Oxidative stress in entomopathogenic fungi grown on insect-like hydrocarbons

Current Genetics

Volumn 61, Issue 3, 2015, Pages 289-297

  Huarte Bonnet, Carla ^a   Juárez, M Patricia ^a   Pedrini, Nicolás ^a  

^a INSTITUTO DE INVESTIGACIONES BIOQUÍMICAS DE LA PLATA INIBIOLP   (Argentina)

Author keywords

Alkane degradation; Antioxidant enzymes; Beauveria bassiana; Reactive oxygen species

Indexed keywords

CATALASE; GLUTATHIONE PEROXIDASE; HYDROCARBON; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; UNSPECIFIC MONOOXYGENASE; ALKANE; ANTIOXIDANT; FUNGAL PROTEIN;

ARTICLE; BEAUVERIA BASSIANA; DEGRADATION; ENTOMOPATHOGENIC FUNGUS; FUNGAL GENE; LIPID METABOLISM; LIPID PEROXIDATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; ENERGY METABOLISM; FUNGUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; INSECT; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION;

CORDYCEPS BASSIANA; FUNGI; HEXAPODA;

ALKANES; ANIMALS; ANTIOXIDANTS; ENERGY METABOLISM; FUNGAL PROTEINS; FUNGI; HOST-PATHOGEN INTERACTIONS; HYDROCARBONS; INSECTS; OXIDATION-REDUCTION; OXIDATIVE STRESS;

EID: 84937973357     PISSN: 01728083     EISSN: 14320983     Source Type: Journal    
DOI: 10.1007/s00294-014-0452-z     Document Type: Article

References (52)

