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Applied Microbiology and Biotechnology

, Volume 99, Issue 12, pp 4983–4996 | Cite as

Unexploited potential of some biotechnological techniques for biofertilizer production and formulation

  • N. Vassilev
  • M. Vassileva
  • A. Lopez
  • V. Martos
  • A. Reyes
  • I. Maksimovic
  • B. Eichler-Löbermann
  • E. Malusà
Mini-Review

Abstract

The massive application of chemical fertilizers to support crop production has resulted in soil, water, and air pollution at a global scale. In the same time, this situation escalated consumers’ concerns regarding quality and safety of food production which, due to increase of fertilizer prices, have provoked corresponding price increase of food products. It is widely accepted that the only solution is to boost exploitation of plant-beneficial microorganisms which in conditions of undisturbed soils play a key role in increasing the availability of minerals that otherwise are inaccessible to plants. This review paper is focused on the employment of microbial inoculants and their production and formulation. Special attention is given to biotechniques that are not fully exploited as tools for biofertilizer manufacturing such as microbial co-cultivation and co-immobilization. Another emerging area includes biotechnological production and combined usage of microorganisms/active natural compounds (biostimulants) such as plant extracts and exudates, compost extracts, and products like strigolactones, which improve not only plant growth and development but also plant-microbial interactions. The most important potential and novel strategies in this field are presented as well as the tendencies that will be developed in the near future.

Keywords

Biofertilizers Co-cultivation Solid-state fermentations Co-immobilization Phytostimulants 

Notes

Acknowledgments

This work was supported by Project CTM2011-02779 and CTM2014-53186-R (Ministerio de Ciencia e Innovación, España) and the Polish Innovation Economy Operational Program, contract N. UDA-POIG.01.03.01-10-109/08-00.

Statement

The review has not been published before and is not under consideration for publication anywhere else. The manuscript has been approved by all co-authors.

Compliance with ethical standards/ethical statement

Conflict of interest

N. Vassilev has received Project Grants (CTM2011-02779 and CTM2014-53186-R) from the Spanish Ministerio de Ciencia e Innovación. E. Malusà has received a grant from the EU Regional Development Fund through the Polish Innovation Economy Operational Program, contract N. UDA-POIG.01.03.01-10-109/08-00. These authors declare that they have no conflict of interest.

