- Email: [email protected]
Antioxidant and antibacterial activities of the chlorine pigment sclerotiorin from Penicillium mallochii and its chemotaxonomic significance
Biochemical Systematics and Ecology 86 (2019) 103915
Contents lists available at ScienceDirect
Biochemical Systematics and Ecology journal homepage: www.elsevier.com/locate/biochemsyseco
Antioxidant and antibacterial activities of the chlorine pigment sclerotiorin from Penicillium mallochii and its chemotaxonomic significance
T
Patrícia O. dos Santosa,∗∗, Caline G. Ferrazb,∗, Paulo R. Ribeiroc, Fabricio M. Mirandab, Franceli da Silvab, Jorge T. de Souzad, Milton R. de A. Roquee, Ana C.F. Soaresb a
Instituto Federal Baiano, R. Glicério Taváres, S/n - Bate-quente, Valença, BA, Brazil Universidade Federal do Recôncavo da Bahia, R. Rui Barbosa, 710, Cruz das Almas, BA, Brazil c Metabolomics Research Group, Departamento de Química Orgânica, Instituto de Química, Universidade Federal da Bahia, Rua Barão de Jeremoabo S/n, 40170-115, Salvador, Brazil d Department of Plant Pathology, Universidade Federal de Lavras Lavras, MG, 37200-000, Brazil e Universidade Federal da Bahia, Instituto de Ciências da Saúde, Vale do Canela, Salvador, BA, Brazil b
ARTICLE INFO
ABSTRACT
Keywords: Bioactive compounds Endophytes Penicillium Pigments
Penicillium mallochii was isolated as an endophyte from Himatanthus sp. and inoculated in liquid potato-dextrose culture medium, with adjusted to pH 3.6, and incubated for 10 days at 24 °C. Successive column chromatography of the hexane extract afforded the chlorine pigment sclerotiorin. Its structure was determined by NMR and by comparison with the literature. Sclerotiorin showed moderate antioxidant activity and moderate antibacterial against Bacillus subtilis, Staphylococcus aureus, and Micrococcus luteus. The isolation of sclerotiorin from P. mallochii support the taxonomic classification within the Penicillium genus, demonstrating a closer evolutionary relationship among the Penicillium species. Therefore, we suggest that sclerotiorin and the sclerotiorin group of metabolites may be used as chemotaxonomic markers for proper identification of Penicillium species.
1. Subject and source
2. Previous work
Species of ascomycetous fungi Penicillium have worldwide distribution inhabiting a diverse panel of environments such as air, soil, and living in association with plants and food products (Santini et al., 2014; Yadav et al., 2018). They are protagonists in a wide range of natural processes, such as decomposing organic matter in natural environments or even causing destructive damages in the food industry (Visagie et al., 2014). Additionally, they are well-known for their production of mycotoxins and pigments (Lebeau et al., 2017; Visagie et al., 2014). Therefore, they present great potential for biotechnological and industrial applications. Penicillium mallochii was isolated as an endophyte from Himatanthus sp. Collected at the Chapada do Araripe – Ceará State, Brazil (−40°12′6″S, 40°1′55″W). The endophyte isolated from Himatanthus sp was identified based the comparison of its cytochrome oxidase 1, internal transcribed spacer, β-tubulin, translation elongation factor 1-α, and calmodulin sequences amplified by PCR with those deposited on GenBank for Penicillium mallochii.
Some studies related to Penicillium mallochii have been published, but none describing the assessment of its chemical composition (Man et al., 2018; Poitevin et al., 2018; Rivera et al., 2012; Rivera and Seifert, 2011; Wang et al., 2017).
∗
3. Present study Penicillium mallochii was inoculated in liquid potato-dextrose culture medium, with adjusted to pH 3.6, and incubated for 10 days at 24 °C. The metabolites produced by the mycelium were extracted by partitioning in hexane. The hexane extract (18.05 g) was subjected to successive column chromatography (60 × 10 cm i.d. column, Merck silica gel 230–400 mesh) eluting with a gradient of hexane and methanol to afford sclerotiorin (Fig. 1). Its structure was determined by NMR (Table 1) and by comparison of its spectral data with those reported previously in the literature (Chidananda and Sattur, 2007). Antioxidant activity was performed by using the 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenge assay as described in Pereira et al. (2014),
Corresponding author. Corresponding author. E-mail addresses: [email protected] (P. O. dos Santos), [email protected] (C.G. Ferraz).
