A Study of the Metabolic Profiles of Penicillium dimorphosporum KMM 4689 Which Led to Its Re-Identification as Penicillium hispanicum

Changes in cultivation conditions, in particular salinity and temperature, affect the production of secondary fungal metabolites. In this work, the extracts of fungus previously described as Penicillium dimorphosporum cultivated in various salinity and temperature conditions were investigated using HPLC UV/MS techniques, and their DPPH radical scavenging and cytotoxicity activities against human prostate cancer PC-3 cells and rat cardiomyocytes H9c2 were tested. In total, 25 compounds, including 13 desoxyisoaustamide-related alkaloids and eight anthraquinones, were identified in the studied extracts and their relative amounts were estimated. The production of known neuroprotective alkaloids 5, 6 and other brevianamide alkaloids was increased in hypersaline and high-temperature conditions, and this may be an adaptation to extreme conditions. On the other hand, hyposalinity stress may induce the synthesis of unidentified antioxidants with low cytotoxicity that could be very interesting for future investigation. The study of secondary metabolites of the strain KMM 4689 showed that although brevianamide-related alkaloids and anthraquinone pigments are widely distributed in various fungi, these metabolites have not been described for P. dimorphosporum and related species. For this reason, the strain KMM 4689 was re-sequenced using the β-tubulin gene and ITS regions as molecular markers and further identified as P. hispanicum.

[1]  O. I. Zhuravleva,et al.  New Marine Fungal Deoxy-14,15-Dehydroisoaustamide Resensitizes Prostate Cancer Cells to Enzalutamide , 2023, Marine drugs.

[2]  M. Sobeh,et al.  Chemical diversity, medicinal potentialities, biosynthesis, and pharmacokinetics of anthraquinones and their congeners derived from marine fungi: a comprehensive update , 2022, RSC advances.

[3]  J. Frisvad,et al.  Production of Fungal Quinones: Problems and Prospects , 2022, Biomolecules.

[4]  R. Durán-Patrón,et al.  Cryptic Metabolites from Marine-Derived Microorganisms Using OSMAC and Epigenetic Approaches , 2022, Marine drugs.

[5]  O. I. Zhuravleva,et al.  New Deoxyisoaustamide Derivatives from the Coral-Derived Fungus Penicillium dimorphosporum KMM 4689 , 2021, Marine drugs.

[6]  M. Beniddir,et al.  Chlorinated bianthrones from the cyanolichen Nephroma laevigatum. , 2020, Fitoterapia.

[7]  Zhange Feng,et al.  Capsulactone: a new 4-hydroxy-α-pyrone derivative from an endophytic fungus Penicillium capsulatum and its antimicrobial activity , 2020, Journal of Asian natural products research.

[8]  T. Zhu,et al.  Penicacids E-G, three new mycophenolic acid derivatives from the marine-derived fungus Penicillium parvum HDN17-478. , 2020, Chinese journal of natural medicines.

[9]  J. Takahashi,et al.  Use of the Versatility of Fungal Metabolism to Meet Modern Demands for Healthy Aging, Functional Foods, and Sustainability , 2020, Journal of fungi.

[10]  H. Raja,et al.  Drug Leads from Endophytic Fungi: Lessons Learned via Scaled Production , 2020, Planta Medica.

[11]  J. Frisvad,et al.  Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): An overview of families, genera, subgenera, sections, series and species , 2020, Studies in mycology.

[12]  Simon Rogers,et al.  Feature-Based Molecular Networking in the GNPS Analysis Environment , 2019, Nature Methods.

[13]  Christine M. Aceves,et al.  Reproducible molecular networking of untargeted mass spectrometry data using GNPS , 2019, Nature Protocols.

[14]  H. Correa,et al.  Discovery of Primarolides A and B from Marine Fungus Asteromyces cruciatus Using Osmotic Stress and Treatment with Suberoylanilide Hydroxamic Acid , 2019, Marine drugs.

[15]  D. Taşdemir,et al.  Rapid Metabolome and Bioactivity Profiling of Fungi Associated with the Leaf and Rhizosphere of the Baltic Seagrass Zostera marina , 2019, Marine drugs.

[16]  M. Pinto,et al.  Chromone Derivatives and Other Constituents from Cultures of the Marine Sponge-Associated Fungus Penicillium erubescens KUFA0220 and Their Antibacterial Activity , 2018, Marine drugs.

[17]  Sudhir Kumar,et al.  MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. , 2018, Molecular biology and evolution.

[18]  Shuzhao Li,et al.  One Step Forward for Reducing False Positive and False Negative Compound Identifications from Mass Spectrometry Metabolomics Data: New Algorithms for Constructing Extracted Ion Chromatograms and Detecting Chromatographic Peaks. , 2017, Analytical chemistry.

[19]  M. Rateb,et al.  Does Osmotic Stress Affect Natural Product Expression in Fungi? , 2017, Marine drugs.

[20]  A. B. Tiku,et al.  Emodin and Its Role in Chronic Diseases. , 2016, Advances in experimental medicine and biology.

