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Potential application of glycerol in the production of plant beneficial microorganisms

  • Fermentation, Cell Culture and Bioengineering - Review
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

This review highlights the importance of research for development of biofertilizer and biocontrol products based on the use of glycerol for further process scale-up to industrial microbiology. Glycerol can be used successfully in all stages of production of plant beneficial microorganisms. It serves as an excellent substrate in both submerged and solid-state fermentation processes with free and immobilized microbial cells. Glycerol is also one of the most attractive formulation agents that ensures high cell density and viability including in harsh environmental conditions. Future research is discussed to make this inexpensive material a base for industrial production of plant beneficial microorganisms.

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References

  1. Ali RM, Elfeky SS, Abbas H (2008) Response of salt stressed Ricinus communis L. to exogenous application of glycerol and/or aspartic acid. J Biol Sci 8:171–175

    Article  CAS  Google Scholar 

  2. Alotaibi KD, Schoenau JJ (2011) Enzymatic activity and microbial biomass in soil amended with biofuel production byproducts. Appl Soil Ecol 48:227–235

    Article  Google Scholar 

  3. Amaral PFF, Ferreira TF, Fontes GC, Coelho MAZ (2009) Glycerol valorization: new biotechnological routes. Food Bioprod Proc 87:179–186

    Article  CAS  Google Scholar 

  4. Anandham R, Choi KH, Indira Gandhi P, Yim WJ, Park SJ, Kim KA, Madhaiyan M, Sa TM (2007) Evaluation of shelf life and rock phosphate solubilization of Burkholderia sp. in nutrient-amended clay, rice bran and rock phosphate-based granular formulation. World J Microbiol Biotechnol 23:1121–1129

    Article  CAS  Google Scholar 

  5. Anonymous (2011) Uses of glycerine. The Glycrine Producers’ Association, London, UK. (http://www.aciscience.org/docs/Uses of Glycerine.pdf). Accessed 6 May 2016

  6. Arias A, Martinez-Drets G (1976) Glycerol metabolism in Rhizobium. Can J Microbiol 22:150–153

    Article  CAS  PubMed  Google Scholar 

  7. Bashan Y, Trejo A, de-Bashan LE (2011) Development of two culture media for mass cultivation of Azospirillum spp. and for production of inoculants to enhance plant growth. Biol Fertil Soils 47:963–969

    Article  CAS  Google Scholar 

  8. Ben Rebah F, Tyagi RD, Prévost D (2002) Production of S. meliloti using wastewater sludge as a raw material: effect of nutrient addition and pH control. Environ Technol 23:623–629

    Article  CAS  PubMed  Google Scholar 

  9. Burton JC (1979) Rhizobium species. In: Peppler HJ, Perlman D (eds) Microbial technology: microbial processes, vol 1, 2nd edn. Academic, New York, pp 29–58

    Google Scholar 

  10. Carvalho M, Matos M, Roca C, Reis MAM (2014) Succinic acid production from glycerol by Actinobacillus succinogenes using dimethylsulfoxide as electron acceptor. New Biotechnol. doi:10.1016/j.nbt.2013.06.006

    Google Scholar 

  11. Ciriminna R, Pina C, Rossi M, Pagiliaro M (2014) Understanding the glycerol market. Eur J Lipid Sci Technol 116:1432–1439

    Article  CAS  Google Scholar 

  12. Dale EB (1984) Fermentation substrates and economics. Ann Rep Fermen Proc 7:107–134

    Article  CAS  Google Scholar 

  13. Dayamani KJ, Brahmaprakash GP (2014) Influence of form and concentration of the osmolytes in liquid inoculants formulations of plant growth promoting bacteria. Intern J Sci Res Publ 4:1–6

    Google Scholar 

  14. Declerck S, Van Coppenolle A (2000) Cryopreservation of entrapped monoxenically produced spores of an arbuscular mycorrhizal fungus. New Phytol 148:169–176

    Article  Google Scholar 

  15. Delabona PS, Lima DJ, Robi D, Rabelo SC, Farinas CS, Pradella JGC (2016) Enhanced cellulase production by Trichoderma harzianum by cultivation on glycerol followed by induction on cellulosic substrates. J Ind Microbiol Biotechnol 43:617–626

    Article  CAS  Google Scholar 

  16. Ding H, Yip CB, Geddes BA, Oresnik IJ, Hynes MF (2012) Glycerol utilization by Rhizobium leguminosarum requires an ABC transporter and affects competition for nodulation. Microbiol 158:1369–1378

