Plasma Chemistry and Plasma Processing

, Volume 39, Issue 1, pp 1–19 | Cite as

Plasma Activated Organic Fertilizer

  • David B. Graves
  • Lars B. Bakken
  • Morten B. Jensen
  • Rune Ingels
Original Paper


Improved utilization of organic waste for fertilizer has significant worldwide economic and ecological potential and the use of plasma can help unlock this potential. Organic waste that are used as fertilizer includes animal waste (manure and urine), human sewage, food waste and biogas digestate. Air plasma treatment of aqueous solutions of organic fertilizer (plasma activated organic fertilizer, or PAOF) has multiple advantages such as reduction or elimination of atmospheric emission of volatile organic carbon (VOC) compounds, CH\({_4}\) and NH\({_3}\). Although the emission of N\(_2\mathrm{O}\) from the fertilized soil may be enhanced by PAOF, we surmise that N\(_2\mathrm{O}\) emission at large is reduced because the losses of reactive nitrogen from the agro-ecosystem (which cause N\(_2\mathrm{O}\) emissions elsewhere) are significantly reduced. In addition, PAOF will improve the commercial value of fertilizer that can be made from organic waste. This includes altering both the quantity and chemical form of N contained in the organic fertilizer, as well as odor reduction. PAOF appears to function using chemical reactivity similar to well-studied natural antimicrobial processes, resulting in significant antibacterial effects in treated waste. The commercial viability of PAOF depends on numerous factors, the most important of which are the energy efficiency and capital costs associated with the plasma process and associated processing equipment; the cost of electricity; and the nature and extent of government regulations regarding pollution from organic waste and all types of fertilizer. We estimate that if the total cost of plasma production of reactive nitrogen is below about €2/kg N–€3/kg N, the process will be economically viable in the absence of penalties or subsidies.


Plasma agriculture Organic fertilizer Plasma activated water 



DBG gratefully acknowledges partial support from US Department of Energy OFES Grant DE-SC0001934 and US National Science Foundation Grant 1606062.


  1. 1.
    Schlter O, Ehlbeck J, Hertel C, Habermeyer M, Roth A, Engel K-H, Holzhauser T, Knorr D, Eisenbrand G (2013) Opinion on the use of plasma processes for treatment of foods. Mol Nutr Food Res 57(5):920–927CrossRefGoogle Scholar
  2. 2.
    Ohta T (2016) Plasma in agriculture. In: Misra NN, Schlüter O, Cullen PJ (eds) Cold plasma in food and agriculture. Elsevier, Amsterdam, pp 205–221CrossRefGoogle Scholar
  3. 3.
    Puač N, Gherardi M, Shiratani M (2018) Plasma agriculture: a rapidly emerging field. Plasma Processes Polym 15(2):1700174CrossRefGoogle Scholar
  4. 4.
    Pankaj SK, Bueno-Ferrer C, Misra NN, Milosavljević V, O’Donnell CP, Bourke P, Keener KM, Cullen PJ (2014) Applications of cold plasma technology in food packaging. Trends Food Sci Technol 35(1):5–17CrossRefGoogle Scholar
  5. 5.
    Pankaj SK, Keener KM (2018) Cold plasma processing of fruit juices. In: Rajauria G, Tiwari BK (eds) Fruit juices. Elsevier, pp 529–537Google Scholar
  6. 6.
    Shaw A, Shama G, Iza F (2015) Emerging applications of low temperature gas plasmas in the food industry. Biointerphases 10(2):029402CrossRefGoogle Scholar
  7. 7.
    Noriega E, Shama G, Laca A, Daz M, Kong MG (2011) Cold atmospheric gas plasma disinfection of chicken meat and chicken skin contaminated with Listeria innocua. Food Microbiol 28(7):1293–1300CrossRefGoogle Scholar
  8. 8.
    Frhling A, Durek J, Schnabel U, Ehlbeck J, Bolling J, Schlter O (2012) Indirect plasma treatment of fresh pork: decontamination efficiency and effects on quality attributes. Innov Food Sci Emerg Technol 16:381–390CrossRefGoogle Scholar
  9. 9.
    Fernndez A, Thompson A (2012) The inactivation of Salmonella by cold atmospheric plasma treatment. Food Res Int 45(2):678–684CrossRefGoogle Scholar
  10. 10.
    Yong HI, Park J, Kim H-J, Jung S, Park S, Lee HJ, Choe W, Jo C (2018) An innovative curing process with plasma-treated water for production of loin ham and for its quality and safety. Plasma Process Polym 15(2):1700050CrossRefGoogle Scholar
  11. 11.