References

  1. Abad LV, Kudo H, Saiki S, Nagasawa N, Tamada M, Katsumura Y (2009) Radiation degradation studies of carrageenans. Carbohydr Polym 78:100–106Google Scholar
  2. Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886PubMedGoogle Scholar
  3. Aftab T, Khan MMA, Idrees M, Naeem M, Hashmi N, Varshney L (2011) Enhancing the growth, photosynthetic capacity and artemisinin content in Artemisia annua L. by irradiated sodium alginate. Radiat Phys Chem 80:833–836Google Scholar
  4. Akiyama H, Endo T, Nakakita R, Murata K, Yonemoto Y, Okayama K (1992) Effect of depolymerized alginates on the growth of bifidobacteria. Biosci Biotechnol Biochem 56:355–356PubMedGoogle Scholar
  5. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedGoogle Scholar
  6. Alagawadi AR, Gaur AC (1988) Associative effect of Rhizobium and phosphate solubilizing bacteria on the yield and nutrient uptake of chickpea. Plant Soil 105:241–246Google Scholar
  7. Albersheim P, McNeil M, Labavitch JM (1977) The wall of growing cells. In: Pilet PE (ed) Plant growth regulation. Sprineger Verlag, Berlin, pp 1–12Google Scholar
  8. Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295–22. Appl Environ Microbiol 65:2926–2933PubMedCentralPubMedGoogle Scholar
  9. Ariyo BT, Bucke C, Keshavarz T (1997) Alginate oligosaccharides as enhancers of penicillin production in cultures of Penicillium chrysogenum. Biotechnol Bioeng 53:17–20PubMedGoogle Scholar
  10. Ariyo BT, Bucke C, Keshavarz T (1998) Enhanced penicillin production by oligosaccharides from batch cultures of Penicillium chrysogenum in stirred-tank reactors. FEMS Microbiol Lett 166:165–170PubMedGoogle Scholar
  11. Babana AH, Antoun H (2006) Effect of Tilemsi phosphate rock-solubilizing microorganisms on phosphorus uptake and yield of field-grown wheat (Triticum aestivum L.) in Mali. Plant Soil 287:51–58Google Scholar
  12. Balakrishnan K, Pandey A (1996) Production of biologically active secondary metabolites in solid state fermentation. J Sci Ind Res 55:365–372Google Scholar
  13. Bardi L, Malusà E (2012) Drought and nutritional stresses in plant: alleviating role of rhizospheric microorganisms. In: Haryana N, Punj S (eds) Abiotic stress: new research. Nova Science Publishers Inc, Hauppauge, pp 1–57Google Scholar
  14. Bashan Y, de-Bashan L E, Prabhu SR, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33Google Scholar
  15. Bertrand S, Bohni N, Schnee S, Schumpp O, Gindro K, Wolfender J-L (2014) Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv 32:1180–1204PubMedGoogle Scholar
  16. Besserer A, Puech-Pages V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais J-C, Roux C, Becard G, Sejalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226PubMedCentralPubMedGoogle Scholar
  17. Bethlenfalway GJ, Brown MS, Stafford AE (1985) Glycine-Glomus-Rhizobium symbiosis. Plant Physiol 79:1054–1058Google Scholar
  18. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350PubMedGoogle Scholar
  19. Bianciotto V, Bonfante P (2002) Arbuscular mycorrhizal fungi: a specialised niche for rhizospheric and endocellular bacteria. Antonie Van Leeuwenhoek 81:365–371PubMedGoogle Scholar
  20. Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631Google Scholar
  21. Brenner K, Arnold FH (2011) Self-organization, structure, and aggregation enhance persistence of a synthetic biofilm consortium. PLoS ONE 6:e16791PubMedCentralPubMedGoogle Scholar
  22. Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41Google Scholar
  23. Cannel E, Moo-Young M (1980) Solid-state fermentation systems. Proc Biochem 4:2–7Google Scholar
  24. Capalbo DMF, Morales IO (1997) Use of agro-industrial residues for bioinsecticidal endotoxin production by Bacillus thuringiensis var. israelensis or kurstaki in solid state fermentation. In: Roussos S, Lonsane BK, Viniegra-Gonzalez RM (eds) Advances in Solid State Fermentation. Montpellier, Springer Netherlands, pp 473–480Google Scholar
  25. Cariello ME, Castañeda L, Riobo I, Gonzalez J (2007) Inoculante de microorganismos endógenos para acelerar el proceso compostaje de residuos sólidos urbanos. J Soil Sci Plant Nutr 7:26–37Google Scholar
  26. Cassidy MB, Lee H, Trevors JT (1996) Environmental applications of immobilized microbial cells: a review. J Ind Microbiol 16:79–101Google Scholar
  27. Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea lour.): isolation and properties of a potent stimulant. Science 154:1189–1190PubMedGoogle Scholar
  28. Corkidi L, Allen EB, Merhaut D, Allen MF, Downer J, Bohn J, Evans M (2004) Assessing the infectivity of commercial mycorrhizal inoculants in plant nursery conditions. J Environ Hortic 22:149–154Google Scholar
