Selecting Phosphorus-Solubilizing Strains of Purple Nonsulfur Bacteria Isolated From Pineapple Cultivated Acid Sulfate Soils

https://doi.org/10.55230/mabjournal.v53i2.2881

Authors

  • Tran Ngoc Huu Faculty of Crop Science, College of Agriculture, Can Tho University, Vietnam
  • Ha Ngoc Thu Can Tho University
  • Nguyen Huynh Minh Anh Faculty of Crop Science, College of Agriculture, Can Tho University, Vietnam
  • Nguyen Duc Trong Faculty of Crop Science, College of Agriculture, Can Tho University, Vietnam
  • Tran Chi Nhan An Giang University; Vietnam National University Ho Chi Minh City, Vietnam
  • Le Thi My Thu Faculty of Crop Science, College of Agriculture, Can Tho University, Vietnam
  • Ly Ngoc Thanh Xuan An Giang University; Vietnam National University Ho Chi Minh City, Vietnam
  • Le Thanh Quang Faculty of Crop Science, College of Agriculture, Can Tho University, Vietnam
  • Nguyen Quoc Khuong Faculty of Crop Science, College of Agriculture, Can Tho University, Vietnam

Keywords:

Acid sulfate soil, phosphorus, pineapple, purple nonsulfur bacteria

Abstract

The presence of acid sulfate soils is such an obstacle for pineapple cultivation in Vietnam due to their low pH, high toxicity and poor nutrient availability, especially phosphorus (P), which is immobilized by cations in the soils. Therefore, the study occurred to select purple nonsulfur bacteria (PNSB) strains that can solubilize P under toxic and acidic conditions. There were 33 strains that can tolerate the acidic condition, and they were selected and tested for viability and P solubilization under conditions containing Al3+, Fe2+, and Mn2+ toxins. Four strains, including W15, W39, W42 and W48 suffered from growth inhibition by Al3+, Fe2+ and Mn2+ less than the other strains under both microaerobic light and aerobic dark conditions (ML and AD conditions). In addition, there were four strains (W15, W25, W42 and W48) solubilizing Al-P well (21.4-25.2 mg L-1), two strains (W23 and W42) solubilizing Fe-P well (15.9-17.3 mg L-1), and two strains (W17 and W42) solubilizing Ca-P well (23.0-36.4 mg L-1) under both ML and AD conditions. Ultimately, there were five strains selected (W17, W23, W25, W42 and W48) and identified as Rhodopseudomonas palustris strain W17 and W23, Cereibacter sphaeroides strain W23, W42 and W48 based on the 16S rRNA technique. The selected strains also produced ALA, EPS and siderophores at 1.31-2.19 mg L-1, 0.78-1.89 mg L-1, and 16.2-55.6%, respectively. Therefore, these strains were promising in providing nutrients for pineapples in the form of biofertilizer.

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References

Agegnehu, G., Amede, T., Erkossa, T., Yirga, C., Henry, C., Tyler, R. & Sileshi, G.W. 2021. Extent and management of acid soils for sustainable crop production system in the tropical agroecosystems: A review. Acta Agriculturae Scandinavica, Section B Soil and Plant Science, 71(9): 852-869.

Alyousif, N.A. 2022. Review of genetic analysis and mechanisms of phosphate solubilization by phosphate solubilizing bacteria. Marsh Bulletin, 17(1): 8-21.

Andriesse, W. & Van Mensvoort, M.E.F. 2002. Acid sulfate soils, distribution and extent. In: Encyclopedia of Soil Science. R. Lal (Eds.). CRC Press, Boca Raton. pp. 6.

Babu-Khan, S., Yeo, T.C., Martin, W.L., Duron, M.R., Rogers, R.D. & Goldstein, A.H. 1995. Cloning of a mineral phosphate-solubilizing gene from Pseudomonas cepacia. Applied and Environmental Microbiology, 61(3): 972-978.

Barrow, N.J. &, & Hartemink, A.E. 2023. The effects of pH on nutrient availability depend on both soils and plants. Plant and Soil, 487: 21-37.

