitrifying microbial communities in nitrate enrichments of subsurface sediments","volume":"24","author":"Wang","year":"2013","journal-title":"Biodegradation"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.plaphy.2012.11.007","article-title":"Arsenic effect on the model crop symbiosis Bradyrhizobium-soybean","volume":"63","author":"Talano","year":"2013","journal-title":"Plant Physiol. Biochem."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1111\/1751-7915.13578","article-title":"Co-occurrence of antibiotic, biocide, and heavy metal resistance genes in bacteria from metal and radionuclide contaminated soils at the Savannah River Site","volume":"13","author":"Thomas","year":"2020","journal-title":"Microb. Biotechnol."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Arregui, G., Hip\u00f3lito, P., Pallol, B., Lara-Dampier, V., Garc\u00eda-Rodr\u00edguez, D., Varela, H.P., Tavakoli Zaniani, P., Balomenos, D., Paape, T., and Coba de la Pe\u00f1a, T. (2021). Mercury-Tolerant Ensifer medicae Strains Display High Mercuric Reductase Activity and a Protective Effect on Nitrogen Fixation in Medicago truncatula Nodules Under Mercury Stress. Front. Plant Sci., 11.","DOI":"10.3389\/fpls.2020.560768"},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Agashe, R., George, J., Pathak, A., Fasakin, O., Seaman, J., and Chauhan, A. (2024). Shotgun Metagenomics Analysis Indicates Bradyrhizobium spp. as the Predominant Genera for Heavy Metal Resistance and Bioremediation in a Long-Term Heavy Metal-Contaminated Ecosystem. Microbiol. Resour. Announc., 13.","DOI":"10.1128\/mra.00245-24"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"112547","DOI":"10.1016\/j.jenvman.2021.112547","article-title":"Heavy Metals Multi-Tolerant Bradyrhizobium Isolated from Mercury Mining Region in Algeria","volume":"289","author":"Salmi","year":"2021","journal-title":"J. Environ. Manag."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s42452-019-1932-z","article-title":"Bioavailability of Arsenic in Agricultural Soils Under the Influence of Different Soil Properties","volume":"2","author":"Singh","year":"2020","journal-title":"SN Appl. Sci."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"930","DOI":"10.1007\/s00267-020-01351-z","article-title":"Assessing the Plant Growth Promoting and Arsenic Tolerance Potential of Bradyrhizobium japonicum CB1809","volume":"66","author":"Seraj","year":"2020","journal-title":"Environ. Manag."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"88066","DOI":"10.1007\/s11356-022-21443-z","article-title":"Promising Co-Inoculation Strategies to Reduce Arsenic Toxicity in Soybean","volume":"29","author":"Vezza","year":"2022","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"127410","DOI":"10.1016\/j.chemosphere.2020.127410","article-title":"Unraveling the Impact of Arsenic on the Redox Response of Peanut Plants Inoculated with Two Different Bradyrhizobium sp. Strains","volume":"259","author":"Peralta","year":"2020","journal-title":"Chemosphere"},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Seiler, C., and Berendonk, T.U. (2012). Heavy Metal Driven Co-selection of Antibiotic Resistance in Soil and Water Bodies Impacted by Agriculture and Aquaculture. Front. Microbiol., 3.","DOI":"10.3389\/fmicb.2012.00399"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.tim.2006.02.006","article-title":"Co-selection of Antibiotic and Metal Resistance","volume":"14","author":"Wright","year":"2006","journal-title":"Trends Microbiol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"60","DOI":"10.26814\/cps2021008","article-title":"Weed Management with Pre-emergent Herbicides in Soybean Crops","volume":"11","author":"Salomao","year":"2021","journal-title":"Commun. Plant Sci."},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Rodrigues, T.F., Bender, F.R., Sanzovo, A.W.S., Ferreira, E., Nogueira, M.A., and Hungria, M. (2020). Impact of Pesticides in Properties of Bradyrhizobium spp. and in the Symbiotic Performance with Soybean. World J. Microbiol. Biotechnol., 36.","DOI":"10.1007\/s11274-020-02949-5"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"127046","DOI":"10.1016\/j.chemosphere.2020.127046","article-title":"Changes in Rhizobacterial Community Mediating Atrazine Dissipation by Arbuscular Mycorrhiza","volume":"256","author":"Fan","year":"2020","journal-title":"Chemosphere"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"149200","DOI":"10.1016\/j.scitotenv.2021.149200","article-title":"Synergetic Toxicity of Silver Nanoparticle and Glyphosate on Wheat (Triticum aestivum L.)","volume":"797","author":"Feng","year":"2021","journal-title":"Sci. Total Environ."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"825","DOI":"10.2134\/jeq2004.0825","article-title":"Impact of Glyphosate on the Bradyrhizobium japonicum Symbiosis with Glyphosate-Resistant Transgenic Soybean: A Minireview","volume":"33","author":"Zablotowicz","year":"2004","journal-title":"J. Environ. Qual."},{"key":"ref_103","first-page":"84","article-title":"Herbicide-Induced Oxidative Stress in Bradyrhizobium and Its Effects on Symbiotic Nitrogen Fixation","volume":"336","author":"Verma","year":"2017","journal-title":"J. Hazard. Mater."},{"key":"ref_104","first-page":"323","article-title":"Impact of Herbicides on Soil Microbial Communities and Resistance of Bradyrhizobium to Herbicides","volume":"72","author":"Saxena","year":"2020","journal-title":"Agric. Microbiol."