    Article  CAS  Google Scholar 

  17. Dishisha T, Ibrahim MHA, Cavero VH, Alvarez MT, Hatti-Kaul (2015) Improved propionic acid production from glycerol: combining cyclic batch- and sequential batch fermentations with optimal nutrient composition. Biores Technol 176:80–87

    Article  CAS  Google Scholar 

  18. Dobson R, Gray V, Rumbold K (2012) Microbial utilization of crude glycerol for the production of value-added products. J Ind Microbiol Biotechnol 39:217–226

    Article  CAS  PubMed  Google Scholar 

  19. Duquenne P, Chenu C, Richard G, Catroux G (1999) Effect of carbon source supply and its location on competition between inoculated and established bacterial strains in sterile soil microcosm. FEMS Microbiol Ecol 29:331–339

    Article  CAS  Google Scholar 

  20. European Biodiesel Board (2015) Statistics: The EU biodiesel industry. http://www.ebb-eu.org/stats.php. Accessed 20 June 2016

  21. França CRRSE, Lira MA Jr, Figueiredo MVB, Stamford NP, Silva GAE (2013) Feasibility of rhizobia conservation by liquid conditioners. Rev Ciên Agron 44:661–668

    Article  Google Scholar 

  22. Gungormusler M, Gonen C, Azbar N (2011) Continuous production of 1,3-propanediol using raw glycerol with immobilized Clostridium beijerinckii NRRL B-593 in comparison to suspended culture. Bioprocess Biosyst Eng. doi:10.1007/s00449-011-0522-2

    PubMed  Google Scholar 

  23. Halos S, Halos P (2008) Stable organic-carrier-based microbial inoculants and method for producing the same. WO 2008156380:A2

    Google Scholar 

  24. Heckly RJ (1978) Preservation of microorgnaisms. Adv Appl Microbiol 34:1–54

    Article  Google Scholar 

  25. Hegde SV (2002) Liquid biofertilizers in Indian agriculture. Biofert News Lett 12:17–22

    Google Scholar 

  26. Hubalek Z (2003) Protectants used in the cryopreservation of microorganisms. Cryobiology 46:205–229

    Article  CAS  PubMed  Google Scholar 

  27. Krey T, Vassilev N, Baum C, Eichler-Lobermann B (2013) Effects of long-term phosphorus application and plant-growth promoting rhizobacteria on maize phosphorus nutrition under field conditions. Eur J Soil Biol 55:124–130

    Article  CAS  Google Scholar 

  28. Lalaymia I, Cranenbrouck S, Declerck S (2014) Maintenance and preservation of ectomycorrhizal and arbuscular mycorrhizal fungi. Mycorrhiza 24:323–337

    Article  PubMed  Google Scholar 

  29. Lopez Zafra D, Mendes G, Eihler-Löbermann B, Vassilev N, Vassileva M (2014) Effect of abiotic stress factors on phosphate solubilisation by Aspergillus niger in submerged and solid-state fermentation. In: Méndez-Vilas A (ed) Industrial, medical and environmental applications of microorganisms. Current status and trends. Wageningen Academic Publishers, The Netherlands, pp 99–103

    Google Scholar 

  30. Lorda G, Balatti A (1996) Designing media I and II. In: Ballatti, Freire (eds) Legume inoculants. Selection and characterization of strains, production, use and management. Editorial Kingraf, Buenos Aires, p 148

    Google Scholar 

  31. Malusa E, Vassilev N (2014) A contribution to set a legal framework for biofertilisers. Appl Microbiol Biotechnol 98:6599–6607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Manikandan R, Saravanakumar D, Rajendran L, Raguchander T, Samiyappan R (2010) Standardization of liquid formulation of Pseudomonas fluorescens Pf1 for its efficacy against Fusarium wilt of tomato. Biol Control 54:83–89

    Article  Google Scholar 

  33. Marketsandmarkets (2013) Global biofertilizers market by types, applications and geography—trends and forecasts to 2017. Marketsandmarkets, Dallas

    Google Scholar 

  34. Martens DA, Frankenberger WRT Jr (1993) Soil saccharide extraction and detection. Plant Soil 149:145–147

    Article  CAS  Google Scholar 

  35. Medina A, Jakobsen I, Vassilev N, Azcón R, Larsen J (2007) Fermentation of sugar beet waste by Aspergillus niger facilitates growth and P uptake of external mycelium of mixed populations of arbuscular mycorrhizal fungi. Soil Biol Biochem 39:485–492