    Wang RX, Nian WF, Wu HY, Feng HQ, Zhang K, Zhang J, Zhu WD, Becker KH, Fang J (2012) Atmospheric-pressure cold plasma treatment of contaminated fresh fruit and vegetable slices: inactivation and physiochemical properties evaluation. Eur Phys J D 66(10):276CrossRefGoogle Scholar
  12. 12.
    Tappi S, Berardinelli A, Ragni L, Dalla Rosa M, Guarnieri A, Rocculi P (2014) Atmospheric gas plasma treatment of fresh-cut apples. Innov Food Sci Emerg Technol 21:114–122CrossRefGoogle Scholar
  13. 13.
    Misra NN, Patil S, Moiseev T, Bourke P, Mosnier JP, Keener KM, Cullen PJ (2014) In-package atmospheric pressure cold plasma treatment of strawberries. J Food Eng 125:131–138CrossRefGoogle Scholar
  14. 14.
    Baier M, Foerster J, Schnabel U, Knorr D, Ehlbeck J, Herppich WB, Schlter O (2013) Direct non-thermal plasma treatment for the sanitation of fresh corn salad leaves: evaluation of physical and physiological effects and antimicrobial efficacy. Postharvest Biol Technol 84:81–87CrossRefGoogle Scholar
  15. 15.
    Ponraj SB, Sharp JA, Kanwar JR, Sinclair AJ, Kviz L, Nicholas KR, Dai XJ (2017) Argon gas plasma to decontaminate and extend shelf life of milk. Plasma Processes Polym 14(11):1600242CrossRefGoogle Scholar
  16. 16.
    Yannam SK, Estifaee P, Rogers S, Thagard SM (2018) Application of high voltage electrical discharge plasma for the inactivation of Escherichia coli ATCC 700891 in tangerine juice. LWT 90:180–185CrossRefGoogle Scholar
  17. 17.
    Dobrin D, Magureanu M, Mandache NB, Ionita M-D (2015) The effect of non-thermal plasma treatment on wheat germination and early growth. Innov Food Sci Emerg Technol 29:255–260CrossRefGoogle Scholar
  18. 18.
    Zhou R, Zhou R, Zhang X, Zhuang J, Yang S, Bazaka K, Ostrikov KK (2016) Effects of atmospheric-pressure N2, He, Air, and O2 microplasmas on mung bean seed germination and seedling growth. Sci Rep 6(1):32603CrossRefGoogle Scholar
  19. 19.
    Sarinont T, Amano T, Koga K, Shiratani M, Hayashi N (2015) Multigeneration effects of plasma irradiation to seeds of arabidopsis thaliana and Zinnia on their growth. In: MRS Proceedings, p 1723Google Scholar
  20. 20.
    Ji S-H, Choi K-H, Pengkit A, Im JS, Kim JS, Kim YH, Park Y, Hong EJ, Jung S, Choi E-H, Park G (2016) Effects of high voltage nanosecond pulsed plasma and micro DBD plasma on seed germination, growth development and physiological activities in spinach. Arch Biochem Biophys 605:117–128CrossRefGoogle Scholar
  21. 21.
    Koga K, Thapanut S, Amano T, Seo H, Itagaki N, Hayashi N, Shiratani M (2016) Simple method of improving harvest by nonthermal air plasma irradiation of seeds of Arabidopsis thaliana (L.). Appl Phys Express 9(1):016201CrossRefGoogle Scholar
  22. 22.
    Randeniya LK, de Groot GJJB (2015) Non-thermal plasma treatment of agricultural seeds for stimulation of germination, removal of surface contamination and other benefits: a review: non-thermal plasma treatment of agricultural seeds. Plasma Process Polym 12(7):608–623CrossRefGoogle Scholar
  23. 23.
    Panngom K, Lee SH, Park DH, Sim GB, Kim YH, Uhm HS, Park G, Choi EH (2014) Non-thermal plasma treatment diminishes fungal viability and up-regulates resistance genes in a plant host. PLoS ONE 9(6):e99300CrossRefGoogle Scholar
  24. 24.
    Siddique SS, Hardy GESJ, Bayliss KL (2018) Cold plasma: a potential new method to manage postharvest diseases caused by fungal plant pathogens. Plant Pathol 67(5):1011–1021CrossRefGoogle Scholar
  25. 25.
    Stryczewska HD, Ebihara K, Takayama M, Gyoutoku Y, Tachibana M (2005) Non-thermal plasma-based technology for soil treatment. Plasma Process Polym 2(3):238–245CrossRefGoogle Scholar
  26. 26.
