Copper stress and filamentous fungus Humicola lutea 103 - ultrastructural changes and activities of key metabolic enzymes

Canadian Journal of Microbiology

Volumn 58, Issue 12, 2012, Pages 1335-1343

  Krumova, Ekaterina Ts ^a   Stoitsova, Stoyanka R ^a   Paunova Krasteva, Tsvetelina S ^a   Pashova, Svetlana B ^a   Angelova, Maria B ^a  

^a INSTITUTE OF MICROBIOLOGY   (Bulgaria)

Author keywords

Copper stress; Fungi; Key metabolic enzymes; Ultrastructure

Indexed keywords

COPPER; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HEAVY METAL; HEXOKINASE; ISOCITRATE DEHYDROGENASE; MALATE DEHYDROGENASE;

CATION; CONCENTRATION (COMPOSITION); COPPER; DOSE-RESPONSE RELATIONSHIP; ENZYME ACTIVITY; FUNGUS; HEAVY METAL; MITOCHONDRION; MOLECULAR ANALYSIS; OXIDATION; POLLUTION TOLERANCE; ULTRASTRUCTURE;

ARTICLE; BIOMASS PRODUCTION; CELL MIGRATION; CELL ULTRASTRUCTURE; CITRIC ACID CYCLE; CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; ENZYME METABOLISM; FUNGUS; FUNGUS GROWTH; GLYCOLYSIS; HUMICOLA LUTEA; NONHUMAN; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL;

ASCOMYCOTA; BIOMASS; CITRIC ACID CYCLE; COPPER; GLUCOSEPHOSPHATE DEHYDROGENASE; GLYCOLYSIS; HEXOKINASE; HYPHAE; ISOCITRATE DEHYDROGENASE; MALATE DEHYDROGENASE; MICROSCOPY, ELECTRON; OXIDATIVE STRESS; PENTOSE PHOSPHATE PATHWAY;

FUNGI; HUMICOLA LUTEA;

EID: 84870781457     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/w2012-112     Document Type: Article

References (62)