  29. Darvill AG, Albersheim P, McNeil M, Lau JM, York WS, Stevenson TT, Thomas J, Doares S, Gollin DJ, Chelf P, Davis K (1985) Structure and function of plant cell wall polysaccharides. J Cell Sci Suppl 2:203–217PubMedGoogle Scholar
  30. De Jaeger N, Declerck S, De la Providencia IE (2010) Mycoparasitism of arbuscular mycorrhizal fungi: a pathway for the entry of saprotrophic fungi into roots. FEMS Microbiol Ecol 73:312–322PubMedGoogle Scholar
  31. De Jaeger N, de la Providencia IE, Rouhier H, Declerck S (2011) Co-entrapment of Trichoderma harzianum and Glomus sp. within alginate beads: impact on the arbuscular mycorrhizal fungi life cycle. J Appl Microbiol 111:125–135PubMedGoogle Scholar
  32. De Roy K, Marzorati M, Van den Abbeele P, Van de Wiele T, Boon N (2013) Synthetic microbial ecosystems: an exciting tool to understand and apply microbial communities. Environ Microbiol. doi: 10.1111/462-2920.12343 PubMedGoogle Scholar
  33. De Salamone IEG, Di Salvo LP, Ortega JSE, Sorte PMFB, Urquiaga S, Teixeira KRS (2010) Field response of rice paddy crop to Azospirillum inoculation: physiology of rhizosphere bacterial communities and the genetic diversity of endophytic bacteria in different parts of the plants. Plant Soil 336:351–362Google Scholar
  34. Declerck S, Strullu DG, Plenchette C, Guillemette T (1996) Entrapment of in vitro produced spores of Glomus versiforme in alginate beads: in vitro and in vivo inoculum potentials. J Biotechnol 48:51–57Google Scholar
  35. Dommergues YR, Diem HG, Divies C (1979) Polyacrylamide-entrapped Rhizobium as an inoculant for legumes. Appl Environ Microbiol 37:779–781Google Scholar
  36. Downey J, van Kessel C (1990) Dual inoculation of Pisum sativum with Rhizobium leguminosarum and Penicillium bilaji. Biol Fertil Soils 10:194–196Google Scholar
  37. Dwivedi P, Vivekanand V, Pareek N, Sharma A, Singh RP (2011) Co-cultivation of mutant Penicillium oxalicum SAU E-3.510 and Pleurotus ostreatus for simultaneous biosynthesis of xylanase and laccase under solid-state fermentation. New Biotechnol 28:616–626Google Scholar
  38. Eisenhauer N (2012) Aboveground–belowground interactions as a source of complementarity effects in biodiversity experiments. Plant Soil 351:1–22Google Scholar
  39. EU Commission (2012) Report from the commission to the European Parliament, the Council, the European economic and social committee and the committee of the regions. The implementation of the soil thematic strategy and ongoing activities. COM 46 final, p. 15Google Scholar
  40. EU Regulation N. 2003/2003 of the European Parliament and of the Council of 13 October 2003 relating to fertilisers. Official Journal of the European Union L 304, 1–194Google Scholar
  41. Ezzi MI, Lynch JM (2005) Biodegradation of cyanide by Trichoderma spp. and Fusarium spp. Enzym Microb Technol 36:849–854Google Scholar
  42. Faessel L, Gomy C, Nassr N, Tostivint C, Hipper C, Dechanteloup A (2014) Produits de stimulation en agriculture visant a ameliorer les fonctionnalites biologiques des sols et des plantes. BIO & RITTMO. 156 pp. http://agriculture.gouv.fr/IMG/pdf/Rapport_final_ETUDE_Produits_de_stimulation_en_agriculture_2014_cle8632c3.pdf Accessed 01 April 2015
  43. Faye A, Dalpé Y, Ndung'u-Magiroi K, Jefwa J, Ndoye ID, Lesueur D (2013) Evaluation of commercial arbuscular mycorrhizal inoculants on maize in Kenya. Can J Plant Sci 93:1201–1208Google Scholar
  44. Feldmann F, Hommes M (2013) Endophytes for plant protection: the registration process at a glance. In: Schneider C, Leifert C, Feldmann F (eds) Endophytes for plant protection: the state of the art. Deutsche Phytomedizinische Gesellshaft, Baunschweig, pp 214–222Google Scholar
  45. Fernendez-Larrea Vega O (1999) A review of Bacillus thuringiensis (Bt) production and use in Cuba. Biocontrol News Inform 20:47N–48NGoogle Scholar
  46. Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different microorganisms. New Phytol 141:525–533Google Scholar
  47. Finley R (2004) Mycorrhizal fungi and their multifunctional roles. Mycologist 18:91–96Google Scholar
  48. Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity–productivity relationship in an N-limited grassland. Ecology 90:408–418PubMedGoogle Scholar
  49. Fracchia S, Mujica MT, Garcia-Romera I, Garcia-Garrido JM, Martin J, Ocampo JA, Godeas A (1998) Interactions between Glomus mosseae and arbuscular mycorrhizal sporocarp-associated saprophytic fungi. Plant Soil 200:131–137Google Scholar
  50. Fracchia S, Sampedro I, Scervino JM, Garcia-Romera I, Ocampo JA, Godeas A (2004) Influence of saprobe fungi and their exudates on arbuscular mycorrhizal symbioses. Symbiosis 36:162–182Google Scholar
  51. Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59Google Scholar
  52. Gemell LG, Hartley EJ, Herridge DF (2005) Point-of-sale evaluation of preinoculated and custom-inoculated pasture legume seed. Anim Prod Sci 45:161–169Google Scholar
