امکان‌سنجی جداسازی تثبیت‌کنندگان نیتروژن اتوتروفی و هتروتروفی از زیست‌لایه پریفایتون در شالیزار و بررسی اثرات آن بر رشد گیاه برنج در شرایط گلخانه‌ای

مقالات آماده انتشار

نوع مقاله : مقاله پژوهشی

نویسندگان

1 گروه علوم و مهندسی خاک، دانشکدگان کشاورزی و منابع طبیعی، دانشگاه تهران، تهران، ایران

2 گروه علوم ومهندسی خاک، دانشکدگان پردیس کشاورزی و منابع طبیعی دانشگاه تهران، کرج، ایران

چکیده

هدف از انجام این پژوهش بررسی پتانسیل زیست‌لایه پریفایتون و تثبیت‌کنندگان ساکن در آن برای تقویت تثبیت بیولوژیکی نیتروژن و بهبود حاصلخیزی خاک در شالیزارها بود. برای این منظور، نمونه‌های زیست‌لایه پریفایتونی از شالیزارهای استان گیلان جمع‌آوری شد و با تثبیت‌کنندگان جداشده از خود زیست‌لایه که در آزمون توان تثبیت نیتروژن برتر شناخته شده بودند، غنی‌سازی شدند. به مدت 40 روز در شرایط گلخانه‌ای اثر تیمارهای مختلف بر خاک و گیاه پایش گردید. نتایج نشان داد که زیست‌لایه پریفایتون پتانسیل بسیار بالایی در حاصلخیزی خاک و حمایت از رشد گیاه برنج دارد. تیمار پریفایتون‌غنی‌شده با باکتری و سیانوباکتری به طور قابل‌توجهی ویژگی‌های خاک از جمله میزان نیتروژن کل (37/83 درصد)، آمونیوم (42/1 درصد)، فسفر قابل‌جذب (35 درصد) و پتاسیم قابل‌دسترس (15/36) را افزایش داد. حاصلخیزی خاک منجر به افزایش کارایی جذب نیتروژن توسط گیاه شد. افزایش فراهمی نیتروژن در محلول خاک، افزایش در پارامترهای رشد از جمله ارتفاع گیاه، وزن خشک، میزان نیتروژن (3/97 درصد)، فسفر (5/18 درصد) و پتاسیم (5/21 درصد) در بافت گیاهچه‌های برنج را به دنبال داشت. نتایج حاصل از این تحقیق نشان داد که زیست‌لایه‌های موجود در شالیزارهای شمال ایران به مانند ریزوسفر گیاه برنج، میزبان طیف وسیعی از PGPRها از جمله انواع تثبیت‌کنندگان می‌باشند که با بهره‌گیری از آن‌ها، می‌توان راهکاری نوین در کشت محصولی سالم و پایدار ارائه داد. کودهای زیستی مبتنی بر پریفایتون به عنوان روشی جدید می‌توانند سلامت خاک و گیاه را تضمین کنند.

کلیدواژه‌ها

موضوعات

عنوان مقاله [English]

Feasibility of Isolating Heterotrophic and Autotrophic Diazotrophs from Periphyton Biofilm in Rice Fields and Evaluating Their Effects on Rice Growth under Greenhouse Conditions

نویسندگان [English]

  • Mehran Gholami 1
  • Hosseinali Alikhani 2
  • Hassan Etesami 1
  • Zahra Karami 1
  • Mohaddeseh Shirinzadeh 1
  • Hamidreza Zare Guildehi 1
1 Department of soil science, University of Tehran, Tehran, Iran
2 Soli Science and Engineering, College of Agriculture & Natural Resources, University of Tehran, َKaraj, Iran
چکیده [English]