1. Alconada TM, Juárez MP (2006) Acyl-CoA oxidase activity from Beauveria bassiana, an entomopathogenic fungus. J Basic Microbiol 46:435–443
2. Ali S, Huang Z, Li H, Bashir MH, Ren S (2013) Antioxidant enzyme influences germination, stress tolerance, and virulence of Isaria fumosorosea. J Basic Microbiol 53:489–497
3. Baud O, Greene AE, Li J, Wang H, Volpe JJ, Rosenberg PA (2004) Glutathione peroxidase–catalase cooperativity is required for resistance to hydrogen peroxide by mature rat oligodendrocytes. J Neurosci 4(7):1531–1540
4. Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140
5. Bizzi A, Veneroni E, Tacconi MT, Codegoni AM, Pagani R, Cini M, Garattini S (1980) Accumulation and metabolism of uneven fatty acids present in single cell protein. Toxicol Lett 5:227–240
6. Boucias DG, Pendland JC (1991) The fungal cell wall and its involvement in the pathogenic process in insect hosts. In: Latge JP, Boucias DG (eds) Fungal cell wall and immune response, vol H53. Springer, Berlin, pp 303–316
7. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–309
8. Chen Q, Nijenhuis A, Preusting H, Dolfing J, Janssen DB, Witholt B (1995) Effects of octane on the fatty acid composition and transition temperature of Pseudomonas oleovorans membrane lipids during growth in two-liquid-phase continuous culture. Enzyme Microb Technol 17:647–652
9. Crespo R, Juárez MP, Cafferata LFR (2000) Biochemical interaction between entomopathogenous fungi and their host-like hydrocarbons. Mycologia 92:528–536
10. Crespo R, Juárez MP, Dal Bello GM, Padín S, Calderón Fernández G, Pedrini N (2002) Increased mortality of Acanthoscelides obtectus by alkane-grown Beauveria bassiana. Biocontrol 47:685–696
11. Fang GC, Hanau RM, Vaillancourt LJ (2002) The SOD2 gene, encoding a manganese-type superoxide dismutase, is upregulated during conidiogenesis in the plant-pathogenic fungus Colletotrichum graminicola. Fungal Genet Biol 36:155–165
12. Ferron P (1985) Fungal control. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Academic Press, New York, pp 313–346
13. Forlani L, Juárez MP, Lavarías S, Pedrini N (2014) Toxicological and biochemical response of the entomopathogenic fungus Beauveria bassiana after exposure to deltamethrin. Pest Manag Sci 70:751–756
14. Freimoser FM, Hu G, St Leger RJ (2005) Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro. Microbiology 151:361–371
15. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112
16. Habig W, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases. J Biol Chem 249:7130–7139
17. Hansberg W, Aguirre J (1990) Hyperoxidant states cause microbial cell differentiation by cell isolation from dioxygen. J Theor Biol 142(2):201–221
18. Inoue Y, Matsuda T, Sugiyama K, Izawa S, Kimura A (1999) Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae. J Biol Chem 274:27002–27009
19. Juárez MP, Crespo R, Calderón-Fernández G, Lecuona RE, Cafferata LFR (2000) Characterization and carbon metabolism in fungi pathogenic to Triatoma infestans, a Chagas disease vector. J Invertebr Pathol 76:198–207
20. Juárez MP, Pedrini N, Crespo R (2004) Mycoinsecticides against Chagas disease vectors: biochemistry involved in insect host hydrocarbon degradation. In: Mas-Comas S (ed) Multidisciplinarity for parasites, vectors and parasitic diseases. Monduzzi Editore, Bologna, pp 137–142
21. Karlsson M, Stenlid J, Olson A (2005) Identification of a superoxide dismutase gene from the conifer pathogen Heterobasidion annosum. Physiol Mol Plant Pathol 66:99–107
22. Ketterer B, Coles B, Meyer DJ (1983) The role of glutathione in detoxification. Environ Health Perspect 49:59–69
23. Lecuona RE, Clement J-L, Riba G, Joulie C, Juárez MP (1997) Spore germination and hyphal growth of Beauveria sp. on insect lipids. J Econ Entomol 89:119–123
24. Mantilla JG, Galeano NF, Gaitan AL, Cristancho MA, Keyhani NO, Gongora CE (2012) Comparative transcriptome analysis of the entomopathogenic fungus Beauveria bassiana grown on the coffee berry borer (Hypothenemus hampei). Microbiology 158:1826–1842
25. Marklund SL, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474
26. Michán S, Lledías F, Baldwin JD, Natvig DO, Hansberg W (2002) Regulation and oxidation of two large monofunctional catalases. Free Radic Biol Med 33:521–532
27. Michán S, Lledías F, Hansberg W (2003) Asexual development is increased in Neurospora crassa cat-3-null mutant strains. Eukaryot Cell 2(4):798–808
28. Michiels C, Raes M, Toussaint O, Remacle J (1994) Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic Biol Med 17(3):235–248