  53. Gera C, Srivastava S (2006) Quorum-sensing: the phenomenon of microbial communication. Curr Sci 90:566–677Google Scholar
  54. Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823PubMedGoogle Scholar
  55. Green H, Larsen J, Olsson PA, Jensen DF, Jakobsen I (1999) Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root-free soil. Appl Environ Microbiol 65:1428–1434PubMedCentralPubMedGoogle Scholar
  56. Gupte A, Madamwar D (1997) Solid state fermentation of ligno-cellulosic wastes for cellulase and beta-glucosidase production by co-culturing of Aspergillus ellipticus and Aspergillus fumigatus. Biotechnol Progress 13:166–169Google Scholar
  57. Gutierrez-Correa M, Tengerdy RP (1997) Production of cellulase on sugar cane bagasse by fungal mixed culture solid substrate fermentation. Biotechnol Lett 19:665–667Google Scholar
  58. Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257Google Scholar
  59. Hashmia N, Khana MMA, Moinuddina, Idreesa M, Khana ZH, Ali A, Varshney L (2012) Depolymerized carrageenan ameliorates growth, physiological attributes, essential oil yield and active constituents of Foeniculum vulgare Mill. Carbohydr Polym 90:407–412Google Scholar
  60. Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285Google Scholar
  61. Herrmann L, Lesueur D (2013) Challenges of formulation and quality of biofertilizers for successful inoculation. Appl Microbiol Biotechnol 97:8859–8873PubMedGoogle Scholar
  62. Hickert LR, Cruz MM, Dillon AJP, Fontana RC, Rosa CA, Záchia Ayub MA (2014) Fermentation kinetics of acid–enzymatic soybean hull hydrolysate in immobilized-cell bioreactors of Saccharomyces cerevisiae, Candida shehatae, Spathaspora arborariae, and their co-cultivations. Biochem Eng J 88:61–67Google Scholar
  63. Hien NQ, Nagasawa N, Tham LX, Yoshii F, Dang HV, Mitomo H (2000) Growth promotion of plants with depolymerised alginates by irradiation. Radiat Phys Chem 59:97–101Google Scholar
  64. Hildebrandt U, Janetta K, Bothe H (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl Environ Microbiol 68:1919–1924PubMedCentralPubMedGoogle Scholar
  65. Holker U, Lenz J (2005) Solid-state fermentation—are there any biotechnological advantages. Curr Opinion Microbiol 8:301–306Google Scholar
  66. Hölker U, Höfer M, Lenz J (2004) Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Appl Microbiol Biotechnol 64:175–186PubMedGoogle Scholar
  67. Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:1–13Google Scholar
  68. Hu HL, van den Brink J, Gruben BS, Wösten HAB, Gu J-D, de Vries RP (2011) Improved enzyme production by co-cultivation of Aspergillus niger and Aspergillus oryzae and with other fungi. Int Biodeterior Biodegrad 65:248–252Google Scholar
  69. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13PubMedGoogle Scholar
  70. John M, Rohrig H, Schmidt J, Walden R, Schell J (1997) Cell signalling by oligosaccharides. Trends Plant Sci 3:111–115Google Scholar
  71. Joner EJ, Jakobsen I (1995) Growth and extracellular phosphatase activity of arbuscular mycorrhizal hyphae as influenced by soil organic matter. Soil Biol Biochem 27:1153–1159Google Scholar
  72. Keen NT (1975) Specific elicitors of plant phytoalexin production: determinants of race specificity in pathogens? Science 187:74–75PubMedGoogle Scholar
  73. Keen NT (1992) The molecular biology of disease resistance. Plant Mol Biol 19:109–122PubMedGoogle Scholar
  74. Kim HJ, Boedicker JQ, Choi JW, Ismagilov RF (2008) Defined spatial structure stabilizes a synthetic multispecies bacterial community. Proc Natl Acad Sci U S A 105:18188–18193PubMedCentralPubMedGoogle Scholar
  75. Kitcha S, Cheirsilp B (2014) Enhanced lipid production by co-cultivation and co-encapsulation of oleaginous yeast Trichosporonoides spathulata with microalgae in alginate gel beads. Appl Biochem Biotechnol 173:522–534PubMedGoogle Scholar
  76. Kolasa M, Kiær Ahring B, Lübeck PS, Lübeck M (2014) Co-cultivation of Trichoderma reesei RutC30 with three black Aspergillus strains facilitates efficient hydrolysis of pretreated wheat straw and shows promises for on-site enzyme production. Bioresour Technol 169:143–148PubMedGoogle Scholar
  77. Kpomblekou AK, Tabatabai MA (1994) Effect of organic acids on release of phosphorus from phosphate rocks. Soil Sci 158:442–453Google Scholar
  78. Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:3–8Google Scholar
  79. Kucey RMN (1987) Increased phosphorus uptake by wheat and field beans inoculated with a phosphorus-solubilizing Penicillium bilaji strain and with vesicular-arbuscular mycorrhizal fungi. Appl Environ Microbiol 53:2699–2703PubMedCentralPubMedGoogle Scholar