Background and Objectives: Rice, a key staple crop for over half the global population, is mainly grown in Asia and heavily depends on synthetic nitrogen fertilizers, which harm the environment and raise costs. Improving nitrogen use efficiency (NUE) in rice is essential, as current NUE is 28–35%, below the global average. Strategies to enhance NUE include balanced fertilization, slow-release fertilizers, nitrification inhibitors, precision nitrogen management, and breeding for efficient varieties. However, these approaches face challenges like high costs, labor intensity, and technological inaccessibility for small farmers. Biological nitrogen fixation (BNF) offers a promising alternative, using nitrogen-fixing bacteria to enhance NUE and yield while reducing chemical inputs. Studies show rice roots host beneficial bacteria like Azospirillum and Burkholderia, which support BNF. Yet, their effectiveness can be limited by soil and environmental factors. Periphytic biofilms, formed at the soil-water interface in rice paddies, are emerging as a valuable component in nitrogen cycling. Rich in microorganisms such as cyanobacteria and protozoa, these biofilms stabilize nitrogen in the ecosystem, reduce nitrogen losses, and act as natural biofertilizers. They support nitrogen fixation and nutrient uptake, boosting rice growth.Despite their benefits, periphytic biofilms are understudied. Recent research focuses on isolating nitrogen-fixing bacteria from these biofilms to assess their impact on nitrogen levels and rice growth. This study highlights the potential of diazotrophic biofilm enrichment as a sustainable solution to reduce fertilizer dependency, improve crop productivity, and promote environmental sustainability in rice farming.




Materials and Methods: This study focused on evaluating soil, water, and periphytic biofilms in paddy fields in Guildeh, Iran, to investigate the impact of nitrogen-fixing microorganisms on rice plant nutrition. Soil, water, and periphyton samples were collected and analyzed for chemical properties using standard methods. Soil parameters such as pH, texture, nitrogen, phosphorus, and potassium content were measured. Microbial populations, including fungi and bacteria, were counted using plate count methods. To isolate nitrogen-fixing microbes (diazotrophs), periphyton samples were cultured on selective media. Bacterial and cyanobacterial isolates capable of growing on nitrogen-free media were identified through morphological and genetic analysis using 16S rRNA gene sequencing. Delftia lacustris (bacterial) and Nostoc sp. (cyanobacterial) were selected for further testing based on their nitrogen-fixing abilities. A greenhouse experiment was conducted in a completely randomized design with three replicates to assess the effects of these isolates, alone and in combination, on rice plant growth. Treatments included natural periphyton, periphyton enriched with isolates, and controls with and without nitrogen fertilizer. Rice seeds were planted in pots with paddy soil, and periphyton treatments were applied. Growth conditions were controlled, and plants were monitored for 40 days. At the end of the experiment, soil and plant samples were analyzed for nutrient content. Plant height, dry weight, nitrogen (by Kjeldahl method), phosphorus (by spectrophotometry), and potassium (by flame photometry) concentrations were measured. The study aimed to compare the effectiveness of microbial inoculants with chemical fertilizers in enhancing rice plant nutrition, supporting the use of diazotrophic organisms as sustainable alternatives in agriculture.
Results: The study demonstrated that applying periphytic biofilms, enriched with beneficial microorganisms, significantly improved soil fertility by enhancing the availability of nitrogen, phosphorus, and potassium in paddy fields. The enriched periphyton treatment (P+B+C) increased total soil nitrogen by 37.8% and ammonium by 42.1% compared to the unfertilized control. This improvement is largely due to biological nitrogen fixation carried out by microorganisms such as Nostoc species and Delftia lacustris, which convert atmospheric nitrogen into forms accessible to plants. Ammonium content also rose across all periphyton treatments after the growth period, indicating the active role of these microbial communities in nitrogen cycling. Soil phosphorus levels increased significantly with periphyton treatments (35%). The biofilms enhanced phosphorus availability by harboring phosphate-solubilizing microorganisms that release enzymes such as phosphatases. These enzymes break down organic phosphorus into forms that plants can absorb. Additionally, the periphyton helped regulate phosphorus availability over time, ensuring a steady supply during different growth stages of rice plants. Potassium availability also improved due to the presence of potassium-solubilizing microorganisms within the periphyton (15.36%). These microbes released substances that aided in converting fixed potassium into soluble forms, which plants can uptake. Periphyton also served as a reservoir, storing potassium early in the plant’s development and releasing it when needed later in the growth cycle. Rice plants treated with periphyton showed clear improvements in growth, including greater height, biomass, and higher nutrient content. These benefits were linked to the activity of plant growth-promoting microbes that produce hormones, facilitate nutrient absorption, and protect against stress. Notably, Delftia lacustris and Nostoc species were crucial contributors to these effects. Overall, periphyton-based treatments offer a sustainable and effective alternative to chemical fertilizers, enhancing nutrient cycling and supporting healthier, more productive rice cultivation systems.




