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Article

Fungi in Microbial Culture Collections and Their Metabolites

by
Alexander Vasilenko
,
Natalya Ivanushkina
,
Galina Kochkina
and
Svetlana Ozerskaya
*
All-Russian Collection of Microorganisms (VKM), Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences (PSCBR RAS), G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms Russian Academy of Sciences (IBPM RAS), 142290 Pushchino, Russia
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(7), 507; https://doi.org/10.3390/d14070507
Submission received: 6 May 2022 / Revised: 6 June 2022 / Accepted: 20 June 2022 / Published: 22 June 2022
(This article belongs to the Special Issue Fungal Diversity and Related Metabolites)

Abstract

:
This study presents the results of a comparative analysis of the fungal diversity in the world system of microbial culture collections on one side with a variety of known fungal producers on the other side. The main VKM databases used are FungalDC and Metabolites of Fungi and the central point of analysis is the fungal ability to synthesize promising metabolites for applied use. It indicates that the option of obtaining new promising strains from the collection funds is still underestimated by the scientific community. In particular, it is shown that no more than 3% of the total fungal species fund contained in culture collections are used practically. It is possible that their use will considerably expand the range of studied strains and lead to the acquisition of new scientifically significant data.

Graphical Abstract

1. Introduction

Fungi belong to a kingdom of living organisms with extremely high diversity. According to expert estimates, the number of fungal species currently ranges from 2.2 to 3.8 million. In recent decades, the rate of description of new taxa has increased significantly due to the fast advances in molecular-biological diagnostics [1]. The Mycobank (www.mycobank.org), the premier reference platform for mycology, lists the names of over 440,000 legitimately described species (including synonyms), mostly held in culture collections worldwide, a large part of them in the leading CBS-KNAW Culture Collection (Westerdijk Fungal Biodiversity Institute; https://wi.knaw.nl/page/Collection). Obviously, ex situ conservation of microbial diversity for use in fundamental and applied scientific developments is of great importance. At the same time, culture collections play a decisive role in providing researchers with reliable biological material, which is the basis of any high-quality scientific work [2].
The large Microbial Culture Collections (mCCs) and MicroBiological Resource Center (mBRCs) maintain significant holdings of biological material and related information [3] to facilitate access to the biological resources conserved. They ensure the availability of microorganisms for the further use in sustainable scientific development. The mBRCs presents software for searching the data of required strains in their databases using various parameters. This helps to visualize and analyze the available information, and to make it accessible for the users of the online system.
The diversity of mCC and mBRC mycobiota in collections gets great attention, since fungi and their metabolites may represent an alternative to many currently used chemical compounds in the future [4]. Various new natural substances with promising potential for biological, medical, and industrial applications can be isolated and identified from fungi. The importance of fungal secondary metabolites for biotechnology cannot be overestimated. They can have antimicrobial activity, be enzyme inhibitors, be growth hormones, etc. [5,6].
A wide taxonomic diversity of various collections makes it possible to find strains capable of biosynthesis of specific organic substances. However, experience shows that the main fungal group studied by numerous researchers is very limited. Thus, in analysis of 245 patents related to the production of secondary metabolites and biotransformation processes using endophytic fungi [7], it was discovered that the most frequently mentioned fungi belong to the genera Aspergillus, Fusarium, Trichoderma, Penicillium, and Phomopsis. The representatives of these genera are also used in biomedicine, agriculture, and the food industry. Meanwhile, the biotechnological potential of other fungal groups can also be of high importance. They are, however, excluded from the scope of the research for a variety of reasons.
Therefore, for a global assessment of the biotechnological potential of fungal strains maintained in collections, it is necessary to collect all available and newly received information about their properties in specialized databases [8].
A recent analytical comparison of All-Russian Collection of Microorganisms (VKM) databases with the database ChEBI (Chemical Entities of Biological Interest; https://www.ebi.ac.uk/chebi/) and database ChEMBL (Chemical Database of European Molecular Biology Laboratory; https://www.ebi.ac.uk/chembl/) containing information on fungal metabolites showed that VKM have significant number of potentially interesting strains for a comprehensive study of their metabolome [9].
Due to the constant interest in the search for new producers of biotechnologically promising fungal metabolites, the specialized databases on the diversity of fungi maintained in collections worldwide (FungalDC—Fungal Diversity in Culture Collections) and the ability of fungi to produce secondary metabolites (Metabolites of Fungi) were constructed in VKM.
The goal of this study was to compare on the basis of VKM databases, the diversity of the total fund of fungi in collections worldwide with the diversity of known fungi-producers that synthesize metabolites promising for applied use.