  80. Kume T, Nagasawa N, Yoshii F (2002) Utilization of carbohydrates by radiation processing. Radiat Phys Chem 63:625–627Google Scholar
  81. Lam MK, Lee KT (2012) Immobilization as a feasible method to simplify the separation of microalgae from water for biodiesel production. Chem Eng J 191:263–268Google Scholar
  82. Larsen J, Olsson PA, Jakobsen I (1998) The use of fatty acid signatures to study mycelial interactions between the arbuscular mycorrhizal fungus Glomus intraradices and the saprotrophic fungus Fusarium culmorum in root-free soil. Mycol Res 102:1491–1496Google Scholar
  83. Lee WS, Chen C, Chang CH, Yang SS (2012) Bioethanol production from sweet potato by co-immobilization of saccharolytic molds and Saccharomyces cerevisiae. Renew Energy 39:216–222Google Scholar
  84. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207PubMedGoogle Scholar
  85. Lemanceau P, Bauer P, Kraemer S, Briat J-F (2009) Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes. Plant Soil 321:513–535Google Scholar
  86. Lisette J, Xavier C, Germida JJ (2003) Selective interactions between arbuscular mycorrhizal fungi and Rhizobium leguminosarum bv. viceae enhance pea yield and nutrition. Biol Fertil Soils 37:261–267Google Scholar
  87. Lucy M, Reed E, Glick BR (2004) Application of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25PubMedGoogle Scholar
  88. Lupwayi NZ, Olsen PE, Sande ES, Keyser HH, Collins MM, Singleton PW, Rice WA (2000) Inoculant quality and its evaluation. Field Crops Res 65:259–270Google Scholar
  89. Mäder P, Fließbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity in organic farming. Science 296:1694–1697PubMedGoogle Scholar
  90. Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748PubMedGoogle Scholar
  91. Malusá E, Vassilev N (2014) A contribution to set a legal framework for biofertilizers. Appl Microbiol Biotechnol 98:6599–6607PubMedCentralPubMedGoogle Scholar
  92. Malusà E, Sas-Paszt L, Zurawicz E, Popinska W (2007) The effect of a mycorrhiza-bacteria substrate and foliar fertilization on growth response and rhizosphere pH of three strawberry cultivars. Int J Fruit Sci 6:25–41Google Scholar
  93. Malusá E, Sas-Paszt L, Trzcinski P, Górska A (2012a) Influences of different organic fertilizers and amendments on nematode trophic groups and soil microbial communities during strawberry growth. Acta Hortic (ISHS) 933:253–260Google Scholar
  94. Malusá E, Sas-Paszt L, Ciesielska J (2012b) Technologies for beneficial microorganisms inocula used as biofertilizers. Sci World J. doi: 10.1100/2012/491206 Google Scholar
  95. Manefield M, Turner SL (2002) Quorum sensing in context: out of molecular biology and into microbial ecology. Microbiology 148:3762–3764PubMedGoogle Scholar
  96. Mansfeld-Giese K, Larsen J, Bodker L (2002) Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol Ecol 41:133–140PubMedGoogle Scholar
  97. Marmann A, Aly AH, Lin WH, Wang BG, Proksch P (2014) Co-cultivation—a powerful emerging tool for enhancing the chemical diversity of microorganisms. Mar Drugs 12:1043–1065PubMedCentralPubMedGoogle Scholar
  98. Martin G, Guggiari M, Bravo D, Zopfi J, Cailleau G, Aragno M, Job D, Verrecchia E, Junier P (2012) Fungi, bacteria and soil pH: the oxalate–carbonate pathway as a model for metabolic interaction. Environ Microbiol 14:2960–2970PubMedGoogle Scholar
  99. Martinez A, Obertello M, Pardo A, Ocampo JA, Godeas A (2004) Interactions between Trichoderma pseudokoningii strains and the arbuscular mycorrhizal fungi Glomus mosseae and Gigaspora rosea. Mycorrhiza 14:79–84PubMedGoogle Scholar
  100. McAllister CB, Garcıa-Romera I, Godeas A, Ocampo JA (1994a) Interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae: effects on plant growth, arbuscular mycorrhizas and the saprophyte inoculants. Soil Biol Biochem 26:1363–1367Google Scholar
  101. McAllister CB, Garcia-Romera I, Godeas A, Ocampo JA (1994b) In vitro interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae. Soil Biol Biochem 26:1369–1374Google Scholar
  102. Medina A, Vassilev N, Alguacil M, Roldan A, Azcon R (2004) Increased plant growth, nutrient uptake and soil enzymatic activities in a decertified Mediterranean soil amended with treated residues and inoculated with native AM fungi and plant-growth-promoting yeast. Soil Sci 169:260–270Google Scholar
  103. 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 39:485–492Google Scholar
  104. Mercier L, Lafitte C, Borderies G, Briand X, Esquerré-Tugayé MT, Fournier J (2001) The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol 149:43–51Google Scholar
  105. Mitchell DA, Berovic M, Krieger N (2002) Overview of solid state bioprocessing. Biotechnol Annu Rev 8:183–225PubMedGoogle Scholar