Conclusion: The results show that applying periphyton can significantly improve soil fertility and enhance the nutritional status of rice plants. Periphyton, rich in plant growth-promoting rhizobacteria (PGPR), plays a key role in supporting rice growth. Treatments involving periphyton produced better outcomes than other treatments, especially when enriched with Delftia lacustris and Nostoc species, which greatly increased nitrogen availability compared to natural periphyton and controls. While nitrogen improvement was the main focus, phosphorus and potassium levels in the soil also showed notable increases. These nutrient enhancements supported greater rice plant height and dry weight, highlighting the value of periphyton enrichment in improving soil quality and plant development. The study emphasizes the potential of using microbial communities like periphytic biofilms to promote sustainability in rice production systems. Future research should explore the long-term effects of periphyton application across different environmental conditions to optimize its use in sustainable agriculture worldwide. Understanding the role of these biofilms in nitrogen cycling can inform biofertilization strategies aimed at reducing synthetic fertilizer use and increasing agricultural productivity. Overall, the findings suggest that periphytic biofilms act as important reservoirs for nitrogen-fixing microbes, playing a vital role in nutrient cycling in both aquatic and terrestrial ecosystems.

کلیدواژه‌ها [English]

  • Biofertilizer
  • Biological nBiofertilizer
  • Biological nitrogen fixation
  • Cyanobacteria
  • Nitrogen
  • Sustainable agriculture