∗∗
https://doi.org/10.1016/j.bse.2019.103915 Received 20 April 2019; Received in revised form 29 May 2019; Accepted 15 June 2019 0305-1978/ © 2019 Elsevier Ltd. All rights reserved.
Biochemical Systematics and Ecology 86 (2019) 103915
P. O. dos Santos, et al.
((3E,5E)-5,7-dimethyl-2-methylenenona-3, 5-dienyl)-2,4-dihydroxy-3methylbenzaldehyde (5)) isolated from P. citreonigrum (Wang et al., 2010). Wortmin is a member of the sclerotiorin group of metabolites, but this metabolite has been isolated from P. wortmanni Klöcker (Merlini et al., 1973), which belongs to the genus Talaromyces. Although Penicillium species present unique morphotaxonomic structures, the identification at species levels is still difficult. The taxonomic identification of Penicillium species show complex challenges and usually more than one approach is necessary to ensure proper classification (Lund and Frisvad, 1994). This multiplatform approach encompasses morphological, biochemical, and molecular analysis (Lund and Frisvad, 1994). Therefore, chemotaxonomic traits may greatly contribute for the classification of Penicillium species. The isolation of sclerotiorin from P. mallochii provide further evidence to support the taxonomic classification of Penicillium genus, demonstrating a closer evolutionary relationship among the Penicillium species. Therefore, we suggest that sclerotiorin and the sclerotiorin group of metabolites may be used as chemotaxonomic markers for proper identification of Penicillium species.
Fig. 1. Chemical structure of sclerotiorin. Table 1 1 H (500 MHz) and13C NMR (125 MHz) spectral data of sclerotiorin in CDCl3. Position
δH (J in Hz)
δC
gHMBC
1
7.94 (1H, s)
152.63
3 4 4a 5 6 7 8 8a 9
– 6.65 (1H, s) – – – – –
158.09 106.34 114.50 138.70 191.72 84.54 185.94 110.70 115.62
C-2, C-3, C-4, C-5, C-6, C-8a
COSY
C-2, C-4, C-6, C-8a
Acknowledgements
13
6.07 (1H, d, 15.65 Hz) 7.06 (1H, d, 15.65 Hz) – 5.70 (1H, d, 9.80 Hz) 2.48 (1H, m)
14a
1.32 (1H, m)
30.02
C-10, C-13, C-14, C16, C-17 C-11, C-12. C-14, C15, C-16 C-12, C-13, C-15, C-16
14b 15
1.44 (1H, 0.87 (3H, 7.40 Hz) 1.01 (3H, 6.65 Hz) 1.85 (3H, 1.57 (3H, – 2.17 (3H,
m) t,
– 11.92
C-12, C-13, C-15, C-16 C-13, C-14, C-16
H-14b, H-15, H-16 H-14a, H-15 H-14a, H-14b
d,
20.16
C-13, C-14, C-16
H-13
s) s)
12.32 22.50 170.06 20.03
C-11, C-12, C-13 C-6, C-7, C-8
H-12
10 11 12
16 17 18 19 20
s)
142.85 131.93 148.83 35.09
Financial support was provided by FINEP, CAPES, CNPq, and FAPESB. We thank the Nuclear Magnetic Resonance (NMR) Facility at Brazilian Biosciences National Laboratory (LNBio), for the use of the NMR spectrometer (500 MHz, Agilent DD2).
