Sesquiterpenoids from culture of the fungus Stereum complicatum (Steraceae): structural diversity, antifungal and phytotoxic activities
Graphical abstract
Introduction
The Steraceae family (Basidiomycete) contains about 22 genera and 125 species. Among these genera, Stereum comprises 27 species with a widespread geographical distribution (Kirk et al., 2008). Species of Stereum are found to thrive in several types of dead wood, dead leaves, and sometimes on living leaves, thus, they are considered as saprobic organisms. The isolation and purification of secondary metabolites have been described only for a few Stereum species, with Stereum hirsutum and its sesquiterpenoids the most studied species and common metabolites found, respectively. Stereum species comprise an important source of structurally diverse sesquiterpenoids of the hirsutane, sterpurane, cadinane, stereumane, isolactarane, drimane, illudalane and norilludalane types (Liermann et al., 2010; Jinlun et al., 1992; Zheng et al., 2013; Li et al., 2011; Till et al., 2008; Young-Hee et al., 2006; Masahiko et al., 2012). Additionally, other classes of metabolites such as benzoate and benzofuran derivatives, triterpenes, sterols, and isoindolinone alkaloids have also been described in Stereum species (Ke et al., 2014; Rong et al., 2011; Jian-Neng et al., 2017; Meng-Qing et al., 2017; Ito-Kobayashi et al., 2008). Compounds isolated from Stereum have been reported for their cytotoxic activity, nematicidal, antifungal, human pancreatic lipase inhibition and antibacterial activities (Jian-Neng et al., 2017; Jun-Mei et al., 2017; Aqueveque et al., 2017; Hahk-Soo and Jong-Pyung, 2016; Yuan-Chang et al., 2018).
Stereum complicatum was found to infect living turnip (Brassica rapa var. rapa L.) leaves in Oxford MS, causing necrotic lesions (Fig. 1A). Most plant pathogens produce phytotoxins. Hence, we hypothesized that this fungus could be secreting phytotoxins that induce tissue necrosis. Very little information is available on the secondary metabolites of Stereum complicatum (Mellows et al., 1973). There is a robust literature on phytotoxins isolated from fungi; however, we have found no studies on the phytotoxic activity of compounds isolated from any species of Stereum (Martínez-Luisa et al., 2005; Molitor et al., 2012; Meepagala et al., 2015). Terpenoids are among the different phytotoxins reported from fungi (Favaretto et al., 2019; Yoo et al., 2006). In this paper we describe the isolation and structure elucidation of seven sesquiterpenoids, including four new compounds with illudane, hirsutane and sterpurane-like backbones from the ethyl acetate extract of the potato dextrose broth (PDB) culture of S. complicatum. All purified compounds were evaluated for their phytotoxic, antifungal and antibacterial activities.
Section snippets
Isolation and structure elucidation
The ethyl acetate extract from the culture broth filtrate of S. complicatum showed both antifungal and phytotoxic activity. Therefore, this medium polarity extract was further fractionated in a silica gel cartridge using flash chromatography. The most active fractions from ethyl acetate were further screened as sources of phytotoxins and antifungal compounds. Compounds from active fractions were finally purify either using silica gel flash chromatography or reversed-phase high-performance
General Experimental Procedures
Optical rotations were determined on an Autopol IV Automatic Polarimeter model 589-546 (Rudolph Research Analytical, Hackettstown, NJ, USA).
1D and 2D NMR spectra were recorded on a Bruker NMR spectrometer (Billerica, MA, USA) operating at 400 or 500 MHz (1H) and 100 or 125 MHz (13C) at 30 °C, using standard Bruker pulse programs. Samples were run in MeOH-d4 and the chemical shifts are given in δ (ppm) referenced to residual solvent signals.
Direct analysis in real time - high resolution mass
Declaration of Competing Interest
None
Acknowledgments
Authors thank Jessie L. Robertson and Robert D. Johnson from USDA ARS-NPURU for technical assistance in antifungal and phytotoxin bioassays. This research was supported in part by an appointment to the ARS Research Participation Program administered by ORISE through an interagency between the DOE and USDA. ORISE is managed by ORAU under DOE contract number DE-SC0014664. All opinions expressed in this paper are the authors' and do not necessarily reflect the policies and views of USDA, ARS, DOE
References (35)
- et al.
Antifungal activities of secondary metabolites isolated from liquid fermentations of Stereum hirsutum (Sh134-11) against Botrytis cinereal (grey mould agent)
Food Chem. Toxicol.
(2017) - et al.
Sesquiterpenoid metabolites from Stereum complicatum
Phytochemistry.
(1973) - et al.
Secondary metabolites from a Gloeophyllum species
Phytochemistry.
(2000) - et al.
Dictionary of the Fungi
(2008) - et al.
Hirsutane-Type Sesquiterpenes with Uncommon Modifications from Three Basidiomycetes
Org. Chem.
(2010) - et al.
Isolation and identification of two new metabolites from silver leaf fungus Stereum purpureum
Org. Chem.
(1992) - et al.
Stereumins K-P, sesquiterpenes from the fungus Stereum sp. CCTCC AF 2012007
Phytochemistry
(2013) - et al.
Stereumins H−J, Stereumane-Type Sesquiterpenes from the Fungus Stereum sp
J. Nat. Prod.
(2011) - et al.
New Isolactarane Type Sesquiterpenoids with Antifungal Activity from Stereum sp. IBWF 01060
Antibiot.
(2008) - et al.
Methoxylaricinolic Acid, a New Sesquiterpene from the Fruiting Bodies of Stereum Ostrea
Antibiot.
(2006)
Sterostreins F–O, illudalanes and norilludalanes from cultures of the Basidiomycete Stereum ostrea BCC 22955
Phytochemistry.
New benzoate derivatives and hirsutane type sesquiterpenoids with antimicrobial activity and cytotoxicity from the solid-state fermented rice by the medicinal mushroom Stereum hirsutum
Food Chem.
Two new benzofuran derivatives from the fungus Stereum sp. YMF1.1684
Phytochem. Lett.
Lanostane triterpenoids from fruiting bodies of basidiomycete Stereum sp., structures and biological activities
Antibiot.
A new compound from Stereum insigne CGMCC5.57
Nat. Prod. Res.
Antibiot.
B, C and D, Novel 11b -Hydroxysteroid Dehydrogenase Type 1 Inhibitors from Stereum sp. SANK 21205
Phytochem. Lett.
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