مراجع

  1. Abod, É., Laslo, É., Szentes, S., Lányi, S., & Mara, G. (2019). Plant growth-promoting bacteria: strategies to improve wheat growth and development under sustainable agriculture. Plant Growth Promoting Rhizobacteria for Agricultural Sustainability: From Theory to Practices, 1-17.
  2. Agafonova, N., Doronina, N., Kaparullina, E., Fedorov, D., Gafarov, A., Sazonova, O., Sokolov, S., & Trotsenko, Y. A. (2017). A novel Delftia plant symbiont capable of autotrophic methylotrophy. Microbiology, 86, 96-105.
  3. Al-Maliki, S., & Ebreesum, H. (2020). Changes in soil carbon mineralization, soil microbes, roots density and soil structure following the application of the arbuscular mycorrhizal fungi and green algae in the arid saline soil. Rhizosphere, 14, 100203.
  4. Alikhani, H. A., Ahmadi, H., Etesami, H., Noroozi, M., Rahmani, H. A., & Emami, S. (2023). Studies on Autotrophic Components of Periphyton in Some Iranian Aquatic Ecosystems. International Journal of Environmental Research, 17(2), 24.
  5. Alikhani, H. A., Beheshti, M., Pourbabaee, A. A., Etesami, H., Asadi Rahmani, H., & Noroozi, M. (2023). Phosphorus Use Management in Paddy Fields by Enriching Periphyton with Its Phosphate-Solubilizing Bacteria and Fungi at the Late Stage of Rice Growth. Journal of Soil Science and Plant Nutrition, 23(2), 1896-1912. https://doi.org/10.1007/s42729-023-01145-2
  6. Alikhani, H., Ahmadi, H., Etesami, H., Noroozi, M., Asadi Rahmani, H., & Emami, S. (2021). Study of periphyton (algae flora) community in aquatic ecosystems of Guilan province. Journal of Soil Biology, 9(1), 29-39. (In Persian).
  7. Álvarez, C., Jiménez-Ríos, L., Iniesta-Pallarés, M., Jurado-Flores, A., Molina-Heredia, F. P., Ng, C. K., & Mariscal, V. (2023). Symbiosis between cyanobacteria and plants: from molecular studies to agronomic applications. Journal of Experimental Botany, 74(19), 6145-6157.
  8. Álvarez, C., Navarro, J. A., Molina-Heredia, F. P., & Mariscal, V. (2020). Endophytic colonization of rice (Oryza sativa L.) by the symbiotic strain Nostoc punctiforme PCC 73102. Molecular Plant-Microbe Interactions, 33(8), 1040-1045.
  9. Arnon, D. I. (1949). Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1), 1.
  10. Arvind, G., Sood, S., Rahi, P., Thakur, R., Chauhan, S., & Nee Chadha, I. C. (2011). Diversity analysis of diazotrophic bacteria associated with the roots of tea (Camellia sinensis (L.) O. Kuntze). Journal of microbiology and biotechnology, 21(6), 545-555.
  11. Bahadur, I., Maurya, R., Roy, P., & Kumar, A. (2019). Potassium-solubilizing bacteria (KSB): a microbial tool for K-solubility, cycling, and availability to plants. Plant Growth Promoting Rhizobacteria for Agricultural Sustainability: From Theory to Practices, 257-265.
  12. Baird, R. B., Eaton, A. D., & Rice, E. W. (Eds.). (2017). Standard methods for the examination of water and wastewater. American Public Health Association.
  13. Bao, J., Zhuo, C., Zhang, D., Li, Y., Hu, F., Li, H., Su, Z., Liang, Y., & He, H. (2021). Potential applicability of a cyanobacterium as a biofertilizer and biopesticide in rice fields. Plant and Soil, 463, 97-112.
  14. Beheshti, M., Alikhani, H. A., Pourbabaee, A. A., Etesami, H., Asadi Rahmani, H., & Noroozi, M. (2022). Enriching periphyton with phosphate-solubilizing microorganisms improves the growth and concentration of phosphorus and micronutrients of rice plant in calcareous paddy soil. Rhizosphere, 24, 100590. https://doi.org/10.1016/j.rhisph.2022.100590
  15. Beheshti, M., Alikhani, H. A., Pourbabaee, A. A., Etesami, H., Asadi Rahmani, H., & Noroozi, M. (2021). Periphytic biofilm and rice rhizosphere phosphate-solubilizing bacteria and fungi: A possible use for activating occluded P in periphytic biofilms in paddy fields. Rhizosphere, 19, 100395. https://doi.org/https://doi.org/10.1016/j.rhisph.2021.100395
