Skip to main content

Advertisement

Log in

Acidithiobacillus thiooxidans IW16 and Sulfur Synergistically with Struvite Aggrandize the Phosphorus Bioavailability to Wheat in Alkaline Soil

  • Original Paper
  • Published:
Journal of Soil Science and Plant Nutrition Aims and scope Submit manuscript

Abstract

Environmentally hazardous wastewaters from various origins could prove an impending source for phosphorus (P) recovery as struvite. This study aimed to employ an eco-friendly approach for P utilization from struvite, and to neutralize its alkaline effect in the soil through supplementation of sulfur-oxidizing bacteria (SOB) Acidithiobacillus thiooxidans IW16. Struvite precipitated and recovered from wastewater was tested for P release and bioavailability to grow wheat in alkaline soil under greenhouse conditions. Treatments were control (no P application), P from single superphosphate (SSP) fertilizer, P from struvite, P from struvite + sulfur (100 mg kg−1 of soil), and P from rock phosphate; and all these treatments were compared with and without SOB inoculation through irrigation water. Struvite application, especially with sulfur and/or SOB, maintained an adequate P level (as with SSP fertilizer) in both wheat plants and soil throughout the growing period. Wheat plant agronomic attributes were also improved with struvite as for SSP fertilization. Moreover, supplementation of SOB inoculum with struvite and other P sources significantly improved the P bioavailability and crop yield through increased phosphate solubility in alkaline soil. In conclusion, inoculation of SOB especially with sulfur (S) supplementation in struvite treatment caused the pH reduction of alkaline soil through S oxidation (H2SO4 formation), which solubilized the fixed-P in struvite as well as soil and thus improved P bioavailability to wheat plants. These findings strengthen the concept of struvite scavenging from wastewater for environmental safety, and to introduce it as an alternative resource for P fertilization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdel-Fattah MS, Abd-El-Khader AA (2004) Nitrification rate in a clay soil as influenced by some N-sources, sulfur and organic matter application. Egypt J Sci 44(1):19–26

  • Abdel-Fattah MA, Raheed MA, Shafei AM (2005) Phosphorus availability as influenced by different application rates of elemental sulfur to soils. Egypt J Soil Sci 45(2):199–208

    CAS  Google Scholar 

  • Ackerman JN, Zvomuya F, Cicek N, Flaten D (2013) Evaluation of manure-derived struvite as a phosphorus source for canola. Can J Plant Sci 93:419–424

    Article  CAS  Google Scholar 

  • Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum L.). Int J Agri Biol 10:85–88

  • Antonini S, Arias MA, Eichert T, Clemens J (2012) Greenhouse evaluation and environmental impact assessment of different urine-derived struvite fertilizers as phosphorus sources for plants. Chemosphere 89:1202–1210

    Article  CAS  PubMed  Google Scholar 

  • APHA (2005) Standard methods for the examination of water and waste water, 21st edn. American Public Health Association, Washington

  • APHA (2012) Standard methods for the examination of water and waste water, 22nd edn. American Public Health Association, Washington, DC

  • Ara I, Islam MS, Kashem MA, Osman KT (2018) A comparative study of phosphorus availability in an acidic soil and an alkaline soil amended with organic and inorganic phosphorus sources. J Soil Sci Plant Nutr 18(2):466–478

    CAS  Google Scholar 

  • Arai Y, Sparks DL (2007) Phosphate reaction dynamics in soils and soil components: a multiscale approach. In D. Sparks (Ed.). Adv Agron 94:135–179

    Article  CAS  Google Scholar 

  • Aria MM, Lakzian A, Haghnia GH, Berenji AR, Besharati H, Fotovat A (2010) Effect of Thiobacillus, sulfur, and vermicompost on the water-soluble phosphorus of hard rock phosphate. Bioresour Technol 101:551–554

    Article  CAS  PubMed  Google Scholar 

  • Besharati H, Atashnama K, Hatami S (2007) Bio super as a phosphate fertilizer in a calcareous soil with low available phosphorus. Afr J Biotechnol 6(11):1325–1329

