Abstract
Phosphorus use efficiency (PUE) in paddy fields is low, and this fertilizer has lower availability to rice plants. Recently, the application of periphyton to regulate nutrient elements cycle especially P in paddy fields has received special attention. However, the effects of periphyton as well as phosphate-solubilizing microorganisms (PSM) on rice plant growth, P bioavailability, and its use management in calcareous soils have not been investigated. The aim of this study was to investigate the effects of periphyton and their effective PSM on P bioavailability, rice growth parameters, phosphatase activity, P fractionation, and P fertilizer efficiency in a calcareous soil fertilized or non-fertilized with chemical P fertilizer. The results showed that both natural periphytons and PSM-enriched periphytons decreased water-soluble P concentration at the early stages of rice growth but increased the concentration of water-soluble P and soil available P at the late stage of the plant growth. In periphyton treatments, the average pH of water and soil increased by 0.7 and 3 units, respectively. Periphytons led to an increase in the amount of easily available P species, such as Ca2-P, Ca10-P, and Al-P forms, in the calcareous soil. Periphytons also reduced P fixation in the soil and increased the PUE (2–29%) compared to the treatments without periphyton. The periphytons enriched with PSM showed the highest PUE at different levels of P fertilizer. Periphytons significantly increased rice growth parameters and P concentration in different parts of the rice by increasing soil available P concentration, soil organic matter, and soil acid and alkaline phosphatase activity. The use of periphyton enriched with PSM can increase PUE for rice in paddy fields. It seems that the use of PSM to decompose periphyton biomass and release accumulated P at the late stages of rice growth is the best strategy for using periphytons in paddy fields.
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References
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. https://doi.org/10.1016/j.rhisph.2020.100203
Apha Awwa W (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Work Association, Water Environment Federation, Washington, DC
Arai Y, Sparks D (2007) Phosphate reaction dynamics in soils and soil components: a multiscale approach. Adv Agron 94:135–179. https://doi.org/10.1016/S0065-2113(06)94003-6
Ayaga G, Todd A, Brookes PC (2006) Enhanced biological cycling of phosphorus increases its availability to crops in low-input sub-Saharan farming systems. Soil Biol Biochem 38:81–90. https://doi.org/10.1016/j.soilbio.2005.04.019
Azim M (2009a) Photosynthetic periphyton and surfaces.
Azim M (2009b) Photosynthetic periphyton and surfaces. Encyc Inland Waters:184–191
Bakhshandeh E, Rahimian H, Pirdashti H, Nematzadeh GA (2014) Phosphate solubilization potential and modeling of stress tolerance of rhizobacteria from rice paddy soil in northern Iran. World J Microbiol Biotechnol 30:2437–2447. https://doi.org/10.1007/s11274-014-1669-1
Battin TJ, Kaplan LA, Newbold JD, Hansen CM (2003) Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–442. https://doi.org/10.1038/nature02152
Beheshti M, Alikhani HA, Pourbabaee AA, Etesami H, Rahmani HA, 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
Beheshti M, Alikhani HA, Pourbabaee AA, Etesami H, Rahmani HA, Norouzi 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/10.1016/j.rhisph.2021.100395
Bowes M, Ings N, McCall S, Warwick A, Barrett C, Wickham H, Harman S, Armstrong L, Scarlett P, Roberts C (2012) Nutrient and light limitation of periphyton in the River Thames: implications for catchment management. Sci Total Environ 434:201–212. https://doi.org/10.1016/j.scitotenv.2011.09.082
Cho M, Jang T, Jang JR, Yoon CG (2016) Development of agricultural non-point source pollution reduction measures in Korea. Irrig Drain 65:94–101. https://doi.org/10.1002/ird.1993
Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305. https://doi.org/10.1016/j.gloenvcha.2008.10.009
Crispim M, Vieira A, Coelho S, Medeiros A (2009) Nutrient uptake efficiency by macrophyte and biofilm: practical strategies for small-scale fish farming. AActa Limnol Bras 21:387–391
Díaz-Olarte J, Valoyes-Valois V, Guisande C, Torres NN, González-Bermúdez A, Sanabria-Aranda L, Hernández AMM, Duque SR, Marciales LJ, Nuñez-Avellaneda M (2007) Periphyton and phytoplankton associated with the tropical carnivorous plant Utricularia foliosa. Aquat Bot 87:285–291. https://doi.org/10.1016/j.aquabot.2007.06.010
Dodds WK (2003) The role of periphyton in phosphorus retention in shallow freshwater aquatic systems. J Phycol 39:840–849. https://doi.org/10.1046/j.1529-8817.2003.02081.x
Drake W, Scott JT, Evans-White M, Haggard B, Sharpley A, Rogers CW, Grantz EM (2012) The effect of periphyton stoichiometry and light on biological phosphorus immobilization and release in streams. Limnol 13:97–106. https://doi.org/10.1007/s10201-011-0359-z
Ellwood NT, Di Pippo F, Albertano P (2012) Phosphatase activities of cultured phototrophic biofilms. Water Res 46:378–386. https://doi.org/10.1016/j.watres.2011.10.057
Etesami H (2019) Plant growth promotion and suppression of fungal pathogens in rice (Oryza sativa L.) by plant growth-promoting bacteria. In: Field Crops: Sustainable Management by PGPR. Springer, pp 351–383. https://doi.org/10.1007/978-3-030-30926-8_13
Etesami H (2020) Enhanced phosphorus fertilizer use efficiency with microorganisms. In: Nutrient dynamics for sustainable crop production. Springer, pp 215–245. https://doi.org/10.1007/978-981-13-8660-2_8
Etesami H, Alikhani HA, Hosseini HM (2015) Indole-3-acetic acid (IAA) production trait, a useful screening to select endophytic and rhizosphere competent bacteria for rice growth promoting agents. MethodsX 2:72–78. https://doi.org/10.1016/j.mex.2015.02.008
Garikapati S, Sivasakthivelan P (2013) Studies on the influence of bioinoculant consortium on chillies and its effects on soil health management. Inte J ChemTech Res 5:1326–1328
Holfordi IR, Mattingly GEG (1975) The high-and low-energy phosphate adsorbing surfaces in calcareous soils. J Soil Sci 26:407–417. https://doi.org/10.1111/j.1365-2389.1975.tb01964.x
Igwe CA, Zarei M, Stahr K (2010) Fe and Al oxides distribution in some ultisols and inceptisols of southeastern Nigeria in relation to soil total phosphorus. Environ Earth Sci 60:1103–1111. https://doi.org/10.1007/s12665-009-0254-7
Jiang B, Gu Y (1989) A suggested fractionation scheme of inorganic phosphorus in calcareous soils. Fertil Res 20:159–165. https://doi.org/10.1007/BF01054551
Jones JI, Sayer CD (2003) Does the fish–invertebrate–periphyton cascade precipitate plant loss in shallow lakes? Ecology 84:2155–2167. https://doi.org/10.1890/02-0422
Karageorgiou K, Paschalis M, Anastassakis GN (2007) Removal of phosphate species from solution by adsorption onto calcite used as natural adsorbent. J Hazard Mater 139:447–452. https://doi.org/10.1016/j.jhazmat.2006.02.038
Kasai F (1999) Shifts in herbicide tolerance in paddy field periphyton following herbicide application. Chemosphere 38:919–931. https://doi.org/10.1016/S0045-6535(98)00221-5
Kuo S, Sparks D, Page A, Helmke P, Loeppert R (1996) Phosphorus. Methods of soil analysis. Part 3. Chemical methods. Soil Science Society of America, Inc, American Society of Agronomy, Inc, Madison
Lan Z, Lin X, Wang F, Zhang H, Chen C (2012) Phosphorus availability and rice grain yield in a paddy soil in response to long-term fertilization. Biol Fertil Soils 48:579–588. https://doi.org/10.1007/s00374-011-0650-5
Li J-y, Deng K-y, Cai S-j, Lu H-l, Xu R-k (2020) Periphyton has the potential to increase phosphorus use efficiency in paddy fields. Sci Total Environ 720:137711. https://doi.org/10.1016/j.scitotenv.2020.137711