[21]  D. Youssef,et al.  Penicillivinacine, antimigratory diketopiperazine alkaloid from the marine-derived fungus Penicillium vinaceum , 2015 .

[22]  D. Choi,et al.  Natural products from marine organisms with neuroprotective activity in the experimental models of Alzheimer’s disease, Parkinson’s disease and ischemic brain stroke: their molecular targets and action mechanisms , 2015, Archives of pharmacal research.

[23]  R. Krska,et al.  Penicillium strains isolated from Slovak grape berries taxonomy assessment by secondary metabolite profile , 2014, Mycotoxin Research.

[24]  J. Varga,et al.  Identification and nomenclature of the genus Penicillium , 2014, Studies in mycology.

[25]  Pradeep Dewapriya,et al.  Marine microorganisms: An emerging avenue in modern nutraceuticals and functional foods , 2014 .

[26]  Natalie I. Tasman,et al.  A Cross-platform Toolkit for Mass Spectrometry and Proteomics , 2012, Nature Biotechnology.

[27]  Liangdong Guo,et al.  Polyketides with antimicrobial activity from the solid culture of an endolichenic fungus Ulocladium sp. , 2012, Fitoterapia.

[28]  M. Miyazawa,et al.  Synthesis and structure-activity relationships of phenylpropanoid amides of serotonin on tyrosinase inhibition. , 2011, Bioorganic & medicinal chemistry letters.

[29]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[30]  Matej Oresic,et al.  MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data , 2010, BMC Bioinformatics.

[31]  Jian Zhang,et al.  Secalonic Acid D induced leukemia cell apoptosis and cell cycle arrest of G1 with involvement of GSK-3β/β-catenin/c-Myc pathway , 2009 .

[32]  Wan-sheng Chen,et al.  LC–VWD–MS Determination of Three Anthraquinones and One Stilbene in the Quality Control of Crude and Prepared Roots of Polygonum multiflorum Thunb. , 2008 .

[33]  J. Dobias,et al.  Cyanein, a new antibiotic fromPenicillium cyaneum , 1962, Folia Microbiologica.

[34]  Muhammad Nursid,et al.  12,13-Dihydroxyfumitremorgin C, Fumitremorgin C, and Brevianamide F, Antibacterial Diketopiperazine Alkaloids from the Marine-Derived Fungus Pseudallescheria sp. , 2007 .

[35]  S. Shyue,et al.  Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway. , 2005, Biochemical pharmacology.

[36]  E. Lacey,et al.  Calbistrin E and two other new metabolites from an Australian isolate of Penicillium striatisporum. , 2005, Journal of natural products.

[37]  S. Antus,et al.  LC-SSI-MS techniques as efficient tools for characterization of nonvolatile phenolic compounds of a special Hungarian wine. , 2004, Journal of chromatographic science.

[38]  Axel Zeeck,et al.  Big Effects from Small Changes: Possible Ways to Explore Nature's Chemical Diversity , 2002, Chembiochem : a European journal of chemical biology.

[39]  G. Polya,et al.  The Fungal Teratogen Secalonic Acid D is an Inhibitor of Protein Kinase C and of Cyclic AMP-Dependent Protein Kinase , 1996, Planta medica.

[40]  H. Mett,et al.  Protein tyrosine kinase and protein kinase C inhibition by fungal anthraquinones related to emodin. , 1995, The Journal of antibiotics.

[41]  N. L. Glass,et al.  Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes , 1995, Applied and environmental microbiology.

[42]  D. Anderson,et al.  IDENTIFICATION OF GROUP‐ AND STRAIN‐SPECIFIC GENETIC MARKERS FOR GLOBALLY DISTRIBUTED ALEXANDRIUM (DINOPHYCEAE). II. SEQUENCE ANALYSIS OF A FRAGMENT OF THE LSU rRNA GENE 1 , 1994 .

[43]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[44]  J. McAlpine,et al.  Calbistrins, novel antifungal agents produced by Penicillium restrictum. II. Isolation and elucidation of structure. , 1993, The Journal of antibiotics.

[45]  R. Schwartz,et al.  Structure elucidation of restricticin, a novel antifungal agent from penicillium restrictum , 1991 .

[46]  G. Olsen,et al.  The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. , 1985, Molecular biology and evolution.

[47]  L. Vining,et al.  Biosynthetic relationships among the secalonic acids. Isolation of emodin, endocrocin and secalonic acids from Pyrenochaeta terrestris and Aspergillus aculeatus. , 1979, The Journal of antibiotics.

[48]  P. Steyn Austamide, a new toxic metabolite from , 1971 .

[49]  H. Swart Penicillium dimorphosporum sp.nov. , 1970 .

[50]  P. Steyn The isolation, structure and absolute configuration of secalonic acid D, the toxic metabolite of Penicillium oxalicum. , 1970, Tetrahedron.

[51]  M. Piattelli,et al.  Anthraquinone pigments from Xanthoria parientina (L.) , 1968 .

[52]  N. Kiriyama,et al.  Studies on the metabolic products of Aspergillus fumigatus (J-4). Chemical structure of metabolic products. , 1968, Chemical & pharmaceutical bulletin.