    CAS  Google Scholar 

  • Bhatti TM, Yawar W (2010) Bacterial solubilization of phosphorus from phosphate rock containing sulfur mud. Hydrometallurgy 103:54–59

    Article  CAS  Google Scholar 

  • Bridger GL, Salutsky ML, Starostka RW (1962) Micronutrient sources, metal ammonium phosphates as fertilizers. J Agric Food Chem 10:181–188

    Article  CAS  Google Scholar 

  • Cabeza R, Steingrobe B, Romer W, Claasen N (2011) Effectiveness of recycled P products as P fertilizers, as evaluated in pot experiments. Nutr Cycl Agroecosyst 91:173–184

    Article  CAS  Google Scholar 

  • Chapman HD, Pratt FP (1961) Ammonium vanadate-molybdate method for determination of phosphorus. In: Methods of Analysis for Soils, Plants and Water, 1st edn. California University, Agriculture Division 184-203.

  • Cottenie A (1980) Soil and Plant Testing as a Basis of Fertilizer Recommendations. FAO Soil Bulletin 38/2. Food and Agriculture Organization of the United Nations, Rome

  • Dalecha T, Assefa E, Krasteva K, Langergraber G (2012) Experiments on struvite precipitation, application and economic analysis in Arba Minch, Ehtiopia. In: Project Report Under Capacity-Linked Water Supply and Sanitation Improvement for Africa’s Peri urban and Rural Area, International Water Association

  • Desmidt E, Ghyselbrecht K, Monballiu A, Rabaey K, Verstraete W, Meesschaert BD (2013) Factors influencing urease driven struvite precipitation. Sep Purif Technol 110:150–157

    Article  CAS  Google Scholar 

  • Desmidt E, Ghyselbrecht K, Zhang Y, Pinoy L, Van der Bruggen B, Verstraete W, Rabaey K, Meesschaert B (2015) Global phosphorus scarcity and full-scale P-recovery techniques: a review. Crit Rev Environ Sci Technol 45:336–384

    Article  CAS  Google Scholar 

  • El-Assiouty FMM, Abo-Sedra SA (2005) Effect of bio and chemical fertilizers on seed production and quality of spinach (Spinicia aleracea L.). Int J Agric Bio 7(6):947–952

    Google Scholar 

  • Eman AE, Taalab ASM (2004) Dragonhead plants (Dracocephalum moldavica L.) responses to salt stress and different sources of sulfur. Egypt J Appl Sci 19(5):239–257

  • Estefan G, Sommer R, Ryan J (2013) Methods of Soil, Plant, and Water Analysis: A manual for the West Asia and North Africa Region. Beirut: ICARDA

  • Forrest AL, Fattah KP, Mavinic DS, Koch FA (2008) Optimizing struvite production for phosphate recovery in WWTP. J Environ Eng 134:395–402

    Article  CAS  Google Scholar 

  • Ganrot Z, Dave G, Nilsson E (2007) Recovery of N and P from human urine by freezing, struvite precipitation and adsorption to zeolite and active carbon. Bioresour Technol 98:3112–3121

    Article  CAS  PubMed  Google Scholar 

  • Gell K, Ruijter FJ, Kuntke P, Graaff M, Smit AL (2011) Safety and effectiveness of struvite from black water and urine as a phosphorus fertilizer. J Agric Sci 3:67–80

    Google Scholar 

  • Gilbert N (2009) Environment: the disappearing nutrient. Nature 461:716–718

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Ponce R, Garcıa-Lopez-de-Sa ME (2007) Evaluation of struvite as a fertilizer: a comparison with traditional P sources. Agro-chimica 51:301–308

    CAS  Google Scholar 

  • Gonzalez-Ponce R, Lopez-de-Sa EG, Plaza C (2009) Lettuce response to phosphorus fertilization with struvite recovered from municipal wastewater. Hort Sci 44:426–430