C-2, C-3, C-10, C-11
H-10
C-2, C-3, C-9, C-11, C12, C-17
H-9 H-13, H-17
Appendix A. Supplementary data
H-12
Supplementary data to this article can be found online at https:// doi.org/10.1016/j.bse.2019.103915. References Birkinshaw, J.H., 1952. Studies in the biochemistry of micro-organisms. Metabolic products of Penicillium multicolor G.-M. and P. with special reference to sclerotiorin. Biochem. J. 52, 283–288. Chidananda, C., Sattur, A.P., 2007. Sclerotiorin, a novel inhibitor of lipoxygenase from Penicillium frequentans. J. Agric. Food Chem. 55, 2879–2883. Curtin, T.P., Reilly, J., 1940. Sclerotiorin, C20H21O5Cl, a chlorine-containing metabolic product of Penicillium sclerotiorin. Biochem. J. 34. Gray, R.W., Whalley, W.B., 1970. (-)-7-Epi-5-chloroisorotiorin, a novel metabolite of the sclerotiorin group. J. Chem. Soc. D Chem. Commun. 762. Gray, R.W., Whalley, W.B., 1971. The chemistry of fungi. Part LXIII. Rubrorotiorin, a metabolite of Penicillium hirayamae Udagawa. J. Chem. Soc. C: Org. Chem. 3575–3577. Lebeau, J., Venkatachalam, M., Fouillaud, M., Petit, T., Vinale, F., Dufossé, L., Caro, Y., 2017. Production and new extraction method of polyketide red pigments produced by ascomycetous fungi from terrestrial and marine habitats. J. Fungi 3. Lund, F., Frisvad, J.C., 1994. Chemotaxonomy of Penicillium aurantiogriseum and related species. Mycol. Res. 98, 481–492. Man, B., Wang, H., Yun, Y., Xiang, X., Wang, R., Duan, Y., Cheng, X., 2018. Diversity of fungal communities in Heshang Cave of Central China revealed by mycobiome-sequencing. Front. Microbiol. 9. Merlini, L., Mondelli, R., Nasini, G., Hesse, M., 1973. Structure of wortmin, a new metabolite from Penicillium wortmanni. Helv. Chim. Acta 56, 232–239. Pereira, E.P.L., Ribeiro, P.R., Loureiro, M.B., de Castro, R.D., Fernandez, L.G., 2014. Effect of water restriction on total phenolics and antioxidant properties of Amburana cearensis (Fr. Allem) A.C. Smith cotyledons during seed imbibition. Acta Physiol. Plant. 36, 1293–1297. Poitevin, C.G., Porsani, M.V., Poltronieri, A.S., Zawadneak, M.A.C., Pimentel, I.C., 2018. Fungi isolated from insects in strawberry crops act as potential biological control agents of duponchelia fovealis (Lepidoptera: Crambidae). Appl. Entomol. Zool 53, 323–331. Rivera, K.G., Díaz, J., Chavarría-Díaz, F., Garcia, M., Urb, M., Thorn, R.G., Louis-Seize, G., Janzen, D.H., Seifert, K.A., 2012. Penicillium mallochii and P. guanacastense two new species isolated from Costa Rican caterpillars. Mycotaxon 119, 315–328. Rivera, K.G., Seifert, K.A., 2011. A taxonomic and phylogenetic revision of the Penicillium sclerotiorum complex. Stud. Mycol. 70, 139–158. Santini, A., Mikušová, P., Sulyok, M., Krska, R., Labuda, R., Šrobárová, A., 2014. Penicillium strains isolated from Slovak grape berries taxonomy assessment by secondary metabolite profile. Mycotoxin Res. 30, 213–220. Santos, P.M., Batista, D.L.J., Ribeiro, L.A.F., Boffo, E.F., de Cerqueira, M.D., Martins, D., de Castro, R.D., de Souza-Neta, L.C., Pinto, E., Zambotti-Villela, L., Colepicolo, P., Fernandez, L.G., Canuto, G.A.B., Ribeiro, P.R., 2018. Identification of antioxidant and
C-19
*Carbonyl groups were assigned based on their δC.
