Abstract
The morphology of filamentous fungi plays very important role in uptake of metabolites and enzyme production. A filamentous fungus may be fibrous, hyphae, pellets, clumps, etc. Cochliobolus lunatus is a fungus which has previously been reported for silver accumulation and nanoparticles formation. The present study investigated the role of various carbon sources on morphology, biochemical profile, silver accumulation, and biosynthesis of silver nanoparticles by fungal strain C. lunatus. In this investigation, effect of different carbon sources was studied on morphology of C. lunatus and its silver accumulating ability. As a result of different carbon sources like carboxymethyl cellulose (CMC), pectin, starch, agar, sucrose, and mannitol, the organism showed three kinds of morphologies like homogenous smooth branched clumps, tough short fibrous filaments, and tough pellets, as well as silver accumulating ability. Atomic absorption spectroscopy (AAS) studies showed maximum uptake of Ag+: 87.44 ± 0.23 and 82.57 ± 0.19 % in pectin- and CMC-grown biomass, respectively. The crystalline nature of silver nanoparticles (AgNPs) was confirmed by X-ray diffraction studies. Transmission electron microscopy (TEM) micrographs of silver nanoparticles confirmed size ranging from 5 to 38 nm.
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Wyatt, T. T., Golovina, E. A., Leeuwen, R., Hallsworth, J. E., Wösten, H. A. B., & Dijksterhuis, J. (2015). A decrease in bulk water and mannitol and accumulation of trehalose and trehalose‐based oligosaccharides define a two‐stage maturation process towards extreme stress resistance in ascospores of Neosartorya fischeri (Aspergillus fischeri). Environmental Microbiology, 17, 383–394.
Zhang, H., Li, Q., Wang, H., Sun, D., Lu, Y., & He, N. (2007). Accumulation of silver(I) ion and diamine silver complex by Aeromonas SH10 biomass. Applied Biochemistry and Biotechnology, 143, 54–62.
Merroun, M. L., BenOmar, N., Alonso, E., Arias, J. M., & Gonzalez-Munoz, M. T. (2001). Silver sorption to Myxococcus xanthus biomass. Geomicrobiology, 18, 183–192.
Dias, M. A., Lacerda, I. C. A., Pimentel, P. F., DeCastro, H. F., & Rosa, C. A. (2002). Removal of heavy metals by an Aspergillus terreus strain immobilized in a polyurethane matrix. Letters in Applied Microbiology, 34, 46–50.
Mukherjee, P., Ahmad, A., Mandal, D., Senapati, S., Sainkar, S. R., Khan, M. I., Ramani, R., Parischa, R., Ajaykumar, P. V., Alam, M., Sastry, M., & Kumar, R. (2001). Bioreduction of AuCl(4)(−) ions by the fungus, Verticillium sp. and surface trapping of the gold nanoparticles. Angewandte Chemie International Edition, 40, 3585–3588.
Pighi, L., Pumpel, T., & Schinner, F. (1989). Selective accumulation of silver by fungi. Biotechnology Letters, 11, 275–280.
Chen, J. C., Lin, Z. H., & Ma, X. X. (2003). Evidence of the production of silver nanoparticles via pretreatment of Phoma sp.3.2883 with silver nitrate. Letters in Applied Microbiology, 37, 105–108.
Ahmad, A., Mukherjee, P., Senapati, S., Mandal, D., Khan, M. I., Kumar, R., & Sastry, M. (2003). Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids and Surface B, 28, 313–318.
Bhainsa, K. C., & D’Souza, S. F. (2006). Extracellular biosynthesis of silver nanoparticles using the fungus Aspergillus fumigatus. Colloids and Surface B, 47, 160–164.
Vigneshwaran, N., Kathe, A. A., Varadrajan, P. V., Nachane, R. P., & Balasubramanya, R. H. (2006). Biomimetics of silver nanoparticles by white rot fungus Phaenerochaete chrysosporium. Colloids and Surface B, 53, 55–59.
Vigneshwaran, N., Ashtaputre, N. M., Varadarajan, P. V., Nachane, R. P., Paralikar, K. M., & Balasubramanya, R. H. (2007). Biological synthesis of silver nanoparticles using the fungus Aspergillus flavus. Material Letters, 61, 1413–1418.
Ingle, A., Rai, M., Gade, A., & Bawaskar, M. (2008). Fusarium solani: a novel biological agent for the extracellular synthesis of silver nanoparticles. Journal Nanoparticles Research, 11, 2079–2085.
Vitas, M., Smith, K., Rozman, D., & Komel, R. (1994). 1 lfl-Hydroxysteroid dehydrogenase activity in progesterone biotransformation by the filamentous fungus Cochliobolus lunatus. Journal of Steroid Biochemistry and Molecular Biology, 49, 87–92.
