Skip to main content

Advertisement

SpringerLink
Log in

Phosphate solubilization by stress-tolerant soil fungus Talaromyces funiculosus SLS8 isolated from the Neem rhizosphere

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

A promising biotechnological strategy in the management of phosphorus (P) fertilization is the use of phosphate-solubilizing fungi to solubilize rock phosphates and allow the recovery of unavailable P fixed to soil particles. Phosphate-solubilizing rhizosphere fungus, Talaromyces funiculosus SLS8, isolated from Neem (Azadirachta indica) on saline soil, was tolerant to environmental stressors, salinity and agricultural systemic fungicides. Phosphate solubilization under different nutritional conditions was investigated by culturing T. funiculosus SLS8 in Pikovskaya liquid medium containing different nitrogen sources (ammonium sulfate, casein, urea, potassium nitrate or sodium nitrate) and carbon sources (glucose, fructose, galactose or sucrose), NaCl, and three systemic fungicides. The highest concentration of solubilised phosphate (187 mg P L−1) was achieved after 5 days of incubation in the medium with glucose and ammonium sulphate. The culture pH decreased from 6.5 to 4.2 and HPLC demonstrated organic acid production. Phosphate solubilized was highly negatively correlated with pH (r = −0.96). Increasing salinity had no effect on phosphate solubilization. The maximum tolerance limits to systemic fungicides carbendazim, mancozeb, and hexaconazole were 12.5 μg mL−1, 2,000 μg mL−1 and 250 μl mL−1 respectively. At these concentrations carbendazim, mancozeb and hexaconazole were found to decrease phosphate solubilization by 55 %, 37 %, and 30 %, respectively. Our results indicate that T. funiculosus SLS8 may be a potential candidate for the development of a biofertilizer for maintaining available phosphate levels in environmentally stressed soils such as saline agricultural soils impacted by systemic fungicide application or seed treatment.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahemad M, Khan MS (2010) Plant growth promoting activities of phosphate solubilizing Enterobacter asburiae as influenced by fungicides. Eur Asia J Biosci 4:88–95

    Article  Google Scholar 

  • Alam S, Khalil S, Ayub N, Rashid M (2002) In vitro solubilization of inorganic phosphate by phosphate solubilizing microorganisms (PSM) from maize rhizosphere. Int J Agric Biol 4:454–458

    CAS  Google Scholar 

  • APHA, American Public Health Association (1998) American Water Works Association, and Water Environment Federation, in LS Clesceri, AE Greenberg, AD Eaton (eds) Standard methods for the examination of water and wastewater. Washington, DC

  • Asea PEA, Kucey RMN, Stewart JWB (1988) Inorganic phosphate solubilisation by two Penicillium species in solution culture and soil. Soil Biol Biochem 20:459–464

    Article  CAS  Google Scholar 

  • Barroso CB, Pereira GT, Nahas E (2006) Solubilization of CaHPO4 and ALPO4 by Aspergillus niger in culture media with different carbon and nitrogen sources. Braz J Microbiol 37:434–438

    Google Scholar 

  • Chai B, Wu Y, Liu P, Liu B, Gao M (2011) Isolation and phosphate-solubilizing ability of a fungus Penicillium sp. from soil of an alum mine. J Basic Microbiol 51:5–14

    Article  CAS  PubMed  Google Scholar 

  • Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilising bacteria from tropical soil and their tricalcium phosphate solubilising abilities. Appl Soil Ecol 34:33–41

    Article  Google Scholar 

  • Corden ME, Young RA (1965) Changes in the soil microflora following fungicide treatments. Soil Sci 99:272–277

    Article  CAS  Google Scholar 

  • Edi–Premono M, Moawad MA, Vleck PLG (1996) Effect of phosphate solubilising Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indones J Crop Sci 11:13–23

    Google Scholar 

  • Estrada B, Barea JM, Aroca R, Ruiz-Lozano JM (2013) A native Glomus intraradices strain from a Mediterranean saline area exhibits salt tolerance and enhanced symbiotic efficiency with maize plants under salt stress conditions. Plant Soil 366:333–349