Basu, A. & Phale, P.S. 2006. Inducible uptake and metabolism of glucose by the phosphorylative pathway in Pseudomonas putida CSV86. FEMS Microbiology Letters, 259(2): 311-316.

Batool, K. & Rehman, Y. 2017. Arsenic-redox transformation and plant growth promotion by purple nonsulfur bacteria Rhodopseudomonas palustris CS2 and Rhodopseudomonas faecalis SS5. BioMed Research International, 2017: 6250327.

Brown, J.W. 2013. Enrichment and isolation of purple non-sulfur bacteria. Department of Biological Sciences, College of Sciences, North Carolina State University. http://www.mbio.ncsu.edu/mb452/purple_nonsulfurs/purples.html

Burnham, B. F. 1970. [14] δ-Aminolevulinic acid synthase (Rhodopseudomonas spheroides). In: Methods in Enzymology. H. Tabor & C.W Tabor (Eds.). Academic Press. 17: 195-200.

Chen, X., Yan, X., Wang, M., Cai, Y., Weng, X., Su, D. & Zhang, F. 2022. Long-term excessive phosphorus fertilization alters soil phosphorus fractions in the acidic soil of pomelo orchards. Soil and Tillage Research, 215: 105214.

Dhuldhaj, U.P. & Malik, N. 2022. Global perspective of phosphate solubilizing microbes and phosphatase for improvement of soil, food and human health. Cellular, Molecular and Biomedical Reports, 2(3): 173-186.

Dziwornu, A.K., Shrestha, A., Matthus, E., Ali, B., Wu, L. B. & Frei, M. 2018. Responses of contrasting rice genotypes to excess manganese and their implications for lignin synthesis. Plant Physiology and Biochemistry, 123: 252-259.

Elhaissoufi, W., Ghoulam, C., Barakat, A., Zeroual, Y. & Bargaz, A. 2022. Phosphate bacterial solubilization: A key rhizosphere driving force enabling higher P use efficiency and crop productivity. Journal of Advanced Research, 38: 13-28.

Fanning, D.S., Rabenhorst, M.C., Balduff, D.M., Wagner, D.P., Orr, R.S. & Zurheide, P.K. 2010. An acid sulfate perspective on landscape/seascape soil mineralogy in the U.S. Mid-Atlantic region. Geoderma, 154(3-4): 457-464.

Ferreira, M.L., Casabuono, A.C., Stacchiotti, S.T., Couto, A.S., Ramirez, S.A. & Vullo, D.L. 2017. Chemical characterization of Pseudomonas veronii 2E soluble exopolymer as Cd (II) ligand for the biotreatment of electroplating wastes. International Biodeterioration and Biodegradation, 119: 605-613.

Fu, J., Leo, C.P. & Show, P.L. 2022. Recent advances in the synthesis and applications of pH-responsive CaCO3. Biochemical Engineering Journal, 187: 108446.

Gerónimo, E. & Aparicio, V.C. 2022. Changes in soil pH and addition of inorganic phosphate affect glyphosate adsorption in agricultural soil. European Journal of Soil Science, 73(1): e13188.

Ghosh, S., Bhattacharya, J., Nitnavare, R. & Webster, T.J. 2022. Microbial remediation of metals by marine bacteria. In: Development in Wastewater Treatment Research and Processes. S. Rodriguez-Couto & M.P. Shah (Eds.). Elsevier. pp. 131-158.

Gondal, A.H., Hussain, I., Ijaz, A.B., Zafar, A., Ch, B.I., Zafar, H. & Tariq, M. 2021. Influence of soil pH and microbes on mineral solubility and plant nutrition: A review. International Journal of Agriculture and Biological Sciences, 5(1): 71-81.

Hamdali, H., Bouizgarne, B., Hafidi, M., Lebrihi, A., Virolle, M.J. & Ouhdouch, Y. 2008. Screening for rock phosphate solubilizing Actinomycetes from Moroccan phosphate mines. Applied Soil Ecology, 38(1): 12-19.

Holland, J.E., Bennett, A.E., Newton, A.C., White, P.J., McKenzie, B.M., George, T.S. & Hayes, R.C. 2018. Liming impacts on soils, crops and biodiversity in the UK: A review. Science of the Total Environment, 610: 316-332.