Liu J, Liu W, Wang F, Kerr P, Wu Y (2016) Redox zones stratification and the microbial community characteristics in a periphyton bioreactor. Bioresour Technol 204:114–121. https://doi.org/10.1016/j.biortech.2016.01.003
Liu J, Lu H, Wu L, Kerr PG, Wu Y (2021) Interactions between periphytic biofilms and dissolved organic matter at soil-water interface and the consequent effects on soil phosphorus fraction changes. Sci Total Environ 801:149708. https://doi.org/10.1016/j.scitotenv.2021.149708
Lu H, Feng Y, Wu Y, Yang L, Shao H (2016a) Phototrophic periphyton techniques combine phosphorous removal and recovery for sustainable salt-soil zone. Sci Total Environ 568:838–844. https://doi.org/10.1016/j.scitotenv.2016.06.010
Lu H, Liu J, Kerr PG, Shao H, Wu Y (2017) The effect of periphyton on seed germination and seedling growth of rice (Oryza sativa) in paddy area. Sci Total Environ 578:74–80. https://doi.org/10.1016/j.scitotenv.2016.07.191
Lu H, Wan J, Li J, Shao H, Wu Y (2016b) Periphytic biofilm: a buffer for phosphorus precipitation and release between sediments and water. Chemosphere 144:2058–2064. https://doi.org/10.1016/j.chemosphere.2015.10.129
MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world’s croplands. Proc Natl Acad Sci 108:3086–3091. https://doi.org/10.1073/pnas.1010808108
Meena VS, Maurya BR, Verma JP, Meena RS (2016) Potassium solubilizing microorganisms for sustainable agriculture. Springer. https://doi.org/10.1007/978-81-322-2776-2
Najafi N, Towfighi H (2012) Effects of rhizosphere of rice plant on the inorganic phosphorus fractions in the paddy soils (in North Iran) following P fertilizer application. Iran J Soil Water Res 43:231–242
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate, vol 939. US Department of Agriculture
Penn CJ, Camberato JJ (2019) A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture 9:120. https://doi.org/10.3390/agriculture9060120
Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339. https://doi.org/10.1016/S0734-9750(99)00014-2
Saikia S, Das D (2009) Potentiality of periphyton-based aquaculture technology in rice-fish environment. Aust J Sci Res 1:624–634. https://doi.org/10.3329/jsr.v1i3.2114
Saikia S, Nandi S, Majumder S (2013) A review on the role of nutrients in development and organization of periphyton. J Res Biol 3:780–788
Sattari SZ, Bouwman AF, Giller KE, van Ittersum MK (2012) Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc Natl Acad Sci 109:6348–6353. https://doi.org/10.1073/pnas.1113675109
Saxena J, Saini A, Ravi I, Chandra S, Garg V (2015) Consortium of phosphate-solubilizing bacteria and fungi for promotion of growth and yield of chickpea (Cicer arietinum). J Crop Improv 29:353–369. https://doi.org/10.1080/15427528.2015.1027979
Shafqat MN, Pierzynski GM (2014) The Freundlich adsorption isotherm constants and prediction of phosphorus bioavailability as affected by different phosphorus sources in two Kansas soils. Chemosphere 99:72–80. https://doi.org/10.1016/j.chemosphere.2013.10.009
Shen J, Li R, Zhang F, Fan J, Tang C, Rengel Z (2004a) Crop yields, soil fertility and phosphorus fractions in response to long-term fertilization under the rice monoculture system on a calcareous soil. Field Crop Res 86:225–238. https://doi.org/10.1016/j.fcr.2003.08.013
Shen J, Tang C, Rengel Z, Zhang F (2004b) Root-induced acidification and excess cation uptake by N2-fixing Lupinus albus grown in phosphorus-deficient soil. Plant and Soil 260:69–77. https://doi.org/10.1023/B:PLSO.0000030172.10414.e6
Shujie C, Kaiying D, Jun T, Rui S, Hailong L, Jiuyu L, Yonghong W, Renkou X (2021) Characterization of extracellular phosphatase activities in periphytic biofilm from paddy field. Pedosphere 31:116–124. https://doi.org/10.1016/S1002-0160(20)60061-3