  • Huang H, Zhang D, Guom G, Jiang Y, Wang M, Zhang P, Jing L (2018) Dolomite application for the removal of nutrients from synthetic swine wastewater by a novel combined electrochemical process. Chem Eng J 335:665–675

    Article  CAS  Google Scholar 

  • Imtiaz M, Shah KH, Khan P, Siddiqui SH, Memon MY, Aslam M (2003) Response of wheat genotype ‘SI-91195’ to increasing N and P levels and their ratios under agro-climatic conditions of Sindh. Pak J Soil Sci 22:58–63

    Google Scholar 

  • Johnston AE, Richards IR (2003) Effectiveness of different precipitated phosphates as phosphorus sources for plants. Soil Use Manag 19:45–49

    Article  Google Scholar 

  • Kandil H, El-Halfawi MH, Ibrahim SA (2011) Influence of elemental sulfur and/or inoculation with sulfur oxidizing bacteria on growth, and nutrient content of sorghum plants grown on different soils. Factori şi Procese Pedogenetice din Zona Temperată 10:13–27

    Google Scholar 

  • Kataki S, West H, Clarke BDC (2016) Phosphorus recovery as struvite: recent concerns for use of seed, alternative Mg source, nitrogen conservation and fertilizer potential. Resour Conserv Recycl 107:142–156

  • Kim JH, An BM, Lim DH, Park JY (2018) Electricity production and phosphorus recovery as struvite from synthetic wastewater using magnesium-air fuel cell electrocoagulation. Water Res 132:200–210

    Article  PubMed  CAS  Google Scholar 

  • Kozik A, Hutnik N, Piotrowski K, Mazienczuk A, Matynia A (2013) Precipitation and crystallization of struvite from synthetic wastewater under stoichiometric conditions. Adv Chem Eng Sci 3:20–26

    Article  CAS  Google Scholar 

  • Latifian M, Liu J, Mattiasson B (2012) Struvite-based fertilizer and its physical and chemical properties. Environ Technol 33:2691–2697

    Article  CAS  PubMed  Google Scholar 

  • Le Corre KS, Valsami-Jones E, Hobbs P, Parsons SA (2009) Phosphorus recovery from wastewater by struvite crystallization: a review. Crit Rev Environ Sci Technol 39:433–477

    Article  CAS  Google Scholar 

  • Li XZ, Zhao QL (2002) MAP precipitation from landfill leachate and sea water bittern waste. Environ Technol 23:989–1000

    Article  CAS  PubMed  Google Scholar 

  • Li XZ, Zhao QL (2003) Recovery of ammonium-nitrogen from landfill leachate as a multi-nutrient fertilizer. Ecol Eng 20:171–181

    Article  Google Scholar 

  • Li B, Irina B, Wei Y, Hai MH, Tajammal M, Guang QW, Brent RY (2018) Phosphorous recovery through struvite crystallization: challenges for future design. Sci Total Environ 648:1244–1256

    Article  PubMed  CAS  Google Scholar 

  • Liu YH, Kumar S, Kwang JH, Kim JH, Kim JD, Ra CS (2011) Recycle of electrolytically dissolved struvite as an alternative to enhance phosphate and nitrogen recovery from swine wastewater. J Hazard Mater 195:175–181

    Article  CAS  PubMed  Google Scholar 

  • Ma BL, Yan W, Dwyer LM, Fregeau-Reid J, Voldeng HD, Dion Y, Nass H (2004) Graphic analysis of genotypes, environment, nitrogen fertilizer and their interaction on spring wheat yield. J Agron 96:169–180

    Article  Google Scholar 

  • Magda AH, Wafa HM, Naseem MG, Adal Hediya OA (2007) Effect of nitrogen fertilization and sulfur application on the growth and chemical composition of Jerusalem artichoke (Helianthus tuberosus) grown in Lacustrine soil. Arab Conference of Soil and Water Management for Sustainable Agricultural Development 10–11 April 2007, Fac of Agric. Mansoura University