whereas antibacterial activity was performed against Bacillus cereus, B. subtilis, Staphylococcus aureus, and Micrococcus luteus as described in Santos et al. (2018). Sclerotiorin (IC50 of 78.12 ± 2.82 μg mL−1) showed moderate antioxidant activity as compared to the positive control gallic acid (IC50 of 1.26 ± 0.02 μg mL−1). Sclerotiorin also showed moderate antibacterial against B. subtilis (MIC of 200 μg mL−1), Staphylococcus aureus (MIC of 200 μg mL−1), and Micrococcus luteus (MIC of 100 μg mL−1) as compared to the positive control chloramphenicol. Chloramphenicol showed MIC of 1.56 μg mL−1 for B. subtilis, 6.25 μg mL−1 for S. aureus, and 3.12 μg mL−1 for M. luteus. No activity as detected for against Bacillus cereus for concentrations equal or lower than 200 μg mL−1. 4. Chemotaxonomic importance Sclerotiorin is a unusual pigment first obtained from the mycelium of Penicillium sclerotiorum (Curtin and Reilly, 1940). Later it was obtained from P. multicolor (Birkinshaw, 1952), P. hirayamae (Udagawa, 1963), P. frequentans (Chidananda and Sattur, 2007), and P. citreonigrum (Wang et al., 2010). Sclerotiorin is also the main component of the sclerotiorin group of metabolites which includes rubrorotiorin, isolated from P. hirayamae (Gray and Whalley, 1970, 1971), sclerotioramine, ochrephilone, dechloroisochromophilone III and IV, pencolide, and 62
Biochemical Systematics and Ecology 86 (2019) 103915
P. O. dos Santos, et al. antimicrobial compounds from the oilseed crop Ricinus communis using a multiplatform metabolite profiling approach. Ind. Crops Prod. 124, 834–844. Udagawa, S.I., 1963. (—)-Sclerotiorin, a major metabolite of Penicillium hirayamae UDAGAWA. Chem. Pharm. Bull. 11, 366–367. Visagie, C.M., Houbraken, J., Frisvad, J.C., Hong, S.B., Klaassen, C.H.W., Perrone, G., Seifert, K.A., Varga, J., Yaguchi, T., Samson, R.A., 2014. Identification and nomenclature of the genus Penicillium. Stud. Mycol. 78, 343–371. Wang, X.-C., Chen, K., Zeng, Z.-Q., Zhuang, W.-Y., 2017. Phylogeny and morphological analyses of Penicillium section Sclerotiora (Fungi) lead to the discovery of five new
species. Sci. Rep. 7, 8233. Wang, X., Sena Filho, J.G., Hoover, A.R., King, J.B., Ellis, T.K., Powell, D.R., Cichewicz, R.H., 2010. Chemical epigenetics alters the secondary metabolite composition of guttate excreted by an atlantic-forest-soil-derived Penicillium citreonigrum. J. Nat. Prod. 73, 942–948. Yadav, A.N., Verma, P., Kumar, V., Sangwan, P., Mishra, S., Panjiar, N., Gupta, V.K., Saxena, A.K., Gupta, V.K., Rodriguez-Couto, S., 2018. Chapter 1 - Biodiversity of the Genus Penicillium in Different Habitats, New and Future Developments in Microbial Biotechnology and Bioengineering. Elsevier, Amsterdam, pp. 3–18.
3
Contents lists available at ScienceDirect
Biochemical Systematics and Ecology journal homepage: www.elsevier.com/locate/biochemsyseco
Antioxidant and antibacterial activities of the chlorine pigment sclerotiorin from Penicillium mallochii and its chemotaxonomic significance
T
Patrícia O. dos Santosa,∗∗, Caline G. Ferrazb,∗, Paulo R. Ribeiroc, Fabricio M. Mirandab, Franceli da Silvab, Jorge T. de Souzad, Milton R. de A. Roquee, Ana C.F. Soaresb a
Instituto Federal Baiano, R. Glicério Taváres, S/n - Bate-quente, Valença, BA, Brazil Universidade Federal do Recôncavo da Bahia, R. Rui Barbosa, 710, Cruz das Almas, BA, Brazil c Metabolomics Research Group, Departamento de Química Orgânica, Instituto de Química, Universidade Federal da Bahia, Rua Barão de Jeremoabo S/n, 40170-115, Salvador, Brazil d Department of Plant Pathology, Universidade Federal de Lavras Lavras, MG, 37200-000, Brazil e Universidade Federal da Bahia, Instituto de Ciências da Saúde, Vale do Canela, Salvador, BA, Brazil b
ARTICLE INFO
ABSTRACT
Keywords: Bioactive compounds Endophytes Penicillium Pigments
Penicillium mallochii was isolated as an endophyte from Himatanthus sp. and inoculated in liquid potato-dextrose culture medium, with adjusted to pH 3.6, and incubated for 10 days at 24 °C. Successive column chromatography of the hexane extract afforded the chlorine pigment sclerotiorin. Its structure was determined by NMR and by comparison with the literature. Sclerotiorin showed moderate antioxidant activity and moderate antibacterial against Bacillus subtilis, Staphylococcus aureus, and Micrococcus luteus. The isolation of sclerotiorin from P. mallochii support the taxonomic classification within the Penicillium genus, demonstrating a closer evolutionary relationship among the Penicillium species. Therefore, we suggest that sclerotiorin and the sclerotiorin group of metabolites may be used as chemotaxonomic markers for proper identification of Penicillium species.