    Mitsugi F, Abiru T, Ikegami T, Ebihara K, Aoqui S-I, Nagahama K (2016) Influence of ozone generated by surface barrier discharge on nematode and plant growth. IEEE Trans Plasma Sci 44(12):3071–3076CrossRefGoogle Scholar
  27. 27.
    Malik MA, Ghaffar A, Malik SA (2001) Water purification by electrical discharges. Plasma Sour Sci Technol 10(1):82–91CrossRefGoogle Scholar
  28. 28.
    Burlica R, Kirkpatrick MJ, Finney WC, Clark RJ, Locke BR (2004) Organic dye removal from aqueous solution by glidarc discharges. J Electrost 62(4):309–321CrossRefGoogle Scholar
  29. 29.
    Jiang G, Yuan Z (2013) Synergistic inactivation of anaerobic wastewater biofilm by free nitrous acid and hydrogen peroxide. J Hazard Mater 250–251:91–98CrossRefGoogle Scholar
  30. 30.
    Merouani DR, Abdelmalek F, Taleb F, Martel M, Semmoud A, Addou A (2015) Plasma treatment by gliding arc discharge of dyes/dye mixtures in the presence of inorganic salts. Arab J Chem 8(2):155–163CrossRefGoogle Scholar
  31. 31.
    Magureanu M, Mandache NB, Parvulescu VI (2015) Degradation of pharmaceutical compounds in water by non-thermal plasma treatment. Water Res 81:124–136CrossRefGoogle Scholar
  32. 32.
    Utsumi F, Kajiyama H, Nakamura K, Tanaka H, Mizuno M, Ishikawa K, Kondo H, Kano H, Hori M, Kikkawa F (2013) Effect of indirect nonequilibrium atmospheric pressure plasma on anti-proliferative activity against chronic chemo-resistant ovarian cancer cells in vitro and in vivo. PLoS ONE 8(12):e81576CrossRefGoogle Scholar
  33. 33.
    Kurake N, Tanaka H, Ishikawa K, Kondo T, Sekine M, Nakamura K, Kajiyama H, Kikkawa F, Mizuno M, Hori M (2016) Cell survival of glioblastoma grown in medium containing hydrogen peroxide and/or nitrite, or in plasma-activated medium. Arch Biochem Biophys 605:102–108CrossRefGoogle Scholar
  34. 34.
    Bruggeman PJ, Kushner MJ, Locke BR, Gardeniers JGE, Graham WG, Graves DB, Hofman-Caris RCHM, Maric D, Reid JP, Ceriani E, Fernandez Rivas D, Foster JE, Garrick SC, Gorbanev Y, Hamaguchi S, Iza F, Jablonowski H, Klimova E, Kolb J, Krcma F, Lukes P, Machala Z, Marinov I, Mariotti D, Mededovic Thagard S, Minakata D, Neyts EC, Pawlat J, Lj Petrovic Z, Pflieger R, Reuter S, Schram DC, Schrter S, Shiraiwa M, Tarabov B, Tsai PA, Verlet JRR, von Woedtke T, Wilson KR, Yasui K, Zvereva G (2016) Plasma-liquid interactions: a review and roadmap. Plasma Sources Sci Technol 25(5):053002CrossRefGoogle Scholar
  35. 35.
    Lukes P, Dolezalova E, Sisrova I, Clupek M (2014) Aqueous-phase chemistry and bactericidal effects from an air discharge plasma in contact with water: evidence for the formation of peroxynitrite through a pseudo-second-order post-discharge reaction of \(\text{ H }_{2}\text{ O } _{2}\) and \(\text{ HNO }_{2}\). Plasma Sources Sci Technol 23(1):015019CrossRefGoogle Scholar
  36. 36.
    Doubla A, Abdelmalek F, Khe LIFA K, ADDOU A, BRISSET JL (2003) Post-discharge plasma-chemical oxidation of Iron(II) complexes. J Appl Electrochem 33:73–77CrossRefGoogle Scholar
  37. 37.
    Oehmigen K, Hhnel M, Brandenburg R, Wilke C, Weltmann K-D, von Woedtke T (2010) The role of acidification for antimicrobial activity of atmospheric pressure plasma in liquids. Plasma Process Polym 7(3–4):250–257CrossRefGoogle Scholar
  38. 38.
    Oehmigen K, Winter J, Hhnel M, Wilke C, Brandenburg R, Weltmann K-D, von Woedtke T (2011) Estimation of possible mechanisms of escherichia coli inactivation by plasma treated sodium chloride solution. Plasma Process Polym 8(10):904–913CrossRefGoogle Scholar
  39. 39.