1. Al Abboud, M.A., and Alawlaqi, M.M. 2011. Biouptake of copper and their impact on fungal fatty acids. Aust. J. Basic Appl. Sci., 5(11): 283-290.
2. Angelova, M., Genova, L., Pashova, S., Slokoska, L., and Dolashka, P. 1996. Effect of cultural conditions on the synthesis of superoxide dismutase by Humicola lutea 110. J. Ferment. Bioeng. 82(5): 464-468. doi:10.1016/S0922-338X(97)86984-X.
3. Angelova, M.B., Pashova, S.B., Spasova, B.K., Vassilev, S.V., Slokoska, L.S., 2005. Oxidative stress response of filamentous fungi induced by hydrogen peroxide and paraquat. Mycol. Res. 109(2): 150 -158. doi:10.1017/S0953756204001352. PMID:15839099.
4. Araiza-Olivera, D., Sampedro, J.G., Mújica, A., Peña, A., and Uribe-Carvajal, S. 2010. The association of glycolytic enzymes from yeast confers resistance against inhibition by trehalose. FEMS Yeast Res. 10(3): 282-289. doi:10.1111/j.1567-1364.2010.00605.x. PMID:20148975.
5. Azevedo, M.-M., Almeida, B., Ludovico, P., and Cássio, F. 2009. Metal stress induces programmed cell death in aquatic fungi. Aquat. Toxicol. 92(4): 264-270. doi:10.1016/j.aquatox.2009.02.010. PMID:19297034.
6. Baldrain, P. 2010. Effect of heavy metal on saprotrophic soil fungi. In Soil heavy metals. Edited by Irena Sherameti and Ajit Varma. Springer-Verlag, Berlin, Germany. pp. 263-280.
7. Bellion, M., Courbot, M., Jacob, C., Blaudez, D., Chalot, M. 2006. Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol. Lett. 254(2): 173-181.doi:10.1111/j.1574-6968.2005.00044.x. PMID:16445743.
8. Belozerskaya, T., Aslanidi, K., Ivanova, A., Gessler, N., Egorova, A., Karpenko, Yu., and Olishevskaya, S. 2010. Characteristics of extremophylic fungi from chernobyl nuclear power plant. Vol. 1. In Current research, technology and education topics in applied microbiology and microbial biotechnology. Microbiology Series No. 2. Edited by A. Méndez-Vilas. Formatex, Badajoz, Spain. pp. 88-94.
9. Bergmeyer, H.U., and Moellering, H. 1983. Glucose-6-phosphate dehydrogenase. In Methods of enzymatic analysis. Vol. 3. Oxidoreductases, Transferases. 3rd ed. Edited by D.W. Moss. Verlag Chemie, Weinheim, Germany. pp. 191-197.
10. Bergmeyer, H.U., Graßl, M., and Walter, H.-E. 1983. Hexokinase. In Methods of enzymatic analysis. Vol. 2. Samples, reagents, assessment of results. 3rd ed. Edited by H.U. Bergmeyer. Verlag Chemie, Weinheim, Germany. pp. 222-223.
11. Bhattacharjee, S. 2012. The language of reactive oxygen species signaling in plants. J. Bot. 2012: 1-22. doi:10.1155/2012/985298.
12. Borkow, G., and Gabbay, J. 2005. Copper as a biocidal tool. Curr. Med. Chem. 12(18): 2163-2175. doi:10.2174/0929867054637617. PMID:16101497.
13. Briďziuvienė, D., Levinskaitė, L. 2007. Fungal tolerance towards copper-based wood preservatives. Biologija (Vilnius), 53(4): 54-61.
14. Chillappagari, S., Seubert, A., Trip, H., Kuipers, O.P., Marahiel, M.A., and Miethke, M. 2010. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J. Bacteriol. 192(10): 2512-2524. doi:10.1128/JB.00058-10. PMID:20233928.
15. Crichton, R.R. 2012. Metal assimilation pathways biological inorganic chemistry: a new introduction to molecular structure and function. 2nd ed. Elsevier B.V., Amsterdam, Netherlands. pp. 133-154.
16. Dávila Costa, J.S., Albarracín, V.H., Abate, C.M., Dávila. 2011. Responses of environmental Amycolatopsis strains to copper stress. Ecotoxicol. Environ. Saf. 74(7): 2020-2028. doi:10.1016/j.ecoenv.2011.06.017. PMID:21764453.
17. De Freitas, J., Wintz, H., Kim, J.H., Poynton, H., Fox, T., and Vulpe, C. 2003. Yeast, a model organism for iron and copper metabolism studies. Biometals, 16(1): 185-197. doi:10.1023/A:qj1020771000746. PMID:12572678.
18. Du, A., Cao, L., Zhang, R., and Pan, R. 2009. Effects of a copperresistant fungus on copper adsorption and chemical forms in soils. Water Air Soil Pollut. 201(1- 4): 99-107. doi:10.1007/s11270-008-9930-6.
19. Dupont, C.L., Grass, G., and Rensing, C. 2011. Copper toxicity and the origin of bacterial resistance - new insights and applications. Metallomics, 3(11): 1109-1118. doi:10.1039/c1mt00107h. PMID:21984219.
20. Espírito Santo, C., Taudte, N., Nies, D.H., and Grass, G. 2008. Contribution of copper ion resistance to survival of Escherichia coli on metallic copper surfaces. Appl. Environ. Microbiol. 74(4): 977-986. doi:10.1128/AEM.01938-07. PMID:18156321.