    Article  CAS  Google Scholar 

  36. Melgarejo P, Martínez JJ, Hernández F, Salazar DM, Martínez R (2007) Preliminary results on fig soil-less culture. Sci Hort 111:255–259

    Article  Google Scholar 

  37. Mendes GO, Silva NMRM, Anastácio TC, Vassilev NB, Ribeiro JI, Silva IR (2015) Optimization of Aspergillus niger rock phosphate solubilization in solid-state fermentation and use of the resulting product as a P fertilizer. Microb Biotechnol 8:930–939

    Article  CAS  PubMed Central  Google Scholar 

  38. Meher LC, Sagar DV, Naik SN (2006) Technical aspects of biodiesel production by transesterification—a review. Renew Sustain Energy Rev 10:248–268

    Article  CAS  Google Scholar 

  39. Mugnier J, Jung G (1985) Survival of bacteria and fungi in relation to water activity and the solvent properties of water in biopolymer. Appl Environ Microbiol 50:108–114

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Nichols MCA, Garson S, Bowman JP, Raguénès G, Guézennec J (2004) Production of exopolysaccharides by Antarctic marine bacterial isolates. J Appl Microbiol 96:1057–1066

    Article  CAS  Google Scholar 

  41. Papanikolaou S, Fakas S, Fick M, Chevalot I, Galiotou-Panayotou M, Komaitis M, Marc I, Aggelis G (2008) Biotechnological valorisation of raw glycerol discharged after bio-diesel (fatty acid methyl esters) manufacturing process: production of 1,3-propanediol, citric acid and single cell oil. Biomass Bioenergy 32:60–71

    Article  CAS  Google Scholar 

  42. Patiño-Vera M, Jimenez B, Balderas K, Ortiz M, Allende R, Carillo A, Galindo E (2005) Pilot-scale production and liquid formulation of Rhodotorula minuta, a potential biocontrol agent of mango anthracnose. J Appl Microbiol 99:540–550

    Article  PubMed  Google Scholar 

  43. Qiu S, Arthur J, McComb AJ, Bell RW (2008) Ratios of C, N and P in soil water direct microbial immobilisation–mineralisation and N availability in nutrient amended sandy soils in southwestern Australia. Agric Ecosys Environ 127:93–99

    Article  CAS  Google Scholar 

  44. Qian P, Schoenau J, Urton R (2011) Effect of soil amendment with thin stillage and glycerol on plant growth and soil properties. J Plant Nutr 34:2206–2221

    Article  CAS  Google Scholar 

  45. Quispe CAG, Coronado ChJR, Carvalho J Jr (2013) Glycerol: production, consumption, prices, characterization and new trends in combustion. Renew Sustain Energy Rev 27:475–493

    Article  CAS  Google Scholar 

  46. Redmile-Gordon MA, Evershed RP, Kuhl A, Armenise E, White RP, Hirsch PR, Goulding KWT, Brookes PC (2015) Engineering soil organic matter quality: biodiesel Co-Product (BCP) stimulates exudation of nitrogenous microbial biopolymers. Geoderma 259–260:205–212

    Article  PubMed  PubMed Central  Google Scholar 

  47. Rywinska A, Rymowicz W (2010) High-yield production of citric acid by Yarrowia lipolytica on glycerol in repeated-batch bioreactors. J Ind Microbiol Biotechnol 37:431–435

    Article  CAS  PubMed  Google Scholar 

  48. Sabuquillo P, De Cal A, Melgarejo P (2005) Dispersal improvement of a powder formulation of Penicillium oxalicum, a biocontrol agent of tomato wilt. Plant Dis 89:1317–1323

    Article  Google Scholar 

  49. Sandhya V, SkZ Ali (2015) The production of exopolysaccharide by Pseudomonas putida gap_p45 under various abiotic stress conditions and its role in soil aggregation. Microbiology 84:512–519

    Article  CAS  Google Scholar 

  50. Shankaramand VS, Lonsane BK (1994) Ability of Aspergillus niger to tolerate metal ions and minerals in a solid-state fermentation system for the production of citric acid. Process Biochem 29:29–37

    Article  Google Scholar 

  51. Bo Shen, Hohmann S, Jensen RG, Bohnert HJ (1999) Roles of sugar alcohols in osmotic stress adaptation. Replacement of glycerol by mannitol and sorbitol in yeast. Plant Physiol 121:45–52