Hulisz, P., Michalski, A., Boman, A., Dąbrowski, M. & Kwasowski, W. 2020. Identification of potential acid sulfate soils at the Reda River mouth (northern Poland) using pH measurements. Soil Science Annual, 71(2): 53-61.

Huu , T.N., Nhan, T.C., Xuan, L.N.T., Thu, L.T.M., Trong, N.D., Thu, H.N., Ngan, N.T., Quang, L.T., Khuong, N.Q. 2024. Selection for nitrogen-providing purple nonsulfur bacteria from acid sulfate soil that grows pineapple. Malaysian Journal of Microbiology. Under review

Kang, S.M., Imran, M., Shaffique, S., Kwon, E.H., Park, Y.S. & Lee, I.J. 2022. Growth and photosynthetic characteristics of sesame seedlings with gibberellin-producing Rhodobacter sphaeroides SIR03 and biochar. International Journal of Plant Biology, 13(3): 257-269.

Kar, D., Pradhan, A.A. & Datta, S. 2021. The role of solute transporters in aluminum toxicity and tolerance. Physiologia Plantarum, 171(4): 638-652.

Khan, M.S., Zaidi, A. & Wani, P.A. 2009. Role of phosphate solubilizing microorganisms in sustainable agriculture-a review. In: Sustainable agriculture. E. Lichtfouse, M. Navarrete, P. Debaeke, S. Véronique & C. Alberola (Eds). Springer, Dordrecht. pp. 551-570.

Khuong, N.Q., Kantachote, D., Onthong, J. & Sukhoom, A. 2017. The potential of acid-resistant purple nonsulfur bacteria isolated from acid sulfate soils for reducing toxicity of Al3+ and Fe2+ using biosorption for agricultural application. Biocatalysis and Agricultural Biotechnology, 12: 329-340.

Khuong, N.Q., Kantachote, D., Onthong, J., Xuan, L.N.T. & Sukhoom, A. 2018. Enhancement of rice growth and yield in actual acid sulfate soils by potent acid-resistant Rhodopseudomonas palustris strains for producing safe rice. Plant and Soil, 429: 483-501.

Khuong, N.Q., Kantachote, D., Thuc, L.V., Nookongbut, P., Xuan, L.N.T., Nhan, T.C., Xuan, N.T.T. & Tantirungkij, M. 2020a. Potential of Mn2+ -resistant purple nonsulfur bacteria isolated from acid sulfate soils to act as bioremediators and plant growth promoters via mechanisms of resistance. Journal of Soil Science and Plant Nutrition, 20: 2364-2378.

Khuong, N.Q., Kantachote, D., Nookongbut, P., Onthong, J., Xuan, L.N.T. & Sukhoom, A. 2020b. Mechanisms of acid-resistant Rhodopseudomonas palustris strains to ameliorate acidic stress and promote plant growth. Biocatalysis and Agricultural Biotechnology, 24: 101520.

Khuong, N.Q., Huu, T.N., Thuc, L.V., Thu, L.T.M., Xuan, D.T., Quang, L.T., Nhan, T.C., Tran, H.N., Tien, P.D., Xuan, L.N.T. & Kantachote, D. 2021. Two strains of Luteovulum sphaeroides (purple nonsulfur bacteria) promote rice cultivation in saline soils by increasing available phosphorus. Rhizosphere, 20: 100456.

Khuong, N.Q., Kantachote, D., Thuc, L.V., Huu, T.N., Nhan, T.C., Nguyen, P.C., Thu, L.T. M., Van, T.T.B., Xuan, N.T.T., Xuan, L.N.T. & Xuan, D.T. 2022. Use of potent acid resistant strains of Rhodopseudomonas spp. in Mn-contaminated acidic paddies to produce safer rice and improve soil fertility. Soil and Tillage Research, 221: 105393.

Khuong, N.Q., Kantachote, D., Dung, N.T.T., Huu, T.N., Thuc, L.V., Thu, L.T.M., Quang, L.T., Xuan, D.T., Nhan, T.C., Tien, P.D. & Xuan, L.N.T. 2023a. Potential of potent purple nonsulfur bacteria isolated from rice-shrimp systems to ameliorate rice (Oryza sativa L.) growth and yield in saline acid sulfate soil. Journal of Plant Nutrition, 46(3): 473-494.