  16. Bharti, A., Velmourougane, K., & Prasanna, R. (2017). Phototrophic biofilms: diversity, ecology and applications. Journal of Applied Phycology, 29, 2729-2744.
  17. Borsodi, A. K., Rusznyák, A., Molnár, P., Vladár, P., Reskóné, M. N., Tóth, E. M., Sipos, R., Gedeon, G., & Márialigeti, K. (2007). Metabolic activity and phylogenetic diversity of reed (Phragmites australis) periphyton bacterial communities in a Hungarian shallow soda lake. Microbial ecology, 53, 612-620.
  18. Bremner, J., & Keeney, D. (1966). Determination and isotope‐ratio analysis of different forms of nitrogen in soils: 3. Exchangeable ammonium, nitrate, and nitrite by extraction‐distillation methods. Soil Science Society of America Journal, 30(5), 577-582.
  19. Chen, X., Chen, X., Zhao, Y., Zhou, H., Xiong, X., & Wu, C. (2020). Effects of microplastic biofilms on nutrient cycling in simulated freshwater systems. Science of the Total Environment, 719, 137276.
  20. Chen, Z., Dolfing, J., Zhuang, S., & Wu, Y. (2022). Periphytic biofilms-mediated microbial interactions and their impact on the nitrogen cycle in rice paddies. Eco-environment & health, 1(3), 172-180.
  21. Ding, L.-J., Cui, H.-L., Nie, S.-A., Long, X.-E., Duan, G.-L., & Zhu, Y.-G. (2019). Microbiomes inhabiting rice roots and rhizosphere. FEMS Microbiology Ecology, 95(5), fiz040.
  22. Etesami, H. (2019). Plant growth promotion and suppression of fungal pathogens in rice (Oryza sativa L.) by plant growth-promoting bacteria. Field crops: sustainable management by PGPR, 351-383.
  23. Gholami, M., Sharifi, Z., Karami, Z., Haghighi, S., Minouei, S. F., Zema, D. A., & Lucas-Borja, M. E. (2020). The potential impacts of soil sampling on erosion. International Journal of Environmental Science and Technology, 17, 4909-4916.
  24. Haghani, Z., Alikhani, H. A., Amirhosseini, K., Emami, S., & Etesami, H. (2024). Assessing the potential of functionally-enhanced periphyton in supplying rice plant phosphorus nutrition in paddy fields. Rhizosphere, 31, 100951. https://doi.org/https://doi.org/10.1016/j.rhisph.2024.100951
  25. Han, J., Sun, L., Dong, X., Cai, Z., Sun, X., Yang, H., Wang, Y., & Song, W. (2005). Characterization of a novel plant growth-promoting bacteria strain Delftia tsuruhatensis HR4 both as a diazotroph and a potential biocontrol agent against various plant pathogens. Systematic and applied microbiology, 28(1), 66-76.
  26. Inglett, P., Reddy, K., & McCormick, P. (2004). Periphyton chemistry and nitrogenase activity in a northern Everglades ecosystem. Biogeochemistry, 67, 213-233.
  27. Iniesta-Pallarés, M., Álvarez, C., Gordillo-Cantón, F. M., Ramírez-Moncayo, C., Alves-Martínez, P., Molina-Heredia, F. P., & Mariscal, V. (2021). Sustaining rice production through biofertilization with N2-fixing cyanobacteria. Applied Sciences, 11(10), 4628.
  28. Jaggi, W. (1976). Die Bestimmung der CO_2-Bildung als Maβ der bodenbiologischen Aktivitat. Schweiz Landwietschaft Forschung Band, 15(314), 317-380.
  29. Jain, D., Saheewala, H., Sanadhaya, S., Joshi, A., Bhojiya, A. A., Verma, A. K., & Mohanty, S. R. (2022). Potassium solubilizing microorganisms as soil health engineers: An insight into molecular mechanism. In Rhizosphere engineering (pp. 199-214). Elsevier.
  30. Jaiswal, P., Dhar, D. W., Sharma, N., Jain, S., Nehra, P., Singh, B., Singh, Y., & Saxena, S. (2021). Evaluating the role of endophytic cyanobacterial isolates on growth promotion and N/P status of rice crop. Vegetos, 1-7.