29. Missall TA, Cherry-Harris JF, Lodge JK (2005) Two glutathione peroxidases in the fungal pathogen Cryptococcus neoformans are expressed in the presence of specific substrates. Microbiology 151:2573–2581
30. Morales Hernandez CE, Padilla Guerrero IE, Gonzalez Hernandez GA, Salazar Solis E, Torres Guzman JC (2010) Catalase overexpression reduces the germination time and increases the pathogenicity of the fungus Metarhizium anisopliae. Appl Microbiol Biotechnol 87:1033–1044
31. Mylonas C, Kouretas D (1999) Lipid peroxidation and tissue damage. Vivo 13(3):295–309
32. Napolitano R, Juárez MP (1997) Entomopathogenous fungi degrade epicuticular hydrocarbons of Triatoma infestans. Arch Biochem Biophys 334:208–214
33. Pedrini N, Juárez M, Crespo R, de Alaniz MJT (2006) Clues on the role of Beauveria bassiana catalases in alkane degradation events. Mycologia 98:528–534
34. Pedrini N, Crespo R, Juarez MP (2007) Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comp Biochem Physiol 146C:124–137
35. Pedrini N, Mijailovsky SJ, Girotti JR, Stariolo R, Cardozo RM, Gentile A, Juárez MP (2009) Control of pyrethroid-resistant Chagas disease vectors with entomopathogenic fungi. PLoS Negl Trop Dis 3(5):e434. doi:10.1371/journal.pntd.0000434
36. Pedrini N, Zhang S, Juárez MP, Keyhani NO (2010) Molecular characterization and expression analysis of a suite of cytochrome P450 enzymes implicated in insect hydrocarbon degradation in the entomopathogenic fungus Beauveria bassiana. Microbiology 156:2549–2557
37. Pedrini N, Ortiz-Urquiza A, Huarte-Bonnet C, Zhang S, Keyhani NO (2013) Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: hydrocarbon oxidation within the context of a host-pathogen interaction. Front Microbiol 4:24. doi:10.3389/fmicb.2013.00024
38. Saito T, Aoki J (1983) Toxicity of free fatty acids on the larval surfaces of two lepidopterous insects towards Beauveria bassiana (Bals.) and Paecilomyces fumosoroseus (Wize) Brown et Smith (Deuteromycetes: Moniliales). Appl Entomol Zool 18:225–233
39. Scheller U, Zimmer T, Becher D, Schauer F, Schunck W-H (1998) Oxygenation cascade in conversion of n-alkanes to α, ω-dioic acids catalyzed by cytochrome P450 52A3. J Biol Chem 273:32528–32534
40. Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16
41. Smith RJ, Grula A (1981) Nutritional requirements for conidial germination and hyphal growth of Beauveria bassiana. J Invertebr Pathol 37:222–230
42. St. Leger RJ, Cooper RM, Charnley AK (1986a) Cuticle-degrading enzymes of entomopathogenic fungi: cuticle degradation in vitro by enzymes from entomopathogens. J Invertebr Pathol 47:167–177
43. St. Leger RJ, Charnley AK, Cooper RM (1986b) Cuticle-degrading enzymes of entomopathogenic fungi: synthesis in culture on cuticle. J Invertebr Pathol 48:85–95
44. Toledo I, Noronha-Dutra AA, Hansberg W (1991) Loss of NAD(P)-reducing power and glutathione disulfide excretion at the start of induction of aerial growth in Neurospora crassa. J Bacteriol 173:3243–3249
45. Toledo I, Rangel P, Hansberg W (1995) Redox imbalance at the start of each morphogenetic step of Neurospora crassa conidiation. Arch Biochem Biophys 319:519–524
46. Wang H, Le Dall M-T, Waché Y, Laroche P, Belin J-M, Gaillardin C, Nicaud J-M (1999) Cloning, sequencing, and characterization of five genes coding for Acyl-CoA oxidase isozymes in the yeast Yarrowia lipolytica. Cell Biochem Biophys 31:165–174
47. Wang ZS, Gu YX, Yuan QS (2006) Effect of nutrition factors on the synthesis of superoxide dismutase, catalase, and membrane lipid peroxide levels in Cordyceps militaris mycelium. Curr Microbiol 52:74–79
48. Wang Z-L, Zhang L-B, Ying S-H, Feng M-G (2013) Catalases play differentiated roles in the adaptation of a fungal entomopathogen to environmental stresses. Environ Microbiol 15(2):409–418
49. Xiao G, Ying S-H, Zheng P, Wang Z-L, Zhang S, Xie X-Q et al (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483. doi:10.1038/srep00483
50. Xie XQ, Ying SH, Feng MG (2010) Characterization of a new Cu/Zn-superoxide dismutase from Beauveria bassiana and two site-directed mutations crucial to its antioxidation activity without chaperon. Enzyme Microb Technol 46:217–222
51. Xie X-Q, Li F, Ying S-H, Feng M-G (2012) Additive contributions of two manganese-cored superoxide dismutases (MnSODs) to antioxidation, UV tolerance and virulence of Beauveria bassiana. PLoS One 7(1):e30298. doi:10.1371/journal.pone.0030298
52. Zhang S, Widemann E, Bernard G, Lesot A, Pinot F, Pedrini N, Keyhani NO (2012) CYP52X1, representing new cytochrome P450 subfamily, displays fatty acid hydroxylase activity and contributes to virulence and growth on insect cuticular substrates in entomopathogenic fungus Beauveria bassiana. J Biol Chem 287:13477–13486