1. Subject and source
2. Previous work
Species of ascomycetous fungi Penicillium have worldwide distribution inhabiting a diverse panel of environments such as air, soil, and living in association with plants and food products (Santini et al., 2014; Yadav et al., 2018). They are protagonists in a wide range of natural processes, such as decomposing organic matter in natural environments or even causing destructive damages in the food industry (Visagie et al., 2014). Additionally, they are well-known for their production of mycotoxins and pigments (Lebeau et al., 2017; Visagie et al., 2014). Therefore, they present great potential for biotechnological and industrial applications. Penicillium mallochii was isolated as an endophyte from Himatanthus sp. Collected at the Chapada do Araripe – Ceará State, Brazil (−40°12′6″S, 40°1′55″W). The endophyte isolated from Himatanthus sp was identified based the comparison of its cytochrome oxidase 1, internal transcribed spacer, β-tubulin, translation elongation factor 1-α, and calmodulin sequences amplified by PCR with those deposited on GenBank for Penicillium mallochii.
Some studies related to Penicillium mallochii have been published, but none describing the assessment of its chemical composition (Man et al., 2018; Poitevin et al., 2018; Rivera et al., 2012; Rivera and Seifert, 2011; Wang et al., 2017).
∗
3. Present study Penicillium mallochii was inoculated in liquid potato-dextrose culture medium, with adjusted to pH 3.6, and incubated for 10 days at 24 °C. The metabolites produced by the mycelium were extracted by partitioning in hexane. The hexane extract (18.05 g) was subjected to successive column chromatography (60 × 10 cm i.d. column, Merck silica gel 230–400 mesh) eluting with a gradient of hexane and methanol to afford sclerotiorin (Fig. 1). Its structure was determined by NMR (Table 1) and by comparison of its spectral data with those reported previously in the literature (Chidananda and Sattur, 2007). Antioxidant activity was performed by using the 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenge assay as described in Pereira et al. (2014),
Corresponding author. Corresponding author. E-mail addresses: [email protected] (P. O. dos Santos), [email protected] (C.G. Ferraz).
∗∗
https://doi.org/10.1016/j.bse.2019.103915 Received 20 April 2019; Received in revised form 29 May 2019; Accepted 15 June 2019 0305-1978/ © 2019 Elsevier Ltd. All rights reserved.
Biochemical Systematics and Ecology 86 (2019) 103915
P. O. dos Santos, et al.
((3E,5E)-5,7-dimethyl-2-methylenenona-3, 5-dienyl)-2,4-dihydroxy-3methylbenzaldehyde (5)) isolated from P. citreonigrum (Wang et al., 2010). Wortmin is a member of the sclerotiorin group of metabolites, but this metabolite has been isolated from P. wortmanni Klöcker (Merlini et al., 1973), which belongs to the genus Talaromyces. Although Penicillium species present unique morphotaxonomic structures, the identification at species levels is still difficult. The taxonomic identification of Penicillium species show complex challenges and usually more than one approach is necessary to ensure proper classification (Lund and Frisvad, 1994). This multiplatform approach encompasses morphological, biochemical, and molecular analysis (Lund and Frisvad, 1994). Therefore, chemotaxonomic traits may greatly contribute for the classification of Penicillium species. The isolation of sclerotiorin from P. mallochii provide further evidence to support the taxonomic classification of Penicillium genus, demonstrating a closer evolutionary relationship among the Penicillium species. Therefore, we suggest that sclerotiorin and the sclerotiorin group of metabolites may be used as chemotaxonomic markers for proper identification of Penicillium species.