    Article  Google Scholar 

  52. Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotechnol 14:407–426

    Article  CAS  Google Scholar 

  53. Singleton P, Keyser H, Sande E (2002) Development and evaluation of liquid inoculants. In: Herridge D (ed) Inoculants and nitrogen fixation of legumes in Vietnam, ACIAR Proceeding 109e. Australian Centre for International Agricultural Research, Canberra, pp 52–66

    Google Scholar 

  54. Smith D (1998) The use of cryopreservation in the ex situ conservation of Fungi. Cryo Lett 19:79–90

    Google Scholar 

  55. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego

    Google Scholar 

  56. Sriram S, Roopa KP, Savitha MJ (2011) Extended shelf-life of liquid fermentation derived talc formulations of Trichoderma harzianum with the addition of glycerol in the production medium. Crop Protect 30:1334–1339

    Article  CAS  Google Scholar 

  57. Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crop Res 65:249–258

    Article  Google Scholar 

  58. Sun FF, Zhao XQ, Hong JP, Tang YJ, Wang L, Sun HY, Li X, Hu JG (2016) Industrially relevant hydrolyzability and fermentability of sugarcane bagasse improved effectively by glycerol organosolv pretreatment. Biotechnol Fuels. doi:10.1186/s13068-016-0472-7

    Google Scholar 

  59. Swift HF (1921) Preservation of stock cultures of bacteria by freezing and drying. J Exp Med 33:69–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Taurian T, Anzuay MS, Angelini JG, Tonelli ML, Ludueña L, Pena D, Ibáñez F, Fabra A (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth- promoting activities. Plant Soil 329:421–431

    Article  CAS  Google Scholar 

  61. Taurian T, Anzuay MS, Ludueña LM, Angelini JG, Muñoz V, Valetti L, Fabra A (2013) Effects of single and co-inoculation with native phosphate solubilising strain Pantoea sp J49 and the symbiotic nitrogen fixing bacterium Bradyrhizobium sp SEMIA 6144 on peanut (Arachis hypogaea L.) growth. Symbiosis 59:77–85

    Article  Google Scholar 

  62. Tisserat and Stuff (2011) Stimulation of short-term plant growth by glycerol applied as foliar sprays and drenches under greenhouse conditions. Hortsci 46:1650–1654

    Google Scholar 

  63. Tittabutr P, Payakapong W, Teaumroong N, Boonkerd N (2005) Cassava as a cheap source of carbon for rhizobial inoculant production using an amylase-producing fungus and a glycerol-producing yeast. World J Microbiol Biotechnol 21:823–829

    Article  CAS  Google Scholar 

  64. US Energy Information Administration (2013) How much biodiesel is produced, imported, exported, and consumed in the United States? http://www.eia.gov/tools/faqs. Accessed 6 May 2016

  65. Vassilev N, Eichler-Löbermann B, Martos V, Vassileva M (2014) Solubilization of animal bone char by Yarrowia lipolytica on medium containing glycerol. New Biotechnol 31:S210

    Article  Google Scholar 

  66. Vassilev N, Eichler-Löbermann B, Vassileva M (2012) Stress-tolerant P-solubilizing microorganisms. Appl Microbiol Biotechnol 95:851–859

    Article  CAS  PubMed  Google Scholar 

  67. Vassilev N, Martos E, Mendes G, Flor-Peregrin E, Martos V, Vassileva M (2013) Biochar of animal origin: a sustainable solution of the high-grade rock phosphate scarcity. J Sci Food Agric 93:1799–1804

    Article  CAS  PubMed  Google Scholar 

  68. Vassilev N, Medina A, Eichler-Löbermann B, Flor-Peregrín E, Vassileva M (2012) Animal bone char solubilization with itaconic acid produced by free and immobilized Aspergillus terreus grown on glycerol-based medium. Appl Biochem Biotechnol 168:1311–1318

    Article  CAS  PubMed  Google Scholar 

  69. Vassilev N, Medina A, Mendes G, Galvez A, Martos V, Vassileva M (2013) Solubilization of animal bonechar by a filamentous fungus employed in solid state fermentation. Ecol Eng 58:165–169

    Article  Google Scholar 

  70. Vassilev N, Mendes G, Costa M, Vassileva M (2014) Biotechnological tools for enhancing microbial solubilization of insoluble inorganic phosphates. Geomicrobiol J 31:751–763

    Article  CAS  Google Scholar 

  71. Vassilev N, Someus E, Bravo V, Vassileva M (2009) Novel approaches in phosphate-fertilizer production based on wastes derived from rock phosphate mining and the food processing industry. In: Samuelson JP (ed) Industrial waste: environmental impact, disposal and treatment. NOVA Science Publishers, NY, pp 387–391