Khuong, N.Q., Thuc, L.V., Giang, C.T., Xuan, L.N.T., Thu, L.T.M., Isao, A. & Jun-Ichi, S. 2023b. Improvement of nutrient uptake, yield of black sesame (Sesamum indicum L.), and alluvial soil fertility in dyke by spent rice straw from mushroom cultivation as biofertilizer containing potent strains of Rhodopseudomonas palustris. The Scientific World Journal, 2023: 1954632.

Khuong, N.Q., Thuc, L.V., Quang, L.T., Huu, T.N., Xuan, D.T., Dac, H.H., Xuan, L.N.T. & Thu, L.T.M. 2023c. Effects of biofertilizer supplementation, Rhodopseudomonas spp., on nitrogen and phosphorus uptakes, growth, and yield of sesame (Sesamum indicum L.) on salt-affected soil. Journal of Plant Nutrition, 41(1): 1-17.

Khuong, N.Q., Sakpirom, J., Oanh, T.O., Thuc, L.V., Thu, L.T.M., Xuan, D.T., Quang, L.T. & Xuan, L.N.T. 2023d. Isolation and characterization of novel potassium-solubilizing purple nonsulfur bacteria from acidic paddy soils using culture-dependent and culture-independent techniques. Brazilian Journal of Microbiology, 54: 2333-2348.

Khuong, N.Q., Trong, N.D., Quang, L.T., Xuan, L.N.T., & Phong, N.T. 2024. The potency of a liquid biofertilizer containing bacterial strains of Rhodopseudomonas spp. on recovery of soil properties damaged by Al3+ and Fe2+ toxins and enhancement of rice yield in acid sulfate soil. International Journal of Phytoremediation, 1-11.

Lee, S.K. & Dang, T.A. 2019. Spatio-temporal variations in meteorology drought over the Mekong River Delta of Vietnam in the recent decades. Paddy and Water Environment, 17(1): 35-44.

Lo, K.J., Lin, S.S., Lu, C.W., Kuo, C.H. & Liu, C.T. 2018. Whole-genome sequencing and comparative analysis of two plant-associated strains of Rhodopseudomonas palustris (PS3 and YSC3). Scientific Reports, 8(1): 12769.

Loc, H.H., Van Binh, D., Park, E., Shrestha, S., Dung, T.D., Son, V.H., Truc, N.H.T., Mai, N.P. & Seijger, C. 2021. Intensifying saline water intrusion and drought in the Mekong Delta: From physical evidence to policy outlooks. Science of the Total Environment, 757: 143919.

Lopes, L.D., Hao, J. & Schachtman, D.P. 2021. Alkaline soil pH affects bulk soil, rhizosphere and root endosphere microbiomes of plants growing in a Sandhills ecosystem. FEMS Microbiology Ecology, 97(4): 1028.

Murphy, J. & Riley, J.P. 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Cchimica Aacta, 27: 31-36.

Nannipieri, P., Giagnoni, L., Landi, L. & Renella, G. 2011. Role of phosphatase enzymes in soil. In: Phosphorus in Action. E. Bünemann, A. Oberson, E. Frossard (Eds.). Springer, Berlin, Heidelberg. pp. 215-243.

Nguyen, K.Q., Kantachote, D., Onthong, J. & Sukhoom, A. 2018. Al3+ and Fe2+ toxicity reduction potential by acid-resistant strains of Rhodopseudomonas palustris isolated from acid sulfate soils under acidic conditions. Annals of Microbiology, 68(4): 217-228.

Nookongbut, P., Kantachote, D., Khuong, N.Q., Sukhoom, A., Tantirungkij, M. & Limtong, S. 2019. Selection of acid-resistant purple nonsulfur bacteria from peat swamp forests to apply as biofertilizers and biocontrol agents. Journal of Soil Science and Plant Nutrition, 19: 488-500.