  • Massey MS, Davis JG, Sheffield RE, Ippolito JA (2007) Struvite production from dairy wastewater and its potential as a fertilizer for organic production in calcareous soils. In: Proceedings of International Symposium on Air Quality and Waste Management for Agriculture, Colorado, USA

    Google Scholar 

  • Massey MS, Davis JG, Ippolito JA, Sheffield RE (2009) Effectiveness of recovered magnesium phosphates as fertilizers in neutral and slightly alkaline soils. J Agron 101:323–329

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Degryse F, da Silva RC, Baird R (2015) Co-granulated elemental sulfur/sulfate fertilizers and their role in crop nutrition. Better Crops with Plant Food 99:7–10

    Google Scholar 

  • Michałowska-Kaczmarczyk AM, Michałowski T (2014) Evaluation of transition points between different solid phases in aqueous media. J Anal Sci Meth Instrum 4:87–94

    Google Scholar 

  • Michałowska-Kaczmarczyk AM, Michałowski T, Toporek M, Pietrzyk A (2015) Solubility and dissolution in terms of generalized approach to electrolytic systems principles. J Anal Sci Meth Instrum 5:47–58

    Google Scholar 

  • Muhmood A, Shubiao W, Jiaxin L, Zeeshan A, Hongzhen L, Renjie D (2018) Nutrient recovery from anaerobically digested chicken slurry via struvite: performance optimization and interactions with heavy metals and pathogens. Sci Total Environ 635:1–9

    Article  CAS  PubMed  Google Scholar 

  • Mutumba FA, Zagal E, Gerding M, Castillo-Rosales D, Paulino L, Schoebitz M (2018) Plant growth promoting rhizobacteria for improved water stress tolerance in wheat genotypes. J Soil Sci Plant Nutr 18(4):1080–1096

    CAS  Google Scholar 

  • Negrea A, Lupa L, Negrea P, Ciopec M, Muntean C (2010) Simultaneous removal of ammonium and phosphate ions from wastewaters and characterization of the resulting product. Chem Bull Politechnica Univ (Timisoara), Ser Chem Environ Eng 55(69):136–142

    Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keey DR (eds). Methods of soil analysis part 2 Am Soc Agron No 9 Wisconsin USA, pp 403-427

  • Pokorna D, Zabranska J (2015) Sulfur-oxidizing bacteria in environmental technology. Biotechnol Adv 33:1246–1259

  • Pastor L, Marti N, Bouzas A, Seco A (2008) Sewage sludge management for phosphorus recovery as struvite in EBPR wastewater treatment plants. Bioresour Technol 99:4817–4824

    Article  CAS  PubMed  Google Scholar 

  • Perez RC, Steingrobe B, Romer W, Claassen N (2009) Plant availability of P fertilizers recycled from sewage sludge and meat-and-bone meal in field and pot experiments. In: Proceedings of International Conference on Nutrient Recovery from Wastewater Streams, International Water Association, British Columbia, Canada

    Google Scholar 

  • Pizzol M, Smart JCR, Thomsen M (2014) External costs of cadmium emissions to soil: a drawback of phosphorus fertilizers. J Clean Prod 84:475–483

    Article  CAS  Google Scholar 

  • Plaza C, Sanz R, Clemente C, Fernandez JM, Gonzalez R, Polo A, Colmenarejo MF (2007) Greenhouse evaluation of struvite and sludges from municipal wastewater treatment works as phosphorus sources for plants. J Agric Food Chem 55:8206–8212

    Article  CAS  PubMed  Google Scholar 

  • Prater J (2014) Improved production of magnesium ammonium phosphate (struvite) from landfill leachate. Final Report. Solid Waste Research Program, University of Wisconsin System

  • Rafie SE, Hawash S, Shalaby MS (2013) Evaluation of struvite precipitated from chemical fertilizer industrial effluents. Adv Appl Sci Res 4:113–123