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.3390\/molecules20011161","article-title":"Degradation Dynamics of Glyphosate in Different Types of Citrus Orchard Soils in China","volume":"20","author":"Zhang","year":"2015","journal-title":"Molecules"},{"key":"ref_106","doi-asserted-by":"crossref","unstructured":"Singh, S., Kumar, V., Gill, J.P.K., Datta, S., Singh, S., Dhaka, V., Kapoor, D., Wani, A.B., Dhanjal, D.S., and Kumar, M. (2020). Herbicide Glyphosate: Toxicity and Microbial Degradation. Int. J. Environ. Res. Public Health, 17.","DOI":"10.3390\/ijerph17207519"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"5033","DOI":"10.1007\/s00253-018-9035-0","article-title":"Recent advances in glyphosate biodegradation","volume":"102","author":"Zhan","year":"2018","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"114155","DOI":"10.1016\/j.ecoenv.2022.114155","article-title":"Influence of glyphosate and its metabolite aminomethylphosphonic acid on aquatic plants in different ecological niches","volume":"246","author":"Qu","year":"2022","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"1991","DOI":"10.1007\/s00284-021-02467-z","article-title":"Glyphosate Biodegradation Potential in Soil Based on Glycine Oxidase Gene (thiO) from Bradyrhizobium","volume":"78","author":"Erijman","year":"2021","journal-title":"Curr. Microbiol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1614\/WT-D-12-00037.1","article-title":"Field Dissipation of Sulfentrazone and Pendimethalin in Colorado","volume":"26","author":"Shaner","year":"2012","journal-title":"Weed Technol."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1590\/S1517-83822010000100030","article-title":"Microbial degradation of sulfentrazone in a Brazilian rhodic hapludox soil","volume":"41","author":"Martinez","year":"2010","journal-title":"Braz. J. Microbiol."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"127033","DOI":"10.1016\/j.chemosphere.2020.127033","article-title":"Does Canavalia ensiformis inoculation with Bradyrhizobium sp. enhance phytoremediation of sulfentrazone-contaminated soil?","volume":"255","author":"Mielke","year":"2020","journal-title":"Chemosphere"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"100434","DOI":"10.1016\/j.cscee.2023.100434","article-title":"Biodegradation potential of 2,4 dichlorophenoxyacetic acid by Cupriavidus campinensis isolated from rice farm cultivated soil","volume":"8","author":"Muhammad","year":"2023","journal-title":"Case Stud. Chem. Environ. Eng."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"5065","DOI":"10.1007\/s00253-019-09838-4","article-title":"Biological agents for 2,4-dichlorophenoxyacetic acid herbicide degradation","volume":"103","author":"Serbent","year":"2019","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"ME21016","DOI":"10.1264\/jsme2.ME21016","article-title":"Multiple Gene Clusters and Their Role in the Degradation of Chlorophenoxyacetic Acids in Bradyrhizobium sp. RD5-C2 Isolated from Non-Contaminated Soil","volume":"36","author":"Hayashi","year":"2021","journal-title":"Microb. Environ."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"132477","DOI":"10.1016\/j.chemosphere.2021.132477","article-title":"Assessment of Flumioxazin Soil Behavior and Thermal Stability in Aqueous Solutions","volume":"288","author":"Eason","year":"2022","journal-title":"Chemosphere"},{"key":"ref_117","doi-asserted-by":"crossref","unstructured":"Xu, Z., Li, B., Jia, Y., Guo, X., and Lv, F. (2023). Biodegradation of Imazethapyr by Bacterial Strain IM9601 Isolated from Agricultural Soil. Curr. Microbiol., 81.","DOI":"10.1007\/s00284-023-03533-4"},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"138581","DOI":"10.1016\/j.chemosphere.2023.138581","article-title":"Short-term responses of plant growth-promoting bacterial community to the herbicides imazethapyr and flumioxazin","volume":"328","author":"Araujo","year":"2023","journal-title":"Chemosphere"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"44415","DOI":"10.1007\/s11356-023-25395-w","article-title":"Enhanced phytoremediation of atrazine-contaminated soil by vetiver (Chrysopogon zizanioides L.) and associated bacteria","volume":"30","author":"Zhang","year":"2023","journal-title":"Environ. Sci. Pollut. Res. Int."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.plaphy.2023.02.007","article-title":"Exogenous application of Bradyrhizobium japonicum AC20 enhances soybean tolerance to atrazine via regulating rhizosphere soil microbial community and amino acid, carbohydrate metabolism related genes expression","volume":"196","author":"Jiang","year":"2023","journal-title":"Plant Physiol. Biochem. PPB"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"115636","DOI":"10.1016\/j.envpol.2020.115636","article-title":"Metagenomic analysis reveals mechanisms of atrazine biodegradation promoted by tree species","volume":"267","author":"Aguiar","year":"2020","journal-title":"Environ. Pollut. (Barking Essex 1987)"},{"key":"ref_122","doi-asserted-by":"crossref","unstructured":"Khalid, U., Aftab, Z.E., Anjum, T., Bokhari, N.A., Akram, W., and Anwar, W. (2024). Harnessing the Biocontrol Potential of Bradyrhizobium japonicum FCBP-SB-406 to Manage Charcoal Rot of Soybean with Increased Yield Response for the Development of Sustainable Agriculture. Microorganisms, 12.","DOI":"10.3390\/microorganisms12020304"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1007\/s10658-019-01828-6","article-title":"PGPR-induced defense responses in the soybean plant against charcoal rot disease","volume":"155","author":"Mufti","year":"2019","journal-title":"Eur. J. Plant Pathol."}],"container-title":["Current Issues in Molecular Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1467-3045\/47\/3\/205\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:56:07Z","timestamp":1760028967000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1467-3045\/47\/3\/205"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,18]]},"references-count":123,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,3]]}},"alternative-id":["cimb47030205"],"URL":"https:\/\/doi.org\/10.3390\/cimb47030205","relation":{},"ISSN":["1467-3045"],"issn-type":[{"value":"1467-3045","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,18]]}}}