Peng, Y., Sun, Y., Fan, B., Zhang, S., Bolan, N. S., Chen, Q. & Tsang, D.C. 2021. Fe/Al (hydr)oxides engineered biochar for reducing phosphorus leaching from a fertile calcareous soil. Journal of Cleaner Production, 279: 123877.

Perez, E., Sulbaran, M., Ball, M.M. & Yarzabal, L.A. 2007. Isolation and characterization of mineral phosphate-solubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region. Soil Biology and Biochemistry, 39(11): 2905-2914.

Richardson, A.E. & Simpson, R.J. 2011. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiology, 156(3): 989-996.

Rodriguez, H., Fraga, R., Gonzalez, T. & Bashan, Y. 2006. Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant and Soil, 287: 15-21.

Rose, T.J. & Wissuwa, M. 2012. Rethinking internal phosphorus utilization efficiency: A new approach is needed to improve PUE in grain crops. Advances in Agronomy, 116: 185-217.

Sade, H., Meriga, B., Surapu, V., Gadi, J., Sunita, M.S.L., Suravajhala, P. & Kishor, P.K. 2016. Toxicity and tolerance of aluminum in plants: Tailoring plants to suit to acid soils. Biometals, 29(2): 187-210.

Sadiq, A.A. & Babagana, U. 2012. Influence of lime materials to ameliorate acidity on irrigated paddy fields: A review. Academic Research International 3(1): 413-420.

Sharma, S.B., Sayyed, R.Z., Trivedi, M.H. & Gobi, T.A. 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus, 2: 587.

Siddique, R., Gul, A., Ozturk, M. & Altay, V. 2021. Phosphate solubilizing bacteria for soil sustainability. In: Handbook of assisted and amendment: enhanced sustainable remediation technology. M.N.V Prasad (Eds.). John Wiley & Sons. pp. 423-435.

Sulbarán, M., Pérez, E., Ball, M.M., Bahsas, A. & Yarzábal, L.A. 2009. Characterization of the mineral phosphate-solubilizing activity of Pantoea aglomerans MMB051 isolated from an iron-rich soil in southeastern Venezuela (Bolivar state). Current Microbiology, 58: 378-383.

Sundar, L.S. & Chao, Y.Y. 2022. Potential of purple non-sulfur bacteria in sustainably enhancing the agronomic and physiological performances of rice. Agronomy, 12(10): 2347.

Suzuki, Y., Kelly, S.D., Kemner, K.M. & Banfield, J.F. 2003. Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment. Applied and Environmental Microbiology, 69(3): 1337-1346.

Timofeeva, A., Galyamova, M. & Sedykh, S. 2022. Prospects for using phosphate-solubilizing microorganisms as natural fertilizers in agriculture. Plants, 11(16): 2119.

Tri, L.V. & van Mensvoort, M.E.F. 2004. Decision trees for farm management on acid sulfate soils, Mekong Delta, Viet Nam. Soil Research, 42(6): 671-684.

Wan, W., Hao, X., Xing, Y., Liu, S., Zhang, X., Li, X. & Huang, Q. 2021. Spatial differences in soil microbial diversity caused by pH-driven organic phosphorus mineralization. Land Degradation and Development, 32(2): 766-776.

Wei, T.T., Fan, X.B. & Quan, Z.X. 2023. Abyssibius alkaniclasticus gen. nov., sp. nov., a novel member of the family Rhodobacteraceae, isolated from the Mariana Trench. International Journal of Systematic and Evolutionary Microbiology, 73(2): 005715.

Yi, Y., Huang, W. & Ge, Y. 2008. Exopolysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World Journal of Microbiology and Biotechnology, 24: 1059-1065.

Published

30-06-2024 — Updated on 04-07-2024

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Huu, T. N., Thu, H. N., Anh, N. H. M., Trong, N. D., Nhan, T. C., Thu, L. T. M., Xuan, L. N. T., Quang, L. T., & Khuong, N. Q. (2024). Selecting Phosphorus-Solubilizing Strains of Purple Nonsulfur Bacteria Isolated From Pineapple Cultivated Acid Sulfate Soils. Malaysian Applied Biology, 53(2), 114–124. https://doi.org/10.55230/mabjournal.v53i2.2881 (Original work published June 30, 2024)

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