    Google Scholar 

  • Rahman MM, Liu YH, Kwag JH, Ra CS (2011) Recovery of struvite from animal wastewater and its nutrient leaching loss in soil. J Hazard Mater 186:2026–2030

    Article  CAS  PubMed  Google Scholar 

  • Rasul GAM, Esmail AO, Mekha RJ (2011) The role of magnesium in increasing of phosphorus fertilizer efficiency and wheat yield. Mesopot J Agric 39:33–39

    Google Scholar 

  • Reinhard C, Planavsky N, Gill BC, Ozaki K, Robbins L, Lyons TW, Fischer WW, Wang C, Cole DB, Konhauser K (2017) Evolution of the global phosphorus cycle. Nature 541:386–389

    Article  CAS  PubMed  Google Scholar 

  • Ryan J, Ibrikci H, Singh M, Matar A, Masri S, Rashid A, Pala M (2008) Response to residual and currently applied phosphorus in dryland cereal/legume rotations in three Syrian Mediterranean agro ecosystems. Eur J Agric 28:126–137

    Article  CAS  Google Scholar 

  • Shu L, Schneider P, Jegatheesan V, Johnsonan J (2006) An economic evaluation of phosphorus recovery as struvite from digester supernatant. Bioresour Technol 97:2211–2216

    Article  CAS  PubMed  Google Scholar 

  • Simons J (2008) Eignung nährstoffreicher Substrate aus zentraler und dezentraler Abwasserbehandlung als Düngemittel (The use of substrates from centralized and decentralized treatment systems as fertilizers). Universitäts- undLandesbibliothek, Bonn

    Google Scholar 

  • Soliman SS, Abo-Sedra SA, El-Soubaty MR (2006) Improvement in the growth, productivity and fruit quality of Maghrabi banana by biofertilizer application. Egypt J Soil Sci 46(3):201–215

    Google Scholar 

  • Stamford NP, Santos PR, Moura AM, Santos CES, Freitas ADS (2003) Biofertilizer with natural phosphate, sulphur and Acidithiobacillus in a soil with low available-P. Sci Agric 60:767–773

    Article  CAS  Google Scholar 

  • Steel RGD, Torrie JH, Dicky DA (1997) Principles and Procedures of Statistics. A Biometrical Approach, 3rd edn. McGraw-Hill Co Inc, New York, pp 400–428

  • Tang K, Baskaran V, Nemati M (2009) Bacteria of the sulphur cycle: an overview of microbiology, biokinetics and their role in petroleum and mining industries. Biochem Eng J 44:73–94

    Article  CAS  Google Scholar 

  • Ullah I, Jilani G, Haq MI, Khan A (2013) Enhancing bio-available phosphorous in soil through sulfur oxidation by Thiobacilli. Brit Microbiol Res J 3:378–392

    Article  Google Scholar 

  • Uysal A, Kuru B (2015) The fertilizer effect of struvite recovered from dairy industry wastewater on the growth and nutrition of maize plant. Fresenius Environ Bull 24(10):3155–3162

  • Uysal A, Demir S (2013) Struvite pyro lysate recycling for removing ammonium from baker’s yeast industry wastewater. In: Proceedings of International Conference on Environment Science and Technology, Turkey

  • Uysal A, Yilmazel YD, Demirer GN (2010) The determination of fertilizer quality of the formed struvite from effluent of a sewage sludge anaerobic digester. J Hazard Mater 181:248–254

    Article  CAS  PubMed  Google Scholar 

  • Uysal A, Demir S, Sayilgan E, Eraslan F, Kucukyumuk Z (2014) Optimization of struvite fertilizer formation from baker’s yeast wastewater: growth and nutrition of maize and tomato plants. Environ Sci Pollut Res 21:3264–3274

    Article  CAS  Google Scholar 

  • Villar-Mir JM, Claudio-stocckle PV, Ferrer F, Aran M (2002) On farm monitoring of soil nitrate nitrogen in irrigated cornfields in the Ebro Valley (Northeast Spain). Agron J 94:373–380