  106. Morales IO, Capalbo DMF, Arruda ROM, Bianchi VL, Ascher KRS (1998) Bacillus thuringiensis development from 1971 to 1996: cases of a research group in Brazil. Isr J Entomol 32:45–48Google Scholar
  107. Morris ON, Knagaratnam P, Converse V (1996) Suitability of 30 agricultural products and by-products as nutrient sources for laboratory production of Bacillus thuringiensis subsp. aizawai (HD133). J Invertebr Pathol 70:113–120Google Scholar
  108. Mulder CPH, Jumpponen A, Högberg P, Huss-Danell K (2002) How plant diversity and legumes affect nitrogen dynamics in experimental grassland communities. Oecologia 133:412–421Google Scholar
  109. Muñoz G, Agosin E, Cotoras M, San Martin R, Volpe D (1995) Comparison of aerial and submerged spore properties of Trichoderma harzianum. FEMS Microbiol Lett 125:63–69Google Scholar
  110. Naeem M, Idrees M, Aftab T, Khan MMA, Varshney L (2012) Depolymerised carrageenan enhances physiological activities and menthol production in Mentha arvensis L. Carbohydr Res 87:1211–1218Google Scholar
  111. Naiman AD, Latronico DA, de Salamone IEG (2009) Inoculation of wheat with Azospirillum brasilense and Pseudomonas fluorescens: impact on the production and culturable rhizosphere microflora. Eur J Soil Biol 45:44–51Google Scholar
  112. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670Google Scholar
  113. Nwokoro O, Uju Dibua ME (2014) Degradation of soil cyanide by single and mixed cultures of Pseudomonas stutzeri and Bacillus subtilis. Arch Ind Hyg Toxicol 65:113–119Google Scholar
  114. Ola AR, Thomy D, Lai D, Brötz-Oesterhelt H, Proksch P (2013) Inducing secondary metabolite production by the endophytic fungus Fusarium tricinctum through coculture with Bacillus subtilis. J Nat Prod 76:2094–2099PubMedGoogle Scholar
  115. Olivian C, Alabouvette C, Steinberg C (2004) Production of a mixed inoculum of Fusarium oxisporum Fo47 and Pseudomonas fluorescens C7 to control Fusarium diseases. Biocontrol Sci Tech 14:227–238Google Scholar
  116. Olsen PE, Rice WA, Collins MM (1994) Biological contaminants in North American legume inoculants. Soil Biol Biochem 27:699–701Google Scholar
  117. Olsen PE, Rice WA, Bordeleau LM, Demidoff AH, Collins MM (1996) Levels and identities of non-rhizobial microorganisms found in commercial legume inoculant made with non-sterile peat carrier. Can J Microbiol 42:72–75PubMedGoogle Scholar
  118. Osorio NW, Habte M (2001) Synergistic influence of an arbuscular mycorrhizal fungus and a P solubilizing fungus on growth and P uptake of Leucaena leucocephala in an oxisol. Arid Land Res Manag 15:263–274Google Scholar
  119. Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphorus acquisition. Appl Soil Ecol 86:41–54Google Scholar
  120. Palacios OA, Bashan Y, de-Bashan LE (2014) Proven and potential involvement of vitamins in interactions of plants with plant growth-promoting bacteria—an overview. Biol Fertil Soils 50:415–432Google Scholar
  121. Pandey A (2003) Solid state fermentation. Biochem Eng J 13:81–84Google Scholar
  122. Pant D, Adholeya A (2010) Development of a novel fungal consortium for the treatment of molasses distillery wastewater. Environmentalist 30:178–182Google Scholar
  123. Pascual S, de Cal A, Magan N, Melgarejo P (2000) Surface hydrophobicity, viability and efficacy in biological control of Penicillium oxalicum spores produced in aerial and submerged culture. J Appl Microbiol 89:847–853PubMedGoogle Scholar
  124. Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martínez-Molina E, Velazquez E (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biol Biochem 33:103–110Google Scholar
  125. Petruccioli M, Piccioni P, Fenice M, Federici F (1994) Glucose oxidase, catalase and gluconic acid production by immobilized mycelium of Penicillium variabile P16. Biotechnol Lett 16:939–942Google Scholar
  126. Petruccioli M, Federici F, Bucke C, Keshavarz T (1999) Enhancement of glucose oxidase production by Penicillium variabile P16. Enzym Microb Technol 24:397–401Google Scholar
  127. Potin P, Bouarab K, Kupper F, Kloareg B (1999) Oligosaccharide recognition signals and defence reactions in marine plant–microbe interactions. Curr Opin Microbiol 2:276–283PubMedGoogle Scholar
  128. Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37:91–102PubMedGoogle Scholar
  129. Raina S, De Vizio D, Odell M, Clements M, Vanhulle S, Keshavarz T (2009) Microbial quorum sensing: a tool or a target for antimicrobial therapy? Biotechnol Appl Biochem 54:65–84PubMedGoogle Scholar
  130. Rateb ME, Hallyburton I, Houssen W, Bull A, Goodfellow M, Santhanam R, Jaspars M, Ebel R (2013) Induction of diverse secondary metabolites in Aspergillus fumigatus by microbial co-culture. RSC Adv 3:14444–14450Google Scholar
  131. Ravnskov S, Larsen J, Olsson PA, Jakobsen I (1999) Effects of various compounds on growth and phosphorus uptake in an arbuscular mycorrhizal fungus. New Phytol 141:517–524Google Scholar