    Naitali M, Kamgang-Youbi G, Herry J-M, Bellon-Fontaine M-N, Brisset J-L (2010) Combined effects of long-living chemical species during microbial inactivation using atmospheric plasma-treated water. Appl Environ Microbiol 76(22):7662–7664CrossRefGoogle Scholar
  40. 40.
    Traylor MJ, Pavlovich MJ, Karim S, Hait P, Sakiyama Y, Clark DS, Graves DB (2011) Long-term antibacterial efficacy of air plasma-activated water. J Phys D Appl Phys 44(47):472001CrossRefGoogle Scholar
  41. 41.
    Machala Z, Tarabova B, Hensel K, Spetlikova E, Sikurova L, Lukes P (2013) Formation of ROS and RNS in water electro-sprayed through transient spark discharge in air and their bactericidal effects: formation of ROS/RNS in water sprayed through spark in air. Plasma Process Polym 10(7):649–659CrossRefGoogle Scholar
  42. 42.
    Jablonowski H, von Woedtke T (2015) Research on plasma medicine-relevant plasma-liquid interaction: What happened in the past five years? Clin Plasma Med 3(2):42–52CrossRefGoogle Scholar
  43. 43.
    Brisset J-L, Pawlat J (2016) Chemical effects of air plasma species on aqueous solutes in direct and delayed exposure modes: discharge, post-discharge and plasma activated water. Plasma Chem Plasma Process 36(2):355–381CrossRefGoogle Scholar
  44. 44.
    Peng L, Boehm D, Bourke P, Cullen PJ (2017) Achieving reactive species specificity within plasma-activated water through selective generation using air spark and glow discharges. Plasma Process Polym 14(8):1600207CrossRefGoogle Scholar
  45. 45.
    Julk J, Hujacov A, Scholtz V, Khun J, Holada K (2018) Contribution to the chemistry of plasma-activated water. Plasma Phys Rep 44(1):125–136CrossRefGoogle Scholar
  46. 46.
    Thirumdas R, Kothakota A, Annapure U, Siliveru K, Blundell R, Gatt R, Valdramidis VP (2018) Plasma activated water (PAW): chemistry, physico-chemical properties, applications in food and agriculture. Trends Food Sci Technol 77:21–31CrossRefGoogle Scholar
  47. 47.
    Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87(1):315–424CrossRefGoogle Scholar
  48. 48.
    Koppenol WH (2001) 100 Years of peroxynitrite chemistry and 11 years of peroxynitrite biochemistry. Redox Rep 6(6):339–341CrossRefGoogle Scholar
  49. 49.
    Molina C, Kissner R, Koppenol WH (2013) Decomposition kinetics of peroxynitrite: influence of pH and buffer. Dalton Trans 42(27):9898CrossRefGoogle Scholar
  50. 50.
    Castellani AG, Niven CF Jr (1955) Factors affecting the bacteriostatic action of sodium nitrite. Appl Microbiol 3(3):154–159Google Scholar
  51. 51.
    Jiang G, Gutierrez O, Yuan Z (2011) The strong biocidal effect of free nitrous acid on anaerobic sewer biofilms. Water Res 45(12):3735–3743CrossRefGoogle Scholar
  52. 52.
    Weller R, Price RJ, Ormerod AD, Benjamin N, Leifert C (2001) Antimicrobial effect of acidified nitrite on dermatophyte fungi, Candida and bacterial skin pathogens. J Appl Microbiol 90(4):648–652CrossRefGoogle Scholar
  53. 53.
    Lundberg JO, Weitzberg E, Gladwin MT (2008) The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7(2):156–167CrossRefGoogle Scholar
  54. 54.
    Lobachev VL, Rudakov ES (2006) The chemistry of peroxynitrite. Reaction mechanisms and kinetics. Russian Chem Rev 75(5):375–396CrossRefGoogle Scholar
  55. 55.
    Shen J, Tian Y, Li Y, Ma R, Zhang Q, Zhang J, Fang J (2016) Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci Rep 6(1):28505CrossRefGoogle Scholar
  56. 56.
    Kissner R, Koppenol WH (2002) Product distribution of peroxynitrite decay as a function of pH, temperature, and concentration. J Am Chem Soc 124(2):234–239CrossRefGoogle Scholar
  57. 57.
    Ingels R, Graves DB (2015) Improving the efficiency of organic fertilizer and nitrogen use via air plasma and distributed renewable energy. Plasma Med 5(2–4):257–270CrossRefGoogle Scholar
  58. 58.