  31. Jalali, M., Antoniadis, V., & Najafi, S. (2021). Assessment of trace element pollution in northern and western Iranian agricultural soils: a review. Environmental Monitoring and Assessment, 193, 1-30.
  32. John, D. M., Whitton, B. A., & Brook, A. J. (2002). The freshwater algal flora of the British Isles: An identification guide to freshwater and terrestrial algae. Cambridge University Press.
  33. Jones, J. B. (2001). Laboratory guide for conducting soil tests and plant analysis. CRC press.
  34. Jørgensen, N. O., Brandt, K. K., Nybroe, O., & Hansen, M. (2009). Delftia lacustris sp. nov., a peptidoglycan-degrading bacterium from fresh water, and emended description of Delftia tsuruhatensis as a peptidoglycan-degrading bacterium. International journal of systematic and evolutionary microbiology, 59(9), 2195-2199.
  35. Karageorgiou, K., Paschalis, M., & Anastassakis, G. N. (2007). Removal of phosphate species from solution by adsorption onto calcite used as natural adsorbent. Journal of Hazardous Materials, 139(3), 447-452.
  36. Keeney, D., & Bremner, J. (1966). A chemical index of soil nitrogen availability. Nature, 211(5051), 892-893.
  37. Khosravi, H., Otadi, A., Alikhani, H., & Etesami, H. (2025). Evaluation and Comparative Analysis of Plant Growth-Promoting Traits in Diverse Groups of Rhizosphere Bacteria. Journal of Soil Biology, 12(2), 235-260. (In Persian).
  38. Khumairah, F. H., Setiawati, M. R., Fitriatin, B. N., Simarmata, T., Alfaraj, S., Ansari, M. J., Enshasy, H. A. E., Sayyed, R., & Najafi, S. (2022). Halotolerant plant growth-promoting rhizobacteria isolated from saline soil improve nitrogen fixation and alleviate salt stress in rice plants. Frontiers in microbiology, 13, 905210.
  39. Knudsen, D., Peterson, G., & Pratt, P. (1982). Lithium, sodium, and potassium. Methods of soil analysis: part 2 chemical and microbiological properties, 9, 225-246.
  40. Kouchaki-Penchah, H., Alizadeh, M. R., & Aghamolki, M. T. K. (2023). Measuring eco-efficiency of rice cropping systems in Iran: An integrated economic and environmental approach. Sustainable Energy Technologies and Assessments, 57, 103281.
  41. Leylasi Marand, M., Alikhani, H., Pourbabaee, A. A., & Shariati, S. (2025). Comparison of the plant growth-stimulating ability of epiphyton and epiphyton microbial communities in some rice fields of Guilan province. Journal of Soil Biology. (In Persian).
  42. Liao, X., & Inglett, P. W. (2012). Biological nitrogen fixation in periphyton of native and restored Everglades marl prairies. Wetlands, 32, 137-148.
  43. Liao, X., & Inglett, P. W. (2014). Dynamics of periphyton nitrogen fixation in short-hydroperiod wetlands revealed by high-resolution seasonal sampling. Hydrobiologia, 722, 263-277.
  44. Lightenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350-382.
  45. Liu, Y., Hu, B., & Chu, C. (2023). Toward improving nitrogen use efficiency in rice: Utilization, coordination, and availability. Current Opinion in Plant Biology, 71, 102327.
  46. Lu, H., Liu, J., Kerr, P. G., Shao, H., & Wu, Y. (2017). The effect of periphyton on seed germination and seedling growth of rice (Oryza sativa) in paddy area. Science of the Total Environment, 578, 74-80.
  47. Mahmud, K., Makaju, S., Ibrahim, R., & Missaoui, A. (2020). Current progress in nitrogen fixing plants and microbiome research. Plants, 9(1), 97.
  48. Olsen, S. R. (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture.
  49. Prasanna, R., Adak, A., Verma, S., Bidyarani, N., Babu, S., Pal, M., Shivay, Y. S., & Nain, L. (2015). Cyanobacterial inoculation in rice grown under flooded and SRI modes of cultivation elicits differential effects on plant growth and nutrient dynamics. Ecological Engineering, 84, 532-541.