Singh GT, Erik NN (2002) Rhizosphere research: a tool for creating phosphorus efficient crop varieties. WCSS 1270:1–15
Singhania R, Goswami N (1978) Transformation of applied phosphorus under simulated conditions of growing rice and wheat in a sequence. J Ind Soc Soil Sci 26:193–197
Su J, Kang D, Xiang W, Wu C (2017) Periphyton biofilm development and its role in nutrient cycling in paddy microcosms. J Soil Sediment 17:810–819. https://doi.org/10.1007/s11368-016-1575-2
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Tiessen H, Moir J (1993) Characterization of available P by sequential extraction. Soil Sampling and Methods of Analysis. Ed MR Carter, pp 75–86
Tiwari K (2001) Phosphorus needs of Indian soils and crops. Better Crop Inte 15:6
Ulloa M, Nunes-Nesi A, da Fonseca-Pereira P, Poblete-Grant P, Reyes-Díaz M, Cartes P (2021) The effect of silicon supply on photosynthesis and carbohydrate metabolism in two wheat (Triticum aestivum L.) cultivars contrasting in response to phosphorus nutrition. Plant Physiol Biochem 169:236–248. https://doi.org/10.1016/j.plaphy.2021.11.022
Vadeboncoeur Y, Steinman AD (2002) Periphyton function in lake ecosystems. Scientific World J 2:1449–1468. https://doi.org/10.1100/tsw.2002.294
Viruel E, Lucca ME, Siñeriz F (2011) Plant growth promotion traits of phosphobacteria isolated from Puna, Argentina. Arch Microbiol 193:489–496. https://doi.org/10.1007/s00203-011-0692-y
Wang Y, Zhao X, Wang L, Zhao P-H, Zhu W-B, Wang S-Q (2016) Phosphorus fertilization to the wheat-growing season only in a rice–wheat rotation in the Taihu Lake region of China. Field Crop Res 198:32–39. https://doi.org/10.1016/j.fcr.2016.08.025
Weigelhofer G, Ramião JP, Pitzl B, Bondar-Kunze E, O’Keeffe J (2018) Decoupled water-sediment interactions restrict the phosphorus buffer mechanism in agricultural streams. Sci Total Environ 628:44–52. https://doi.org/10.1016/j.scitotenv.2018.02.030
Williams CH (1950) Studies on soil phosphorus. I. A method for the partial fractionation of soil phosphorus. J Agric Sci 40:233–242. https://doi.org/10.1017/S0021859600045895
Wu Y, Liu J, Lu H, Wu C, Kerr P (2016) Periphyton: an important regulator in optimizing soil phosphorus bioavailability in paddy fields. Environ Sci Pollut Res 23:21377–21384. https://doi.org/10.1007/s11356-016-7363-0
Wu Y, Liu J, Rene ER (2018) Periphytic biofilms: a promising nutrient utilization regulator in wetlands. Bioresour Technol 248:44–48. https://doi.org/10.1016/j.biortech.2017.07.081
Wu Y, Xia L, Yu Z, Shabbir S, Kerr PG (2014) In situ bioremediation of surface waters by periphytons. Bioresour Technol 151:367–372. https://doi.org/10.1016/j.biortech.2013.10.088
Yang J, Tang C, Wang F, Wu Y (2016) Co-contamination of Cu and Cd in paddy fields: using periphyton to entrap heavy metals. J Hazard Mater 304:150–158. https://doi.org/10.1016/j.jhazmat.2015.10.051
Yang X, Lu X (2014) Drastic change in China’s lakes and reservoirs over the past decades. Sci Rep 4:1–10. https://doi.org/10.1038/srep06041
Zhao Y, Chen X, Xiong X, Wu C (2019) Capture and release of phosphorus by periphyton in closed water systems influenced by illumination and temperature. Water 11:1021. https://doi.org/10.3390/w11051021
Zhou Q, Zhu Y (2003) Potential pollution and recommended critical levels of phosphorus in paddy soils of the southern Lake Tai area, China. Geoderma 115:45–54. https://doi.org/10.1016/S0016-7061(03)00074-0
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Alikhani, H.A., Beheshti, M., Pourbabaee, A.A. et al. Phosphorus Use Management in Paddy Fields by Enriching Periphyton with Its Phosphate-Solubilizing Bacteria and Fungi at the Late Stage of Rice Growth. J Soil Sci Plant Nutr 23, 1896–1912 (2023). https://doi.org/10.1007/s42729-023-01145-2
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DOI: https://doi.org/10.1007/s42729-023-01145-2