Fig. 1. Chemical structure of sclerotiorin. Table 1 1 H (500 MHz) and13C NMR (125 MHz) spectral data of sclerotiorin in CDCl3. Position
δH (J in Hz)
δC
gHMBC
1
7.94 (1H, s)
152.63
3 4 4a 5 6 7 8 8a 9
– 6.65 (1H, s) – – – – –
158.09 106.34 114.50 138.70 191.72 84.54 185.94 110.70 115.62
C-2, C-3, C-4, C-5, C-6, C-8a
COSY
C-2, C-4, C-6, C-8a
Acknowledgements
13
6.07 (1H, d, 15.65 Hz) 7.06 (1H, d, 15.65 Hz) – 5.70 (1H, d, 9.80 Hz) 2.48 (1H, m)
14a
1.32 (1H, m)
30.02
C-10, C-13, C-14, C16, C-17 C-11, C-12. C-14, C15, C-16 C-12, C-13, C-15, C-16
14b 15
1.44 (1H, 0.87 (3H, 7.40 Hz) 1.01 (3H, 6.65 Hz) 1.85 (3H, 1.57 (3H, – 2.17 (3H,
m) t,
– 11.92
C-12, C-13, C-15, C-16 C-13, C-14, C-16
H-14b, H-15, H-16 H-14a, H-15 H-14a, H-14b
d,
20.16
C-13, C-14, C-16
H-13
s) s)
12.32 22.50 170.06 20.03
C-11, C-12, C-13 C-6, C-7, C-8
H-12
10 11 12
16 17 18 19 20
s)
142.85 131.93 148.83 35.09
Financial support was provided by FINEP, CAPES, CNPq, and FAPESB. We thank the Nuclear Magnetic Resonance (NMR) Facility at Brazilian Biosciences National Laboratory (LNBio), for the use of the NMR spectrometer (500 MHz, Agilent DD2).
C-2, C-3, C-10, C-11
H-10
C-2, C-3, C-9, C-11, C12, C-17
H-9 H-13, H-17
Appendix A. Supplementary data
H-12
Supplementary data to this article can be found online at https:// doi.org/10.1016/j.bse.2019.103915. References Birkinshaw, J.H., 1952. Studies in the biochemistry of micro-organisms. Metabolic products of Penicillium multicolor G.-M. and P. with special reference to sclerotiorin. Biochem. J. 52, 283–288. Chidananda, C., Sattur, A.P., 2007. Sclerotiorin, a novel inhibitor of lipoxygenase from Penicillium frequentans. J. Agric. Food Chem. 55, 2879–2883. Curtin, T.P., Reilly, J., 1940. Sclerotiorin, C20H21O5Cl, a chlorine-containing metabolic product of Penicillium sclerotiorin. Biochem. J. 34. Gray, R.W., Whalley, W.B., 1970. (-)-7-Epi-5-chloroisorotiorin, a novel metabolite of the sclerotiorin group. J. Chem. Soc. D Chem. Commun. 762. Gray, R.W., Whalley, W.B., 1971. The chemistry of fungi. Part LXIII. Rubrorotiorin, a metabolite of Penicillium hirayamae Udagawa. J. Chem. Soc. C: Org. Chem. 3575–3577. Lebeau, J., Venkatachalam, M., Fouillaud, M., Petit, T., Vinale, F., Dufossé, L., Caro, Y., 2017. Production and new extraction method of polyketide red pigments produced by ascomycetous fungi from terrestrial and marine habitats. J. Fungi 3. Lund, F., Frisvad, J.C., 1994. Chemotaxonomy of Penicillium aurantiogriseum and related species. Mycol. Res. 98, 481–492. Man, B., Wang, H., Yun, Y., Xiang, X., Wang, R., Duan, Y., Cheng, X., 2018. Diversity of fungal communities in Heshang Cave of Central China revealed by mycobiome-sequencing. Front. Microbiol. 9. Merlini, L., Mondelli, R., Nasini, G., Hesse, M., 1973. Structure of wortmin, a new metabolite from Penicillium wortmanni. Helv. Chim. Acta 56, 232–239. Pereira, E.P.L., Ribeiro, P.R., Loureiro, M.B., de Castro, R.D., Fernandez, L.G., 2014. Effect of water restriction on total phenolics and antioxidant properties of Amburana cearensis (Fr. Allem) A.C. Smith cotyledons during seed imbibition. Acta Physiol. Plant. 