    Article  CAS  Google Scholar 

  • Gadd GM (1999) Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Adv Microb Physiol 41:47–92

    Article  CAS  PubMed  Google Scholar 

  • Gaur AC (1990) Phosphate solubilizing microorganisms as Biofertilizers, 1st edn. Omega Science Publishers, New Delhi

    Google Scholar 

  • Goldstein AH (1986) Bacterial solubilization of mineral phosphates: historical perspectives and future prospect. Am J Altern Agric 1:51–57

    Google Scholar 

  • Hwangbo H, Park RD, Kim YW, Rim YS, Park KH, Kim TH, Suh JS, Kim KY (2003) 2-Ketogluconic acid production and phosphate solubilization by Enterobacter intermedium. Curr Microbiol 47:87–92

    Article  CAS  PubMed  Google Scholar 

  • Illmer P, Barbato A, Schinner F (1995) Solubilisation of hardly-soluble AlPO4 with P solubilizing microorganisms. Soil Biol Biochem 27:265–27

    Article  CAS  Google Scholar 

  • Imfeld G, Vuilleumier S (2012) Measuring the effects of pesticides on bacterial communities in soil: a critical review. Eur J Soil Biol 49:22–30

    Article  CAS  Google Scholar 

  • Jackson ML (1973) Soil Chemical Analysis. Prentice Hall of India, New Delhi

    Google Scholar 

  • Jacobs H, Boswell GP, Ritz K, Fordyce AD, Gadd GM (2002) Solubilization of calcium phosphate as a consequence of carbon translocation by Rhizoctonia solan. FEMS Microbiol Ecol 40:65–71

    Article  CAS  PubMed  Google Scholar 

  • Jain R, Saxena J, Sharma V (2012) Solubilization of inorganic phosphates by Aspergillus awamori S19 isolated from rhizosphere soil of a semi-arid region. Ann Microbiol 62:725–735

    Article  CAS  Google Scholar 

  • Jin H, Germida JJ, Walley FL (2013) Suppressive effects of seed-applied fungicides on arbuscular mycorrhizal fungi (AMF) differ with fungicide mode of action and AMF species. Appl Soil Ecol 72:22–30

    Article  Google Scholar 

  • Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ (2011) Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–886

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Villavicencio M, Aguileta G, Giraud T, de Vienne DM, Lacoste S, Couloux A, Dupont J (2010) Sex in Penicillium: combined phylogenetic and experimental approaches. Fungal Genet Biol 47:693–706

    Article  CAS  PubMed  Google Scholar 

  • Mahamuni SV, Wani PV, Patil AS (2012) Isolation of phosphate solubilizing fungi from rhizosphere of sugarcane and sugar beet using Tcp and Rp solubilisation. Asian J Biochem Pharm Res 2:237–244

    CAS  Google Scholar 

  • Matias SR, Pagano MC, Muzzi FC, Oliveira CA, Carneiro AA, Horta SN, Scotti MR (2009) Effect of rhizobia, mycorrhizal fungi and phosphate-solubilizing microorganisms in the rhizosphere of native plants used to recover an iron ore area in Brazil. Eur J Soil Biol 45:259–266

    Article  CAS  Google Scholar 

  • Mendes GO, de Freitas ALM, Pereira OL, da Silva IR, Vassilev NB, Costa MD (2013) Mechanisms of phosphate solubilization by fungal isolates when exposed to different P sources. Ann Microbiol. doi:10.1007/s13213-013-0656-3

    Google Scholar 

  • Mittal V, Singh O, Nayyar H, Kaur J, Tewari R (2008) Stimulatory effect of phosphate-solubilizing fungal strains (Aspergillus awamori and Penicillium citrinum) on the yield of chickpea (Cicer arientinum L. cv. GPF2). Soil Biol Biochem 40:718–727

    Article  CAS  Google Scholar 

  • Mukadam DS (1997) The Illustrated Kingdom of Fungi. Akshar Ganga Prakashan, Aurangabad

    Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Narsian V, Patel H (2000) Aspergillus aculeatus as a rock phosphate solubilizer. Soil Biol Biochem 32:559–565

    Article  CAS  Google Scholar 

  • Nautiyal CS, Bhadauria S, Kumar P, Lal K, Mondal R, Verma D (2000) Stress induced phosphate solubilization in bacteria isolated from alkaline soils. FEMS Microbiol Lett 182:291–296

    Article  CAS  PubMed  Google Scholar 

  • 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 15:263–274

    Google Scholar 

  • Palaniyandi SA, Yang SH, Damodharan K, Suh J (2013) Genetic and functional characterization of culturable plant-beneficial actinobacteria associated with yam rhizosphere. J Basic Microbiol 00:1–11

    Google Scholar 

  • Park K, Lee O, Jung H, Jeong J, Jeon Y, Hwang D, Lee C, Son H (2010) Rapid solubilisation of insoluble phosphate by a novel environmental stress-tolerant Burkholderia vietmniensis M6 isolated form ginseng rhizospheric soil. Appl Microbiol Biotechnol 86:947–955

    Article  CAS  PubMed  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17:362–370

    CAS  Google Scholar 

  • Pitt JI (1988) A laboratory guide to common Penicillium species. CSIRO, Division of Food Processing, North Ryde

  • Pradhan N, Sukla LB (2005) Solubilization of inorganic phosphates by fungi isolated from agricultural soil. Afr J Biotechnol 5:850–854

    Google Scholar 

  • Rashid M, Khalil S, Ayub N, Alam S, Latif F (2004) Organic acid production and phosphate solubilization by phosphate solubilizing microorganisms under in vitro conditions. Pak J Biol Sci 7:187–196

    Article  Google Scholar 

  • Rasool N, Reshi ZA (2010) Effect of the fungicide Mancozeb at different application rates on enzyme activities in a silt loam soil of the Kashmir Himalaya, India. Trop Ecol 51:199–205

    CAS  Google Scholar 

  • Relwani L, Krishna P, Reddy MS (2008) Effect of carbon and nitrogen sources on phosphate solubilization by a wild type strain and UV- induced mutants of Aspergillus tubingensis. Curr Microbiol 57:401–406

    Google Scholar 

  • Reyes I, Bernier L, Simard RR, Autoum H (1999) Effect of nitrogen source on the phosphate solubilization of different inorganic phosphates by an isolate of Penicillium rugulosum and two UV induced mutants. FEMS Microbiol Ecol 28:281–290

    Article  CAS  Google Scholar 

  • Rinu K, Pandey A (2010) Temperature-dependent phosphate solubilisation by cold and pH-tolerant species of Aspergillus isolated from Himalayan soil. Mycoscience 51:263–271

    Article  CAS  Google Scholar 

  • Roos W, Luckner M (1984) Relationship between proton extrusion and fluxes of ammonium ions and organic acids in Penicillium cyclopium. J Gen Microbiol 130:1007–1014

    Google Scholar 

  • Scervino JM, Mesa MP, Monica ID, Recchi M, Moreno NS, Godeas A (2010) Soil fungal isolates produce different organic acid patterns involved in phosphate salts solubilisation. Biol Fertil Soils 46:755–763

    Article  CAS  Google Scholar 

  • Scervino JM, Papinutti VL, Godoy MS, Rodriguez MA, Della Monica I, Recchi M, Pettinari MJ, Godeas AM (2011) Medium pH, carbon and nitrogen concentrations modulate the phosphate solubilisation efficiency of Penicillium purpurogenum through organic acid production. J Appl Microbiol 10:1215–1223

    Article  Google Scholar 

  • Schneider KD, van Straaten P, Mira de Orduña R, Glasauer S, Trevors J, Fallow D, Smith PS (2009) Comparing phosphorus mobilization strategies using Aspergillus niger for the mineral dissolution of three phosphate rocks. J Appl Microbiol 108:366–374