    Article  Google Scholar 

  • Wang J, Song Y, Yuan P, Peng J, Fan M (2006) Modelling the crystallization of magnesium ammonium phosphate for phosphorus recovery. Chemosphere 65:1182–1187

    Article  CAS  PubMed  Google Scholar 

  • Wei SP, van Rossum F, Gerrit JP, Mari-Karoliina HW (2018) Recovery of phosphorus and nitrogen from human urine by struvite precipitation, air stripping and acid scrubbing: a pilot study. Chemosphere 212:1030–1037

    Article  CAS  PubMed  Google Scholar 

  • Westerman PW (2009) Phosphorus recovery from concentrated wastewater with a continuous-flow struvite crystallizer. National Pork Board

  • Yang ZH, Stoven K, Haneklaus S, Singh BR, Schnug E (2010) Elemental sulfur oxidation by Thiobacillus spp. and aerobic heterotrophic sulfur-oxidizing Bacteria. Pedosphere 20(1):71–79

    Article  Google Scholar 

  • Yavuz B, Türkey M, Engin CO (2007) Autotrophic removal of sulfide from industrial wastewaters using oxygen and nitrate as electron acceptors. Environ Eng Sci 24:457–470

    Article  CAS  Google Scholar 

  • Yetilmezsoy K, Sapci-Zengin Z (2009) Recovery of ammonium nitrogen from the effluent of UASB treating poultry manure wastewater by MAP precipitation as a slow release fertilizer. J Hazard Mater 166(1):260–269

    Article  CAS  PubMed  Google Scholar 

  • Yetilmezsoy K, Sertyesilisik B, Kocak E, Sapci-Zengin Z (2009) Ameliorative effect of different doses of MgNH4PO4·6H2O precipitate recovered from the effluent of UASB treating poultry manure wastewater: growth of Lolium perenne. J Food Agric Environ 7:823–831

    CAS  Google Scholar 

  • Yetilmezsoy K, Turkdogan-Aydinol FI, Gunay A, Ozis I (2011) Post treatment of poultry slaughterhouse wastewater and appraisal of the economic outcome. Environ Eng Manag J 10(11):1635–1645

    Article  CAS  Google Scholar 

  • Yetilmezsoy K, Turkdogan FI, Gunay A, Yilmaz T, Kaleli M (2013) Medicinal plants grown in soil amended with struvite recovered from anaerobically pre-treated poultry manure wastewater. J Anim Plant Sci 23:261–270

    CAS  Google Scholar 

  • Yetilmezsoy K, Ilhan F, Emel K, Havva MA (2017) Feasibility of struvite recovery process for fertilizer industry: a study of financial and economic analysis. J Clean Prod 152:88–102

    Article  CAS  Google Scholar 

  • Zhang DM, Chen YX, Jilani G, Wu WX, Liu WL, Han ZY (2012) Optimization of struvite crystallization protocol for pre-treating the swine wastewater and its impact on subsequent anaerobic biodegradation of pollutants. Bioresour Technol 116:386–396

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Degryse F, Gupta V, McLaughlin MJ (2015) Elemental sulphur oxidation in Australian cropping soils. Soil Sci Soc Am J 79:89–96. https://doi.org/10.2136/sssaj2014.08.0314

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I acknowledge the Institute of Soil Science, PMAS Arid Agriculture University Rawalpindi, Pakistan for all the lab and technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ahmad Khan or Dongmei Zhang.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, A., Jilani, G., Zhang, D. et al. Acidithiobacillus thiooxidans IW16 and Sulfur Synergistically with Struvite Aggrandize the Phosphorus Bioavailability to Wheat in Alkaline Soil. J Soil Sci Plant Nutr 20, 95–104 (2020). https://doi.org/10.1007/s42729-019-00104-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42729-019-00104-0

Keywords

Navigation