36, 1293–1297. Poitevin, C.G., Porsani, M.V., Poltronieri, A.S., Zawadneak, M.A.C., Pimentel, I.C., 2018. Fungi isolated from insects in strawberry crops act as potential biological control agents of duponchelia fovealis (Lepidoptera: Crambidae). Appl. Entomol. Zool 53, 323–331. Rivera, K.G., Díaz, J., Chavarría-Díaz, F., Garcia, M., Urb, M., Thorn, R.G., Louis-Seize, G., Janzen, D.H., Seifert, K.A., 2012. Penicillium mallochii and P. guanacastense two new species isolated from Costa Rican caterpillars. Mycotaxon 119, 315–328. Rivera, K.G., Seifert, K.A., 2011. A taxonomic and phylogenetic revision of the Penicillium sclerotiorum complex. Stud. Mycol. 70, 139–158. Santini, A., Mikušová, P., Sulyok, M., Krska, R., Labuda, R., Šrobárová, A., 2014. Penicillium strains isolated from Slovak grape berries taxonomy assessment by secondary metabolite profile. Mycotoxin Res. 30, 213–220. Santos, P.M., Batista, D.L.J., Ribeiro, L.A.F., Boffo, E.F., de Cerqueira, M.D., Martins, D., de Castro, R.D., de Souza-Neta, L.C., Pinto, E., Zambotti-Villela, L., Colepicolo, P., Fernandez, L.G., Canuto, G.A.B., Ribeiro, P.R., 2018. Identification of antioxidant and
C-19
*Carbonyl groups were assigned based on their δC.
whereas antibacterial activity was performed against Bacillus cereus, B. subtilis, Staphylococcus aureus, and Micrococcus luteus as described in Santos et al. (2018). Sclerotiorin (IC50 of 78.12 ± 2.82 μg mL−1) showed moderate antioxidant activity as compared to the positive control gallic acid (IC50 of 1.26 ± 0.02 μg mL−1). Sclerotiorin also showed moderate antibacterial against B. subtilis (MIC of 200 μg mL−1), Staphylococcus aureus (MIC of 200 μg mL−1), and Micrococcus luteus (MIC of 100 μg mL−1) as compared to the positive control chloramphenicol. Chloramphenicol showed MIC of 1.56 μg mL−1 for B. subtilis, 6.25 μg mL−1 for S. aureus, and 3.12 μg mL−1 for M. luteus. No activity as detected for against Bacillus cereus for concentrations equal or lower than 200 μg mL−1. 4. Chemotaxonomic importance Sclerotiorin is a unusual pigment first obtained from the mycelium of Penicillium sclerotiorum (Curtin and Reilly, 1940). Later it was obtained from P. multicolor (Birkinshaw, 1952), P. hirayamae (Udagawa, 1963), P. frequentans (Chidananda and Sattur, 2007), and P. citreonigrum (Wang et al., 2010). Sclerotiorin is also the main component of the sclerotiorin group of metabolites which includes rubrorotiorin, isolated from P. hirayamae (Gray and Whalley, 1970, 1971), sclerotioramine, ochrephilone, dechloroisochromophilone III and IV, pencolide, and 62
Biochemical Systematics and Ecology 86 (2019) 103915
P. O. dos Santos, et al. antimicrobial compounds from the oilseed crop Ricinus communis using a multiplatform metabolite profiling approach. Ind. Crops Prod. 124, 834–844. Udagawa, S.I., 1963. (—)-Sclerotiorin, a major metabolite of Penicillium hirayamae UDAGAWA. Chem. Pharm. Bull. 11, 366–367. Visagie, C.M., Houbraken, J., Frisvad, J.C., Hong, S.B., Klaassen, C.H.W., Perrone, G., Seifert, K.A., Varga, J., Yaguchi, T., Samson, R.A., 2014. Identification and nomenclature of the genus Penicillium. Stud. Mycol. 78, 343–371. Wang, X.-C., Chen, K., Zeng, Z.-Q., Zhuang, W.-Y., 2017. Phylogeny and morphological analyses of Penicillium section Sclerotiora (Fungi) lead to the discovery of five new
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