    Article  Google Scholar 

  • Seshadri S, Ignacimuthu S, Lakshminarasimhan C (2004) Effect of nitrogen and carbon sources on the inorganic phosphate solubilisation by different Aspergillus niger strains. Chem Eng Commun 191:1043–1052

    Article  CAS  Google Scholar 

  • Singal R, Gupta R, Saxena RK (1994) Rock phosphate solubilization under alkaline conditions by Aspergillus japonicus and A. foetidus. Folia Microbiol (Praha) 39:33–36

    Article  CAS  Google Scholar 

  • Srinivasan R, Yandigeri MS, Kashyap S, Alagawadi AR (2012) Effect of salt on survival and P-solubilization potential of phosphate solubilizing microorganisms from salt affected soils. Saudi J Biol Sci 19:427–434

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Srividya CS, Soumya S, Pooja K (2009) Influence of environmental factors and salinity on phosphate solubilization by a newly isolated Aspergillus niger F7 from agriculture soil. Afr J Biotechnol 8:1864–1870

    CAS  Google Scholar 

  • Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71(2):137–144

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vyas P, Rahi P, Chauhan A, Gulati A (2007) Phosphate solubilisation potential and stress tolerance of Eupenicillium parvum from tea soil. Mycol Res 111:931–938

    Article  CAS  PubMed  Google Scholar 

  • Wakelin SA, Gupta VVSR, Harvey PR, Ryder MH (2007) The effect of penicillium fungi on plant growth and P mobilisation in neutral to alkaline soils from southern Australia. Can J Microbiol 53:106–115

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Hasbullah, Setia R, Marschner P, Zhang F (2012) Potential soil P mobilisation capacity–method development and comparison of rhizosphere soil from different crops. Plant Soil 354:259–267

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols. A Guide to Methods and Applications. Academic Press, San Diego, pp 315–322

    Chapter  Google Scholar 

  • Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate solubilizing fungi. Adv Agron 69:99–151

    Article  CAS  Google Scholar 

  • Whitelaw MA, Harden TJ, Helyar KR (1999) Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biol Biochem 31:655–665

    Google Scholar 

  • Yadav J, Verma JP, Yadav SK, Tiwari KN (2011) Effect of salt concentration and pH on soil inhabiting fungus Penicillium citrinum Thom.for solubilization of tricalcium phosphate. Microbiol J 1:25–32

    Article  Google Scholar 

  • Zaidi A, Khan MS (2007) Stimulatory effects of dual inoculation with phosphate solubilising microorganisms and arbuscular mycorrhizal fungus on chickpea. Aust J Exp Agric 47:1016–1022

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the School of Life Sciences, Swami Ramanand Teerth Marathwada University, Nanded, India for providing necessary facilities for conducting this research and also the National Centre for Cell Science, Pune for the 18SrRNA sequencing.

Conflict of interest

We have no financial, proprietary or any other conflict of interest that might influence opinions and positions.

Author information

Authors and Affiliations

  1. Department of Microbiology, School of Life Sciences, Swami Ramanand Teerth Marathwada University, Nanded, India, 431606

    Omkar Shankarrao Kanse, Tukaram Angadrao Kadam & Hemalata Janardhanrao Bhosale

  2. New South Wales Department of Primary Industries, National Wine & Grape Industry Centre, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW, Australia, 2678

    Melanie Whitelaw-Weckert

Authors
  1. Omkar Shankarrao Kanse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melanie Whitelaw-Weckert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tukaram Angadrao Kadam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hemalata Janardhanrao Bhosale
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Melanie Whitelaw-Weckert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kanse, O.S., Whitelaw-Weckert, M., Kadam, T.A. et al. Phosphate solubilization by stress-tolerant soil fungus Talaromyces funiculosus SLS8 isolated from the Neem rhizosphere. Ann Microbiol 65, 85–93 (2015). https://doi.org/10.1007/s13213-014-0839-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-014-0839-6

Keywords

Search

Navigation