Salunkhe, R. B., Patil, S. V., Salunke, B. K., Patil, C. D., & Sonawane, A. M. (2011). Studies on silver accumulation and nanoparticle synthesis by Cochliobolus lunatus. Applied Biochemistry and Biotechnology, 165(1), 221–234.
Salunkhe, R. B., Patil, S. V., Patil, C. D., & Salunke, B. K. (2011). Larvicidal potential of silver nanoparticles synthesized using fungus Cochliobolus lunatus against Aedes aegypti (Linnaeus, 1762) and Anopheles stephensi Liston (Diptera; Culicidae). Parasitology Research, 109(3), 823–831.
Elamayerhi, H., Scharer, J. M., & Moo-Young, M. (1973). Effects of polymer additives on fermentation parameters in a culture of A. niger. Biotechnology Bioengineering, 15, 845–859.
Yang, W., Hartwieg, E. A., Fang, A., & Demain, A. L. (2003). Effects of carboxymethylcellulose and carboxypolymethylene on morphology of Aspergillus fumigatus NRRL 2346 and fumagillin production. Current Microbiology, 46, 24–27.
Xia, X., & Xie, Z. (2001). Software package for data analysis in molecular biology and evolution. The Journal of Heredity, 92, 371–373.
Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.
Cray, J. A., Stevenson, A., Ball, P., Bankar, S. B., Eleutherio, E. C. A., Ezeji, T. C., Singhal, R. S., Thevelein, J. M., Timson, D. J., & Hallsworth, J. E. (2015). Chaotropicity: a key factor in product tolerance of biofuel-producing microorganisms. Current Opinion in Biotechnology, 33, 228–259.
Cray, J. A., Houghton, J. D. R., Cooke, L. R., & Hallsworth, J. E. (2015). A simple inhibition coefficient for quantifying potency of biocontrol agents against plant-pathogenic fungi. Biological Control, 81, 93–100.
Morin, M., & Ward, O. P. (1989). Investigation of cell wall composition of different mycelia forms of Rihizpus arrhizus. Mycological Research, 93(4), 524–528.
Dubois, M., Gilles, H. Y., Rebers, P., & Smith, F. (1956). The carbohydrates of the Gramineae. A quantitative study of the carbohydrates of wheat germ. Analytical Chemistry, 28, 350–356.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.
Lejeune, R., & Baron, G. V. (1995). Effect of agitation on growth and enzyme production of Trichoderma reesei in batch fermentation. Applied Microbiology and Biotechnology, 43, 249–258.
Vecht-Lifshitz, S. E., Magdassi, S., & Braun, S. (1990). Pellet formation and cellular aggregation in Streptomyces tendae. Biotechnology and Bioengineering, 35, 890–896.
Peberdy, J. F. (1994). Protein secretion in filamentous fungi—trying to understand a highly productive black box. Trends in Biotechnology, 12, 50–57.
Punt, P. J., van Biezen, N., Conesa, A., Albers, A., Mangnus, J., & van den Hondel, C. (2002). Filamentous fungi as cell factories for heterologous protein production. Trends in Biotechnology, 20(5), 200–206.
Pluschkell, S., Hellmuth, K., & Rinas, U. (1996). Kinetics of glucose oxidase excretion by recombinant Aspergillus niger. Biotechnology and Bioengineering, 51, 215–220.
Juge, N., Svensson, B., & Williamson, G. (1998). Secretion, purification, and characterization of barley-amylase produced by heterologous gene expression in Aspergillus niger. Applied Microbiology and Biotechnology, 49, 385–392.
Thomas, P., & Schinner, F. (1986). Silver tolerance and silver accumulation of microorganisms from soil materials of silver mine. Applied Microbiology and Biotechnology, 24, 244–247.
Gonzalez-Munoz, M. T., Merroun, M. L., BenOmar, N., & Arias, J. M. (1997). Biosorption of uranium by Myxococcus xanthus. International Biodeterioration & Biodegradation, 40, 107–114.
BenOmar, N., Merroun, M. L., Arias, J. M., & Gonzalez-Munoz, M. T. (1997). Comparative heavy metal biosorption study of brewery yeast and Myxococcus xanthus biomass. Chemosphere, 35, 2277–2283.
Omar, N. B., Merroun, M.L., Penalver, J. M. A., Munoz, M.T.G. (1997) Comparative heavy metal biosorption study of brewery yeast and Myxococcus xanthus biomass. Chemosphere, 35, 2277–2283.
Merroun, M. L., BenOmar, N., Gonzalez-Munoz, M. T., & Arias, J. M. (1998). Myxococcus xanthus biomass as biosorbent for lead. Journal of Applied Microbiology, 84, 63–67.
Mitard, A., & Riba, J. P. (1988). Morphology and growth of Aspergillus niger ATCC 26036 cultivated at several shear rates. Biotechnology and Bioengineering, 32, 835–840.
Elamayerhi, H., & Scharer, J. M. (1973). Physiological studies on Aspergillus niger fermentation with polymer additives. Journal of General and Applied Microbiology, 76, 277–282.