    Google Scholar 

  72. Vassilev N, Vassileva M (1992) Production of organic acids by immobilized filamentous fungi. Mycol Res 96:563–570

    Article  Google Scholar 

  73. Vassilev N, Vassileva M (2003) Biotechnological solubilization of rock phosphate on media containing agro-industrial wastes. Appl Microbiol Biotechnol 61:435–440

    Article  CAS  PubMed  Google Scholar 

  74. Vassilev N, Vassileva M, Lopez A, Martos V, Reyes A, Maksimovic I, Eichler-Löbermann B, Malusà E (2015) Unexploited potential of some biotechnological techniques for biofertilizer production and formulation. Appl Microbiol Biotechnol 99:4983–4996

    Article  CAS  PubMed  Google Scholar 

  75. Vassilev N, Vassileva M, Spassova D, Hadjiev P (1992) Citric acid production by immobilized Aspergillus niger on starch hydrolysate media. In: Vardar-Sukan F, Suha Sukan S (eds) Recent advances in biotechnology vol 210, NATO ASI Series. Springer, The Netherlands, pp 507–508

    Chapter  Google Scholar 

  76. Vassileva M, Eichler-Lobermann B, Reyes A, Vassilev N (2012) Animal bones char solubilization by gel-entrapped Yarrowia lipolytica on glycerol-based media. Sci World J. doi:10.1100/2012/907143 (Article ID 907143, 5 pages)

    Google Scholar 

  77. Vassileva M, Serrano M, Bravo V, Jurado E, Nikolaeva I, Martos V, Vassilev N (2010) Multifunctional properties of phosphate-solubilizing microorganisms grown on agro-industrial wastes in fermentation and soil conditions. Appl Microbiol Biotechnol 85:1287–1299

    Article  CAS  PubMed  Google Scholar 

  78. Velineni S, Brahmaprakash GP (2011) Survival and phosphate solubilizing ability of Bacillus megaterium in liquid inoculants under high temperature and desiccation stress. J Agr Sci Tech 13:795–802

    CAS  Google Scholar 

  79. Vendan RT, Thangaraju M (2006) Development and standardization of liquid formulation for Azospirillum bioinoculant. Ind J Microbiol 46:379–387

    CAS  Google Scholar 

  80. Vendan R, Thangaraju M (2007) Development and standardization of Azospirillum bioinoculant. Acta Microbiol Immun Hung 54:167–177

    Article  Google Scholar 

  81. Vinocur B, Altman A (2005) Cellular basis of salinity tolerance in plants. Environ Exp Bot 52:113–122

    Google Scholar 

  82. Vodnar DC, Dulf FV, Pop OL, Socaciu C (2013) L (+)-lactic acid production by pellet form Rhizopus oryzae NRRL 395 on biodiesel crude glycerol. Microb Cell Fact 12:92–101

    Article  PubMed  PubMed Central  Google Scholar 

  83. Willke Th, Vorlop K-D (2004) Industrial bioconversion of renewable resources as an alternative to conventional chemistry. Appl Microbiol Biotechnol 66:131–142

    Article  CAS  PubMed  Google Scholar 

  84. Yadav BK, Verma A (2012) Phosphate solubilization and mobilization in soil through microorganisms under arid ecosystems. In: Ali Mahamane (ed) The functioning of ecosystems. InTech, Rijeka, pp 93–108

    Google Scholar 

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Acknowledgments

This work is supported by Project No CTM2014-53186-R, Ministerio de Economia y Competitividad-España and the EC FEDER Fund.

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Authors and Affiliations

  1. Institute of Biotechnology, University of Granada, Granada, Spain

    Nikolay Vassilev, Antonia Reyes Requena, Vanessa Martos, Ana López & Maria Vassileva

  2. Unit of Turin, CRA-Centre for Plant–Soil Systems, Turin, Italy

    Eligio Malusa

  3. University of Novi Sad, Novi Sad, Republic of Serbia

    Ivana Maksimovic

  4. Department of Chemical Engineering, University of Granada, c/Fuentenueva s/n, 18071, Granada, Spain

    Nikolay Vassilev

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  1. Nikolay Vassilev
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  2. Eligio Malusa
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Correspondence to Nikolay Vassilev.

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Vassilev, N., Malusa, E., Requena, A.R. et al. Potential application of glycerol in the production of plant beneficial microorganisms. J Ind Microbiol Biotechnol 44, 735–743 (2017). https://doi.org/10.1007/s10295-016-1810-2

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