  132. Rayner ADM, Boddy L (1988) Fungal communities in the decay of wood. Adv Microb Ecol 10:115–166Google Scholar
  133. Relleve L, Abad L, Aranilla, C, Aliganga A, De La Rosa A, Yoshii F (2000) Biological activities of radiation degraded carrageenan. In Proceedings of the Symposium on Radiation Technology in Emerging Industrial Applications Beijing, People’s Republic of China, 6–10 November, pp. 98–108Google Scholar
  134. Rice WA, Lupwayi NZ, Olsen PE, Schlechte D, Gleddie SC (2000) Field evaluation of dual inoculation of alfalfa with Sinorhizobium meliloti and Penicillium bilaii. Can J Plant Sci 80:303–308Google Scholar
  135. Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339Google Scholar
  136. Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67PubMedGoogle Scholar
  137. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734PubMedCentralPubMedGoogle Scholar
  138. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43PubMedGoogle Scholar
  139. Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140:339–353Google Scholar
  140. Singleton PW, Boonkerd N, Carr TJ, Thompson JA (1997) Technical and market constraints limiting legume inoculant use in Asia. In: Rupela OP, Johansen C, Herridge DF (eds) Extending Nitrogen Fixation Research to Farmers' Fields: Proceedings of an International Workshop on Managing Legume Nitrogen Fixation in the Cropping Systems of Asia. ICRISAT Asia Centre, India, 20 ± 24 August 1996. International Crops Research Institute for the Semi-Arid Tropics, Pantacheru 502 324, Andhra Pradesh, pp. 17–38Google Scholar
  141. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier and Academic, New YorkGoogle Scholar
  142. Tarbell TJ, Koske RE (2007) Evaluation of commercial arbuscular mycorrhizal inocula in a sand/peat medium. Mycorrhiza 18:51–56PubMedGoogle Scholar
  143. Tengerby RP, Szakacs G (2003) Bioconversion of lignocellulose in solid substrate fermentation. Biochem Eng J 13:169–179Google Scholar
  144. Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int 86:32–40. doi: 10.1155/2013/863240 Google Scholar
  145. Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254Google Scholar
  146. Vassilev N, Vassileva M (1992) Production of organic acids by immobilized filamentous fungi. Mycol Res 96:563–570Google Scholar
  147. Vassilev N, Vassileva M (2003) Biotechnological solubilization of mineral phosphates on media containing agro-industrial wastes. Appl Microbiol Biotechnol 61:435–440PubMedGoogle Scholar
  148. Vassilev N, Baca MT, Vassileva M (1994) Plant lignocellulose and fungi: from nature to industrial use. Mycologist 8:113–115Google Scholar
  149. Vassilev N, Baca MT, Vassileva M, Franco I, Azcon R (1995) Rock phosphate solubilization by Aspergillus niger grown on sugar-beet waste medium. Appl Microbiol Biotechnol 44:546–549Google Scholar
  150. Vassilev N, Franco I, Vassileva M, Azcon R (1996) Improved plant growth with rock phosphate solubilized by Aspergillus niger grown on sugar beet waste. Bioresour Technol 55:237–241Google Scholar
  151. Vassilev N, Toro M, Vassileva M, Azcon R, Barea JM (1997) Rock phosphate solubilization by encapsulated Enterobacter sp. in fermentation and soil conditions. Bioresour Technol 61:29–33Google Scholar
  152. Vassilev N, Vassileva M, Fenice M, Federici F (2001a) Immobilized cell technology applied in solubilization of insoluble inorganic (rock) phosphates and P plant acquisition. Bioresour Technol 79:263–271PubMedGoogle Scholar
  153. Vassilev N, Vassileva M, Azcon R, Medina A (2001b) Application of free and Ca-alginate-entrapped Glomus deserticola and Yarrowia lipolytica in a soil-plant system. J Biotechnol 91:237–242PubMedGoogle Scholar
  154. Vassilev N, Vassileva M, Azcon R, Medina A (2001c) Preparation of gel-entrapped mycorrhizal inoculum in the presence or absence of Yarrowia lipolytica. Biotechnol Lett 23:907–909Google Scholar
  155. Vassilev N, Vassileva M, Azcon R, Medina A (2001d) Interactions of an arbuscular mycorrhizal fungus with free and co-encapsulated cells of Rhizobium trifoli and Yarrowia lipolytica inoculated into a soil-plant system. Biotechnol Lett 23:149–151Google Scholar
  156. Vassilev N, Vassileva M, Azcon R, Barea J-M (2002) The use of 32P dilution techniques to evaluate the effect of mycorrhizal inoculation on plant uptake of P from products of fermentation mixtures including agrowastes, Aspergillus niger and rock phosphate. In: Assessment of Soil Phosphorus Status and Management of Phosphatic Fertilizers to Optimize Crop Production. IAEA-TECDOC-1272, pp. 47–53. IAEA Technical Document. FAO/IAEA, Vienna, Austria. http://www.iaea.org/inis/collection/NCLCollectionStore/_Public/33/019/33019223.pdf.