21. Fernandez, O., Béthencourt, L., Quero, A., Sangwan, R.S.C., and Clément, C. 2010. Trehalose and plant stress responses: Friend or foe? Trends Plant Sci. 15(7): 409-417. doi:10.1016/j.tplants.2010.04.004. PMID:20494608.
22. Ferrol, N., González-Guerrero, M., Valderas, A., Benabdellah, K., and Azcón-Aguilar, C. 2009. Survival strategies of arbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem. Rev. 8(3): 551-559. doi:10.1007/s11101-009-9133-9.
23. Fu, K., Liu, L., Fan, L., Liu, T., and Chen, J. 2010. Accumulation of copper in Trichoderma reesei transformants, constructed with the modified Agrobacterium tumefaciens-mediated transformation technique. Biotechnol. Lett. 32(12): 1815-1820. doi:10.1007/s10529-010-0365-y. PMID:20697931.
24. Gadd, G.M. 2007. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol. Res. 111(1): 3-49. doi:10.1016/j.mycres.2006.12.001. PMID:17307120.
25. Gaetke, L.M., and Chow, C.K. 2003. Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology, 189(1-2): 147-163.doi:10.1016/S0300-483X(03)00159-8. PMID:12821289.
26. Gancedo, C., and Flores, C.L. 2004. The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res. 4(4 -5): 351-359. doi:10.1016/S1567-1356(03)00222-8. PMID:14734015.
27. Gokhale, N.H., and Cowan, J.A. 2005. Inactivation of human angiotensin converting enzyme by copper peptide complexes containing ATCUN motifs. Chem. Commun. (Camb.), 47(47): 5916-5918. doi:10.1039/b511081e. PMID:16317474.
28. Green, F., III, and Clausen, C.A. 2003. Copper tolerance of brownrot fungi: time course of oxalic acid production. Int. Biodeterior. Biodegradation, 51(2): 145-149. doi:10.1016/S0964-8305(02)00099-9.
29. Guillén, Y., and Machuca, Á. 2008. The effect of copper on the growth of wood-rotting fungi and a blue-stain fungus. World J. Microbiol. Biotechnol. 24(1): 31-37. doi:10.1007/s11274-007- 9434-3.
30. Hefnawy, M.A., Ali, M.I., and Abdul- Ghanay, S.A. 2009. Influence of copper and cobalt stress on morphology and ultra-structure of Chaetomium globosum and Stachybotrys chartarum. Aust. J. Basic Appl. Sci., 3(4): 3158-3165.
31. Hirt, R.R. 1949. An isolate of Poria xantha on media containing copper. Phytopathologist, 39: 31-36.
32. 2. Methods Enzymol. 1: 705-707. doi:10.1016/0076-6879(55)01123-3.
33. Kosman, D.J. 2003. Molecular mechanisms of iron uptake in fungi. Mol. Microbiol. 47(5): 1185-1197. doi:10.1046/j.1365-2958.2003.03368.x. PMID:12603727.
34. Kostadinova, N., Vassilev, S., Spasova, B., and Angelova, M. 2011. Cold stress in Antarctic fungi targets enzymes of the glycolytic pathway and tricarboxylic acid cycle. Biotechnol. Biotechnol. Equip. 25(4): 50-57. doi:10.5504/bbeq.2011.0122.
35. Krumova, E., Dolashki, A., Pashova, S., Dolashka-Angelova, P., Stevanovic, S., Hristova, R., et al. 2008. Unusual location and characterization of Cu/Zn-containing superoxide dismutase from filamentous fungus Humicola lutea. Arch. Microbiol. 189(2): 121-130. doi:10.1007/s00203-007-0300-3. PMID:17805512.
36. Krumova, E.Z., Pashova, S.B., Dolashka-Angelova, P.A., Stefanova, T., and Angelova, M.B. 2009. Biomarkers of oxidative stress in the fungal strain Humicola lutea under copper exposure. Process Biochem. 44(3): 288-295. doi:10.1016/j.procbio.2008.10.023.
37. Kumar, V., Sahu, N.P., Pal, A.K., Kumar, S., Sinha, A.K., Ranjan, S.J., and Baruah, K. 2010. Modulation of key enzymes of glycolysis, gluconeogenesis, amino acid catabolism, and TCA cycle of the tropical freshwater fish Labeo rohita fed gelatinized and nongelatinized starch diet. Fish Physiol. Biochem. 36(3): 491-499.doi:10.1007/s10695-009-9319-5. PMID:19340598.
38. Landeweert, R., Hoffland, E., Finlay, R.D., Kuyper, T.W., and Van Breemen, N. 2001. Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol. Evol. 16(5): 248-254. doi:10.1016/S0169-5347(01)02122-X. PMID:11301154.
39. Lee, J., Adle, D., and Kim, H. 2006. Molecular mechanisms of copper homeostasis in yeast. In Molecular biology of metal homeostasis and detoxification: from microbes to man. Edited by M.J. Tamás and E. Martinoia. Springer-Verlag, Berlin, Germany. pp. 1-37.
40. Lin, C.M., Kosman, D.J. 1990. Copper uptake in wild type and copper metallothionein-deficient Saccharomyces cerevisiae. Kinetics and mechanism. J. Biol. Chem. 265(16): 9194-9200.PMID:2188974.
41. López-Millán, A.F., Sagardoy, R., Solanas, M., Abadía, A., and Abadía, J. 2009. Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ. Exp. Bot. 65(2-3): 376-385. doi:10.1016/j.envexpbot.2008.11.010.
