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      Taxonomy, chemodiversity, and chemoconsistency of Aspergillus, Penicillium, and Talaromyces species

      review-article

      Frontiers in Microbiology

      Frontiers Media S.A.

      Aspergillus, Penicillium, Talaromyces, secondary metabolites, chemodiversity, chemoconsistency

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          Abstract

          Aspergillus, Penicillium, and Talaromyces are among the most chemically inventive of all fungi, producing a wide array of secondary metabolites (exometabolites). The three genera are holophyletic in a cladistic sense and polythetic classes in an anagenetic or functional sense, and contain 344, 354, and 88 species, respectively. New developments in classification, cladification, and nomenclature have meant that the species, series, and sections suggested are natural groups that share many extrolites, including exometabolites, exoproteins, exocarbohydrates, and exolipids in addition to morphological features. The number of exometabolites reported from these species is very large, and genome sequencing projects have shown that a large number of additional exometabolites may be expressed, given the right conditions (“cryptic” gene clusters for exometabolites). The exometabolites are biosynthesized via shikimic acid, tricarboxylic acid cycle members, nucleotides, carbohydrates or as polyketides, non-ribosomal peptides, terpenes, or mixtures of those. The gene clusters coding for these compounds contain genes for the biosynthetic building blocks, the linking of these building blocks, tailoring enzymes, resistance for own products, and exporters. Species within a series or section in Aspergillus, Penicillium, and Talaromyces have many exometabolites in common, seemingly acquired by cladogenesis, but some the gene clusters for autapomorphic exometabolites may have been acquired by horizontal gene transfer. Despite genome sequencing efforts, and the many breakthroughs these will give, it is obvious that epigenetic factors play a large role in evolution and function of chemodiversity, and better methods for characterizing the epigenome are needed. Most of the individual species of the three genera produce a consistent and characteristic profile of exometabolites, but growth medium variations, stimulation by exometabolites from other species, and variations in abiotic intrinsic and extrinsic environmental factors such as pH, temperature, redox potential, and water activity will add significantly to the number of biosynthetic families expressed in anyone species. An example of the shared exometabolites in a natural group such as Aspergillus section Circumdati series Circumdati is that most, but not all species produce penicillic acids, aspyrones, neoaspergillic acids, xanthomegnins, melleins, aspergamides, circumdatins, and ochratoxins, in different combinations.

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          Most cited references 61

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          Regulation of fungal secondary metabolism.

          Fungi produce a multitude of low-molecular-mass compounds known as secondary metabolites, which have roles in a range of cellular processes such as transcription, development and intercellular communication. In addition, many of these compounds now have important applications, for instance, as antibiotics or immunosuppressants. Genome mining efforts indicate that the capability of fungi to produce secondary metabolites has been substantially underestimated because many of the fungal secondary metabolite biosynthesis gene clusters are silent under standard cultivation conditions. In this Review, I describe our current understanding of the regulatory elements that modulate the transcription of genes involved in secondary metabolism. I also discuss how an improved knowledge of these regulatory elements will ultimately lead to a better understanding of the physiological and ecological functions of these important compounds and will pave the way for a novel avenue to drug discovery through targeted activation of silent gene clusters.
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            Big effects from small changes: possible ways to explore nature's chemical diversity.

            Fungi or bacteria that produce secondary metabolites often have the potential to bring up various compounds from a single strain. The molecular basis for this well-known observation was confirmed in the last few years by several sequencing projects of different microorganisms. Besides well-known examples about induction of a selected biosynthesis (for example, by high- or low-phosphate cultivation media), no overview about the potential in this field for finding natural products was given. We have investigated the systematic alteration of easily accessible cultivation parameters (for example, media composition, aeration, culture vessel, addition of enzyme inhibitors) in order to increase the number of secondary metabolites available from one microbial source. We termed this way of revealing nature's chemical diversity the 'OSMAC (One Strain-Many Compounds) approach' and by using it we were able to isolate up to 20 different metabolites in yields up to 2.6 g L(-1) from a single organism. These compounds cover nearly all major natural product families, and in some cases the high production titer opens new possibilities for semisynthetic methods to enhance even more the chemical diversity of selected compounds. The OSMAC approach offers a good alternative to industrial high-throughput screening that focuses on the active principle in a distinct bioassay. In consequence, the detection of additional compounds that might be of interest as lead structures in further bioassays is impossible and clearly demonstrates the deficiency of the industrial procedure. Furthermore, our approach seems to be a useful tool to detect those metabolites that are postulated to be the final products of an amazing number of typical secondary metabolite gene clusters identified in several microorganisms. If one assumes a (more or less) defined reservoir of genetic possibilities for several biosynthetic pathways in one strain that is used for a highly flexible production of secondary metabolites depending on the environment, the OSMAC approach might give more insight into the role of secondary metabolism in the microbial community or during the evolution of life itself.
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              Identification and nomenclature of the genus Penicillium

              Penicillium is a diverse genus occurring worldwide and its species play important roles as decomposers of organic materials and cause destructive rots in the food industry where they produce a wide range of mycotoxins. Other species are considered enzyme factories or are common indoor air allergens. Although DNA sequences are essential for robust identification of Penicillium species, there is currently no comprehensive, verified reference database for the genus. To coincide with the move to one fungus one name in the International Code of Nomenclature for algae, fungi and plants, the generic concept of Penicillium was re-defined to accommodate species from other genera, such as Chromocleista, Eladia, Eupenicillium, Torulomyces and Thysanophora, which together comprise a large monophyletic clade. As a result of this, and the many new species described in recent years, it was necessary to update the list of accepted species in Penicillium. The genus currently contains 354 accepted species, including new combinations for Aspergillus crystallinus, A. malodoratus and A. paradoxus, which belong to Penicillium section Paradoxa. To add to the taxonomic value of the list, we also provide information on each accepted species MycoBank number, living ex-type strains and provide GenBank accession numbers to ITS, β-tubulin, calmodulin and RPB2 sequences, thereby supplying a verified set of sequences for each species of the genus. In addition to the nomenclatural list, we recommend a standard working method for species descriptions and identifications to be adopted by laboratories working on this genus.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                05 December 2014
                12 January 2015
                2014
                : 5
                Affiliations
                [1]Section of Eukaryotic Biotechnology, Department of Systems Biology, Technical University of Denmark Kongens Lyngby, Denmark
                Author notes

                Edited by: Jonathan Palmer, United States Department of Agriculture Forest Service, USA

                Reviewed by: Antonello Santini, University of Naples Federico II, Italy; Rob Samson, CBS Fungal Biodiversity Centre, Netherlands

                *Correspondence: Jens C. Frisvad, Section for Eukaryotic Biotechnology, Department of Systems Biology, Technical University of Denmark, Søltofts Plads B. 221, 2800 Kongens Lyngby, Denmark e-mail: jcf@ 123456bio.dtu.dk

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology.

                Article
                10.3389/fmicb.2014.00773
                4290622
                f4ef30ff-774b-4438-bf3e-9db246c75e97
                Copyright © 2015 Frisvad.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 0, Tables: 2, Equations: 0, References: 79, Pages: 7, Words: 0
                Categories
                Microbiology
                Mini Review Article

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