  157. Vassilev N, Nikolaeva I, Vassileva M (2005) Polymer-based preparation of soil inoculants: applications to arbuscular mycorrhizal fungi. Rev Environ Sci Bio Technol 4:235–243Google Scholar
  158. Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144PubMedGoogle Scholar
  159. Vassilev N, Nikolaeva I, Vassileva M (2007) An improved technique for preparation of gel-entrapped fungal spores. Minerva Biotechnol 19:51–55Google Scholar
  160. Vassilev N, Requena A, Nieto L, Nikolaeva I, Vassileva M (2009) Production of manganese peroxidase by Phanerochaete chrysosporium grown on medium containing agro-wastes/rock phosphate and biocontrol properties of the final product. Ind Crop Prod 30:28–32Google Scholar
  161. Vassilev N, Eichler-Lobermann B, Vassileva M (2012) Stress tolerant P-solubilizing microorganisms. Appl Microbiol Biotechnol 95:851–859PubMedGoogle Scholar
  162. Vassilev N, Martos E, Mendes G, Flor-Peregrin E, Martos V, Vassileva M (2013a) Biochar of animal origin: a sustainable solution of the high-grade rock phosphate scarcity. J Sci Food Agric 93:1799–1804PubMedGoogle Scholar
  163. Vassilev N, Medina A, Martos E, Galvez A, Mendes G, Martos V, Vassileva M (2013b) Solubilization of animal bonechar by a filamentous fungus employed in solid state fermentation. Ecol Eng 58:165–169Google Scholar
  164. Vassilev N, Mendes G, Costa M, Vassileva M (2014) Biotechnological tools for enhancing microbial solubilization of insoluble inorganic phosphates. Geomicrobiol J 31:751–763. doi: 10.1080/01490451.2013.822615 Google Scholar
  165. Vassileva M, Azcon R, Barea JM, Vassilev N (1999) Effect of encapsulated cells of Enterobacter sp. on plant growth and phosphate uptake. Bioresour Technol 67:229–232Google Scholar
  166. 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. doi: 10.1007/s00253-009-2366-0 PubMedGoogle Scholar
  167. Vassileva M, Fenice M, Galvez A, Vassilev N (2014) Plant growth enhancement by biotechnological tools. New Biotechnol 31:S210Google Scholar
  168. Verma P, Madamwar D (2002) Production of ligninolytic enzymes for dye decolorization by cocultivation of white-rot fungi Pleurotus ostreatus and Phanerochaete chrysosporium under solid-state fermentation. Appl Biochem Biotechnol 102–103:109–118PubMedGoogle Scholar
  169. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586Google Scholar
  170. Wamberg C, Christensen S, Jakobsen I, Müller AK, Sørensen SJ (2003) The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol Biochem 35:1349–1357Google Scholar
  171. Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181PubMedGoogle Scholar
  172. Weber J, Ducousso M, Tham FY, Nourissier-Mountou S, Galiana A, Prin Y, Lee SK (2005) Co-inoculation of Acacia mangium with Glomus intraradices and Bradyrhizobium sp. in aeroponic culture. Biol Fertil Soils 41:233–239Google Scholar
  173. Wen Z, Liao W, Chen S (2005) Production of cellulase/b-glucosidase by the mixed fungi culture Trichoderma reesei and Aspergillus phoenicis on dairy manure. Process Biochem 40:3087–3094Google Scholar
  174. West SA, Griffin AS, Gardner A, Diggle SP (2006) Social evolution theory for microbes. Nat Rev Microbiol 4:597–607PubMedGoogle Scholar
  175. Wu SC, Cao ZH, Li ZG, Cheung KC, Wong MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166Google Scholar
  176. Yoneyama K, Xie X, Yoneyama K, Takeuchi Y (2009) Strigolactones: structures and biological activities. Pest Manag Sci 6:467–470Google Scholar
  177. Zafra D, Mendes G, Eichler-Löbermann B, Vassilev N, Vassileva M (2014) Effect of abiotic stress factors on phosphate solubilization by acid-producing Aspergillus niger in submerged and solid-state fermentations. In: Méndez-Vilas A (ed) Industrial, medical and environmental applications of microorganisms: current status and trends. Wageningen Academic Publishers, pp. 99–103Google Scholar
  178. Zhang H, Hong YZ, Xiao YZ, Yuan J, Tu XM, Zhang XQ (2006) Efficient production of laccases by Trametes sp. AH28-2 in cocultivation with a Trichoderma strain. Appl Microbiol Biotechnol 73:89–94PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • N. Vassilev
    • 1
    • 2
  • M. Vassileva
    • 2
  • A. Lopez
    • 2
  • V. Martos
    • 3
  • A. Reyes
    • 2
  • I. Maksimovic
    • 4
  • B. Eichler-Löbermann
    • 5
  • E. Malusà
    • 6
  1. 1.Institute of BiotechnologyUniversity of GranadaGranadaSpain
  2. 2.Department of Chemical Engineering, Faculty of SciencesUniversity of GranadaGranadaSpain
  3. 3.Department of Plant PhysiologyUniversity of GranadaGranadaSpain
  4. 4.University of Novi SadNovi SadRepublic of Serbia
  5. 5.Faculty of AgricultureUniversity of RostockRostockGermany
  6. 6.Institute of HorticultureSkierniewicePoland

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