42. Lorenc-Plucínska, G., and Stobrawa, K. 2005. Acclimation of popular trees to heavy metals in polluted habitats: I. Carbohydrate metabolism in fine roots of Populus deltoids. Acta Soc. Bot. Pol. 74(1): 11-16.
43. Lowry, O.H., Rosenbrough, N.J., Farr, A.L., and Randall, R.J. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193(1): 265-275.PMID:14907713.
44. Peña, M.M.O., Lee, J., and Thiele, D.J. 1999. A delicate balance: homeostatic control of copper uptake and distribution. J. Nutr. 129(7): 1251-1260.PMID:10395584.
45. Price, M.S., Classen, J.J., and Payne, G.A. 2001. Aspergillus niger absorbs copper and zinc from swine wastewater. Bioresour. Technol. 77(1): 41-49. doi:10.1016/S0960-8524(00)00135-8. PMID:11211074.
46. Quinn, J. 2008. Differences in stress responses between model and pathogenic fungi. In Stress in yeasts and filamentous fungi. Edited by Simon Avery, M. Stratford, and P. Van West. Academic Press, London, UK. pp. 67-86.
47. Rutherford, J.C., and Bird, A.J. 2004. Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot. Cell, 3(1): 1-13. doi:10.1128/EC.3.1.1-13.2004. PMID:14871932.
48. Shafirovich, V., and Geacintov, N.E. 2010. Role of free radical reactions in the formation of DNA damage. In The chemical biology of DNA damage. Edited by N.E. Geacintov and S. Broyde. WILEY-VCH Verlag GmbH&Co. KGaA, Berlin, Germany. pp. 81-104.
49. Shanker, A.K. 2008. Mode of action and toxicity of trace elements. In Trace elements as contaminants and nutrients: consequences in ecosystems and human health. Edited by M.N.V. Prasad. John Wiley & Sons, Inc., Hoboken, N.J., USA. pp. 523-554.
50. Shanmuganathan, A., Avery, S.V., Willetts, S.A., and Houghton, J.E. 2004. Copper-induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway. FEBS Lett. 556(1-3): 253-259. doi:10.1016/S0014-5793(03)01428-5.PMID:14706859.
51. Sharma, S.S., and Dietz, K.-J. 2009. The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci. 14(1): 43-50. doi:10.1016/j.tplants.2008.10.007. PMID:19070530.
52. Smith, A.F. 1983. Malate dehydrogenase. Vol. 3. Oxidoreductases, Transferases. 3rd ed. In Methods of enzymatic analysis. Edited by H.U. Bergmeyer and M. Grassl Verlag Chemie, Weinheim, Germany. pp. 163-171.
53. Srivastava, A.K., Bhargava, P., and Rai, L.C. 2005. Salinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolum. World J. Microbiol. Biotechnol. 21(6 -7): 1291-1298. doi:10.1007/s11274-005-2442-2.
54. Tarhanen, S. 1998. Ultrastructural responses of the lichen Bryoria fuscescens to simulated acid rain and heavy metal deposition. Ann. Bot. (Lond.), 82(6): 735-746. doi:10.1006/anbo.1998.0734.
55. Thannickal, V.J., and Fanburg, B.L. 2000. Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 279(6): L1005-L1028.PMID:11076791.
56. Tsekova, K., and Galabova, D. 2003. Phosphatase production and activity in copper (II) accumulating Rhizopus delemar. Enzyme Microb. Technol. 33(7): 926-931. doi:10.1016/j.enzmictec.2003.06.001.
57. Tsekova, K.V., Marinov, P.G., and Tzekova, A.N. 2000. Copper accumulation by Aspergillus awamori. Folia Microbiol. (Praha), 45(3): 217-220. doi:10.1007/BF02908947. PMID:11271803.
58. Uauy, R., Olivares, M., and Gonzalez, M. 1998. Essentiality of copper in humans. Am. J. Clin. Nutr. 67(Suppl.): 952S-959S.PMID:9587135.
59. Vacchina, V., Baldrian, P., Gabriel, J., and Szpunar, J. 2002. Investigation of the response of wood-rotting fungi to copper stress by size-exclusion chromatography and capillary zone electrophoresis with ICP M.S. detection. Anal. Bioanal. Chem. 372(3): 453-456.doi:10.1007/s00216-001-1104-y. PMID:11939533.
60. Wang, S., Teng, S., and Fan, M. 2010. Interaction between heavy metals and aerobic granular sludge. In Environmental management. Edited by Santosh Kumar Sarkar. Sciyo, Croatia. pp. 173-188.
61. Yoon, J.J., Hattori, T., and Shimada, M. 2002. A metabolic role of the glyoxylate and tricarboxylic acid cycles for development of the copper-tolerant brown-rot fungus Fomitopsis palustris. FEMS Microbiol. Lett. 217(1): 9-14. doi:10.1111/j.1574-6968.2002.tb11449.x. PMID:12445639.
62. Zhou, J., Melman, G., Pita, M., Ornatska, M., Wang, X., Melman, A., and Katz, E. 2009. Biomolecular oxidative damage activated by enzymatic logic systems: biologically inspired approach. ChemBioChem, 10(6): 1084-1090. doi:10.1002/cbic.200800833. PMID:19308926.