    Smil V (2001) Enriching the earth: Fritz Haber, Carl Bosch, and the transformation of world food production. MIT Press, CambridgeGoogle Scholar
  59. 59.
    Smil V (2002) Nitrogen and food production: proteins for human diets. AMBIO: A J Hum Environ 31(2):126–131CrossRefGoogle Scholar
  60. 60.
    Steffen W, Richardson K, Rockstrom J, Cornell SE, Fetzer I, Bennett EM, Biggs R, Carpenter SR, de Vries W, de Wit CA, Folke C, Gerten D, Heinke J, Mace GM, Persson LM, Ramanathan V, Reyers B, Sorlin S (2015) Planetary boundaries: guiding human development on a changing planet. Science 347(6223):1259855–1259855CrossRefGoogle Scholar
  61. 61.
    Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Jack Cosby B (2003) The nitrogen cascade. BioScience 53(4):341CrossRefGoogle Scholar
  62. 62.
    Sutton MA (ed) Our nutrient world: the challenge to produce more food and energy with less pollution ; [global overview on nutrient management]. Centre for Ecology & Hydrology, Edinburgh, 2013. OCLC: 854698050Google Scholar
  63. 63.
    Fangueiro D, Hjorth M, Gioelli F (2015) Acidification of animal slurry: a review. J Environ Manag 149:46–56CrossRefGoogle Scholar
  64. 64.
    Cherkasov N, Ibhadon AO, Fitzpatrick P (2015) A review of the existing and alternative methods for greener nitrogen fixation. Chem Eng Process Process Intensif 90:24–33CrossRefGoogle Scholar
  65. 65.
    Wang W, Patil B, Heijkers S, Hessel V, Bogaerts A (2017) Nitrogen fixation by gliding arc plasma: better insight by chemical kinetics modelling. ChemSusChem 10(10):2145–2157CrossRefGoogle Scholar
  66. 66.
    Birkeland KR (1906) On the oxidation of atmospheric nitrogen in electric arcs. Trans Faraday Soc 2(December):98CrossRefGoogle Scholar
  67. 67.
    Bakken LR, Frostegrd SA (2017) Sources and sinks for N \(_{2}\) O, can microbiologist help to mitigate N \(_{2}\) O emissions?: Sources and sinks for N \(_{2}\) O. Environ Microbiol 19(12):4801–4805CrossRefGoogle Scholar
  68. 68.
    Hink L, Nicol GW, Prosser JI (2017) Archaea produce lower yields of \(\text{ N }_{2}\text{ O }\) than bacteria during aerobic ammonia oxidation in soil: \(\text{ N }_{2}\text{ O }\) production by soil ammonia oxidisers. Environ Microbiol 19(12):4829–4837CrossRefGoogle Scholar
  69. 69.
    Liu B, Frostegard A, Bakken LR (2014) Impaired reduction of N2o to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ. MBio 5(3):e01383–14CrossRefGoogle Scholar
  70. 70.
    Veltoff GL, Oenema O (1993) Nitrous oxide flux from nitric acid treated cattle slurry applied to grassland under semi-controlled conditions. Neth J Agric Sci 41:81–93Google Scholar
  71. 71.
    Crutzen PJ, Mosier AR, Smith KA, Winiwarter W (2008) N2o release from agro-biofuel production negates global warming reduction by replacing fossil fuels. Atmos Chem Phys 7(4):11191–11205CrossRefGoogle Scholar
  72. 72.
  73. 73.
    Graves DB (2012) The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J Phys D Appl Phys 45(26):263001CrossRefGoogle Scholar
  74. 74.
    von Woedtke T, Metelmann H-R, Weltmann K-D (2014) Clinical plasma medicine: state and perspectives of in vivo application of cold atmospheric plasma: clinical plasma medicine: state and perspectives of in vivo application of cold atmospheric plasma. Contrib Plasma Phys 54(2):104–117CrossRefGoogle Scholar
  75. 75.
    Misra NN, Schlüter O, Cullen PJ (eds) (2016) Plasma in food and agriculture. In: Cold plasma in food and agriculture. Elsevier, pp 1–16Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • David B. Graves
    • 1
  • Lars B. Bakken
    • 2
  • Morten B. Jensen
    • 3
  • Rune Ingels
    • 3
  1. 1.Department of Chemical and Biomolecular EngineeringUniversity of CaliforniaBerkeleyUSA
  2. 2.Department of Plant and Environmental SciencesNorwegian University of Life SciencesAsNorway
  3. 3.N2AppliedOsloNorway

Personalised recommendations