Elamayerhi, H. (1975). Mechanisms of pellet formation of Aspergillus niger with additives. Journal of Fermentation Technology, 53, 722–729.
Jones, P., Moore, D., & Trinci, A. P. J. (1988). Effect of Junlon and Hostacerin on the electrokinetic properties of fungal spores. Journal of General Microbiology, 134, 235–256.
Jones, P., Shahab, B. A., Trinci, A. P. J., & Moore, D. (1988). Effect of polymer additives, notably Junlon and Hostacerin, on growth of some basidiomycetes in submerged culture. Transactions of British Mycological Society, 90, 577–583.
Patil, R. H., Patil, S. V., Patil, U. K., Bhat, J. A., Rajput, J., & Chaudhry, R. (2008). Biotransformation of Rifamycin B to Rifamycin S with free and immobilized cells of C. lunata. Journal of Pure and Applied Microbiology, 2(1), 111–114.
Slavica, B., Konstantinovic, S. S., Veljkovic, V. B., Savic, D. S., Lazic, M. L., & Gojgic-Cvijovic, G. (2008). Impact of carboxymethylcellulose on morphology and antibiotic production by Streptomyces hygroscopicus. Current Microbiology, 57, 8–11.
Metz, B., & Kossen, N. W. F. (1977). The growth of molds in the form of pellets—a literature review. Biotechnology and Bioengineering, 19, 781–799.
Nakajima, A., Horikoshi, T., & Sakaguchi, T. (1981). Studies on the accumulation of heavy metal elements in biological systems. Journal of Applied Microbiology and Biotechnology, 12, 76–83.
Bitton, G., & Freihofer, V. (1978). Influence of extracellular parasites on toxicity of copper and cadmium toward Klebsiella aerogenes. Microbial Ecology, 4, 119–125.
Camici, L., Sermonti, G., & Chain, E. B. (1952). Observations on Penicillium chrysogenum in submerged culture. 1. Mycelial growth and autolysis. Bulletin of World Health Organization, 6, 265–276.
Gole, A., Dash, C., Ramachandran, V., Sainkar, S. R., Mandale, A. B., Rao, M., & Sastry, M. (2001). Pepsin-gold colloid conjugates: preparation, characterization, and enzymatic activity. Langmuir, 17, 1674–1679.
Balaji, D. S., Basavaraja, S., Deshpande, R., Mahesh, D. B., Prabhakar, B. K., & Venkataraman, A. (2009). Extracellular biosynthesis of functionalized silver nanoparticles by strains of Cladosporium cladosporioides fungus. Colloids and Surfaces B, 68, 88–92.
Naik, R. R., Sarah, J., Stringer, S. J., Agarwal, G., Jones, S. E., & Stone, M. O. (2002). Biomimetic synthesis and patterning of silver nanoparticles. Nature Materials, 1, 169–172.
Lloyd, J. R. (2003). Microbial reduction of metals and radionuclides. FEMS Microbiology Reviews, 27, 411–425.
Medentsev, A. G., & Alimenko, V. K. (1998). Naphthoquinone metabolites of the fungi. Phytochemistry, 47, 935–959.
Duran, N., Teixeira, M. F. S., De Conti, R., & Esposito, E. (2002). Ecological-friendly pigments from fungi. Critical Reviewes in Food Science and Nutrition, 42, 53–66.
Bell, A. A., Wheeler, M. H., Liu, J., Stipanovic, R. D., Puckhaber, L. S., & Orta, H. (2003). United States Department of Agriculture-Agricultural Research Service studies on polyketide toxins of Fusarium oxysporum f sp. vasinfectum: potential targets for disease control. Pest Management Science, 59, 736–747.
Baker, R. A., & Tatum, J. H. (1998). Novel anthraquinones from stationary cultures of Fusarium oxysporum. Journal of Fermentation and Bioengineering, 85, 359–361.
Newman, D. K., & Kolter, R. (2000). A role for excreted quinones in extracellular electron transfer. Nature, 405, 94–97.
Kathiresan, K., Manivannan, S., Nabeel, M. A., & Dhivya, B. (2009). Studies on silver nanoparticles synthesized by a marine fungus, Penicillium fellutanum isolated from coastal mangrove sediment. Colloids and Surfaces B: Biointerfaces, 71, 133–137.
Pal, S., Tak, Y. K., & Song, J. M. (2007). Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Applied Environmental Microbiology, 27(6), 1712–1720.
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Authors are also thankful to UGC-SAP and DST-FIST for providing financial support to the department.
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Salunkhe, R.B., Borase, H.P., Patil, C.D. et al. Effect of Different Carbon Sources on Morphology and Silver Accumulation in Cochliobolus lunatus . Appl Biochem Biotechnol 177, 1409–1423 (2015). https://doi.org/10.1007/s12010-015-1822-9
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DOI: https://doi.org/10.1007/s12010-015-1822-9