  50. Prasanna, R., Singh, R. N., Joshi, M., Madhan, K., Pal, R. K., & Nain, L. (2011). Monitoring the biofertilizing potential and establishment of inoculated cyanobacteria in soil using physiological and molecular markers. Journal of Applied Phycology, 23, 301-308.
  51. Prescott, G. W. (1962). Algae of the western Great Lakes. Otto Koeltz Science Publishers, Koenigstein, Germany.
  52. Raheb, A., & Heidari, A. (2012). Effects of clay mineralogy and physico-chemical properties on potassium availability under soil aquic conditions. Journal of Soil Science and Plant Nutrition, 12(4), 747-761.
  53. Reddy, K. R., DeLaune, R. D., & Inglett, P. W. (2022). Biogeochemistry of wetlands: science and applications. CRC press.
  54. Renuka, N., Guldhe, A., Prasanna, R., Singh, P., & Bux, F. (2018). Microalgae as multi-functional options in modern agriculture: current trends, prospects and challenges. Biotechnology advances, 36(4), 1255-1273.
  55. Saadatnia, H., & Riahi, H. (2009). Cyanobacteria from paddy fields in Iran as a biofertilizer in rice plants. Plant, Soil and Environment, 55(5), 207-212.
  56. Saha, S., Bulzu, P.-A., Urajová, P., Mareš, J., Konert, G., Câmara Manoel, J., Macho, M., Ewe, D., Hrouzek, P., & Masojídek, J. (2021). Quorum sensing signals from epibiont mediate the induction of bioactive peptides in mat-forming cyanobacteria Nostoc. BioRxiv, 2021.2004. 2023.441229.
  57. Soares, R. A., Roesch, L. F. W., Zanatta, G., de Oliveira Camargo, F. A., & Passaglia, L. M. P. (2006). Occurrence and distribution of nitrogen fixing bacterial community associated with oat (Avena sativa) assessed by molecular and microbiological techniques. Applied Soil Ecology, 33(3), 221-234.
  58. Su, J., Kang, D., Xiang, W., & Wu, C. (2017). Periphyton biofilm development and its role in nutrient cycling in paddy microcosms. Journal of Soils and Sediments, 17, 810-819.
  59. Tang, A., Haruna, A. O., Majid, N. M. A., & Jalloh, M. B. (2020). Potential PGPR properties of cellulolytic, nitrogen-fixing, phosphate-solubilizing bacteria in rehabilitated tropical forest soil. Microorganisms, 8(3), 442.
  60. Teikari, J. E., Russo, D. A., Heuser, M., Baumann, O., Zedler, J. A., Liaimer, A., & Dittmann, E. (2024). Competition and interdependence define multifaceted interactions of symbiotic Nostoc sp. and Agrobacterium sp. under inorganic carbon limitation. bioRxiv, 2024.2007. 2016.603663.
  61. Towfighi, H. (1998). Study of rice response to potassium fertilizer in paddy soils of northern Iran. Iranian Journal of Agricultural Sciences, 29, 869-883.
  62. Wang, B., Zhou, G., Guo, S., Li, X., Yuan, J., & Hu, A. (2022). Improving Nitrogen Use Efficiency in Rice for Sustainable Agriculture: Strategies and Future Perspectives. Life (Basel), 12(10). https://doi.org/10.3390/life12101653
  63. Weigelhofer, G., Ramião, J. P., Pitzl, B., Bondar-Kunze, E., & O'Keeffe, J. (2018). Decoupled water-sediment interactions restrict the phosphorus buffer mechanism in agricultural streams. Science of the Total Environment, 628, 44-52.
  64. Wu, Y., Liu, J., & Rene, E. R. (2018). Periphytic biofilms: a promising nutrient utilization regulator in wetlands. Bioresource technology, 248, 44-48.
  65. Yaghoubi Khanghahi, M., Pirdashti, H., Rahimian, H., Nematzadeh, G., & Ghajar Sepanlou, M. (2018). Potassium solubilising bacteria (KSB) isolated from rice paddy soil: from isolation, identification to K use efficiency. Symbiosis, 76, 13-23.
  66. Zhang, X., Davidson, E. A., Mauzerall, D. L., Searchinger, T. D., Dumas, P., & Shen, Y. (2015). Managing nitrogen for sustainable development. Nature, 528(7580), 51-59.
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