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

Zhang, Shizhu; Widemann, Émilie; Grausem, Bernard; Lesot, Agnés; Pinot, Franck; Pedrini, Nicolás; Keyhani, Nemat O.

doi:10.1074/jbc.m111.338947

Cited by 101 publications

(77 citation statements)

References 47 publications

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“…However, entomopathogenic fungi are incapable of lignin degradation, and no information is available regarding the presence and/or function of these enzymes in this group of fungi. However, entomopathogenic fungi are able to assimilate various hydrocarbon and lipid components of the insect cuticle, responding to surface cues on their hosts to initiate programs for infection (41)(42)(43).…”

Section: Significancementioning

confidence: 99%

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

Pedrini

Ortiz‐Urquiza

Huarte‐Bonnet

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Entomopathogenic fungi and their insect hosts represent a model system for examining invertebrate-pathogen coevolutionary selection processes. Here we report the characterization of competing components of an arms race consisting of insect protective antimicrobial compounds and evolving fungal mechanisms of detoxification. The insect pathogenic fungus Beauveria bassiana has a remarkably wide host range; however, some insects are resistant to fungal infection. Among resistant insects is the tenebrionid beetle Tribolium castaneum that produces benzoquinone-containing defensive secretions. Reduced fungal germination and growth was seen in media containing T. castaneum dichloromethane extracts or synthetic benzoquinone. In response to benzoquinone exposure, the fungus expresses a 1,4-benzoquinone oxidoreductase, BbbqrA, induced >40-fold. Gene knockout mutants (ΔBbbqrA) showed increased growth inhibition, whereas B. bassiana overexpressing BbbqrA (Bb::BbbqrAO) displayed increased resistance to benzoquinone compared with wild type. Increased benzoquinone reductase activity was detected in wild-type cells exposed to benzoquinone and in the overexpression strain. Heterologous expression and purification of BbBqrA in Escherichia coli confirmed NAD(P)H-dependent benzoquinone reductase activity. The ΔBbbqrA strain showed decreased virulence toward T. castaneum, whereas overexpression of BbbqrA increased mortality versus T. castaneum. No change in virulence was seen for the ΔBbbqrA or Bb::BbbqrAO strains when tested against the greater wax moth Galleria mellonella or the beetle Sitophilus oryzae, neither of which produce significant amounts of cuticular quinones. The observation that artificial overexpression of BbbqrA results in increased virulence only toward quinone-secreting insects implies the lack of strong selection or current failure of B. bassiana to counteradapt to this particular host defense throughout evolution.

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Section: Significancementioning

confidence: 99%

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

Pedrini

Ortiz‐Urquiza

Huarte‐Bonnet

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

120

118

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“…Fungal infection is percutaneous, with conidia attaching and germinating on the host cuticle (Holder & Keyhani, 2005). The growing hyphae penetrate the cuticle via expression of a host of cuticle-degrading enzymes, ultimately reaching the insect haemocoel (Fang et al, 2009;Zhang et al, 2012). Once inside the haemocoel, the fungus undergoes a dimorphic transition, elaborating in vivo cells termed hyphal bodies that are able to evade the host immune system and consume the nutrients available in the haemocoel (Wanchoo et al, 2009;Lewis et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

The autophagy gene BbATG5, involved in the formation of the autophagosome, contributes to cell differentiation and growth but is dispensable for pathogenesis in the entomopathogenic fungus Beauveria bassiana

et al. 2013

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Autophagy is a highly conserved process, representing the major eukaryotic degradative pathway of cellular components. Autophagy-mediated recycling of cellular materials contributes to cell differentiation, tissue remodelling and proper development. In fungi, autophagy is required for normal growth and cell differentiation. The entomopathogenic fungus Beauveria bassiana and its invertebrate targets represent a unique model system with which to examine host-pathogen interactions. The ATG5 gene is one of 17 involved in autophagosome formation, and the B. bassiana homologue (BbATG5) was identified. The role of autophagy in B. bassiana growth and virulence was investigated via construction of a targeted gene knockout of BbATG5. The mutant strain displayed increased sensitivity to nutrient limitation, with decreased germination and growth as compared with the wild-type parent. Conidiation was severely compromised and conidia derived from the DBbATG5 strain were altered in morphology. Cell differentiation into blastospores was also greatly reduced. Despite the significant growth and developmental defects, insect bioassays using the oriental leafworm moth, Spodoptera litura, indicated a modest (~40 %) decrease in virulence in the DBbATG5 strain. The phenotypic defects of the DBbATG5 strain could be restored by introduction of an intact copy of BbATG5. These data suggest that unlike several plant and animal pathogenic fungi, where ATG5 is required for infection, in B. bassiana it is dispensable for pathogenesis.

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“…CYP52N1 displayed similar substrate specificity to CYP52M1, but it only catalyzed -hydroxylation of fatty acids, and CYP52E3 has minor -hydroxylation activity toward myristic acid, palmitic acid, palmitoleic acid, and oleic acid. Finally, CYP52X1 showed highest activity against medium-chain fatty acids (C 12:0 and C 14:0 ) and resembles subgroups A3 to A5 with regard to chain length preference (26).…”

Section: Discussionmentioning

confidence: 95%

Expression and Characterization of CYP52 Genes Involved in the Biosynthesis of Sophorolipid and Alkane Metabolism from Starmerella bombicola

Huang

Peter

Schwab

2014

Appl Environ Microbiol

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Three cytochrome P450 monooxygenase CYP52 gene family members were isolated from the sophorolipid-producing yeast Starmerella bombicola (former Candida bombicola), namely, CYP52E3, CYP52M1, and CYP52N1, and their open reading frames were cloned into the pYES2 vector for expression in Saccharomyces cerevisiae. The functions of the recombinant proteins were analyzed with a variety of alkane and fatty acid substrates using microsome proteins or a whole-cell system. CYP52M1 was found to oxidize C 16 to C 20 fatty acids preferentially. It converted oleic acid (C 18:1 ) more efficiently than stearic acid (C 18:0 ) and linoleic acid (C 18:2 ) and much more effectively than ␣-linolenic acid (C 18:3 ). No products were detected when C 10 to C 12 fatty acids were used as the substrates. Moreover, CYP52M1 hydroxylated fatty acids at their -and -1 positions. CYP52N1 oxidized C 14 to C 20 saturated and unsaturated fatty acids and preferentially oxidized palmitic acid, oleic acid, and linoleic acid. It only catalyzed -hydroxylation of fatty acids. Minor -hydroxylation activity against myristic acid, palmitic acid, palmitoleic acid, and oleic acid was shown for CYP52E3. Furthermore, the three P450s were coassayed with glucosyltransferase UGTA1. UGTA1 glycosylated all hydroxyl fatty acids generated by CYP52E3, CYP52M1, and CYP52N1. The transformation efficiency of fatty acids into glucolipids by CYP52M1/UGTA1 was much higher than those by CYP52N1/UGTA1 and CYP52E3/UGTA1. Taken together, CYP52M1 is demonstrated to be involved in the biosynthesis of sophorolipid, whereas CYP52E3 and CYP52N1 might be involved in alkane metabolism in S. bombicola but downstream of the initial oxidation steps.

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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

Cited by 101 publications

References 47 publications

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen

The autophagy gene BbATG5, involved in the formation of the autophagosome, contributes to cell differentiation and growth but is dispensable for pathogenesis in the entomopathogenic fungus Beauveria bassiana

Expression and Characterization of CYP52 Genes Involved in the Biosynthesis of Sophorolipid and Alkane Metabolism from Starmerella bombicola

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