2. Materials and Methods

Materials contained in databases FungalDC and Metabolites of Fungi were used in this research. Each database was constructed with the appropriate structure of tables, forms, and queries in Access 2010.
The FungalDC database [10,11,12] is available online at the VKM website (www.vkm.ru). A hyperlink to this database is provided on the Mycobank portal in the section “External links—Specimens and strains links” for each taxon mentioned on its pages. It should be noted that this database includes only those collections that have available electronic or printed catalogs of their holdings.
The table of the fungal diversity in the culture collections presented in the FungalDC has the following fields:
-
Code.
-
Country.
-
Collection Acronym.
-
WDCM Number.
-
Full Name of Culture Collection.
-
Count of Species.
-
Genus.
-
Species.
-
Variant/Subspecies.
The Metabolites of Fungi database [13] is also available on the VKM website, but only in test mode so far.
The table of the fungal metabolites’ diversity contains the following fields:
-
Code.
-
Name of database.
-
Database ID.
-
Name of Metabolite.
-
Genus.
-
Species.
-
Strain Number.
-
Reference.
The method used here is a comparison of the common data fields with the same values of Genus and Species in two databases. Additional information was obtained from the other fields: the distribution of taxa of the cumulative fungal fund in various collections of different countries; the diversity of unique chemical compounds—fungal metabolites; the number and diversity of the mentioned specific strains.

3. Results

The FungalDC database was analyzed to obtain information on the different types of fungi found in the world’s culture collections (Table 1).
Curation is an essential aspect of FungalDC that distinguishes it from WDCM (http://ccinfo.wdcm.org/). This indicates that virtually every taxon was validated against the Index Fungorum (http://www.indexfungorum.org/) and Mycobank databases. This makes it possible to achieve correspondence in the spelling of the mentioned taxa, and this simplifies the search of the desired taxon by users. In FungalDC, the numerous misspellings and errors of genera names and species epithets that could be found in catalogues of any level collection were corrected. Continued curation work will contribute to the compilation of the most correct list of species of the world fungal fund in FungalDC.
Most of the collections analyzed in FungalDC are WDCM-registered and belong to the World Federation of Culture Collections (WFCC). WFCC maintain information on collections of microorganisms from various countries and accumulate information about the species presented in them, and promote and support the establishment of new culture collections and related services (https://wfcc.info/about_view). The remaining collections included in the database were created at scientific institutions and do not have WDCM registration numbers; however, they publish catalogs of fungal cultures stored in them.
The FungalDC query system allows to see the abbreviations of culture collections, their names, the country where the collection is located, and the number of fungal species in each.
Table 2 presents the number of culture collections per country. The biggest numbers of them are in Asia (such as Thailand, Japan, and India). A complete list of collections that make their catalogues available to users is provided in Appendix A.
The information on the fungal species in the collection catalogues indicates that the total collection fund is more than 4700 genera and 32,000 unique species, including synonyms. Most fungal species are represented in European collections (Figure 1). This is largely due to the capability of the world’s leading mycological collection—CBS—in The Netherlands, which contains over 18,000 fungal species.
The genera whose strains are the most frequently isolated from different habitats and are widely studied in connection with their beneficial or harmful properties are the most numerous in the culture collections: Penicillium, Candida, Aspergillus, Fusarium, Alternaria, Chaetomium, Colletotrichum, Phoma, Diaporthe, and Cladosporium.
It should be noted that representatives of some fungal genera are preserved in the majority of the collections, or at least in a significant part of them (Table 3). These are, first of all, fungi whose metabolome is actively studied (Penicillium, Fusarium), yeasts actively used in the food industry (Saccharomyces), and opportunistic yeasts such as Candida and Cryptococcus. It is these fungi that are most in demand by users for scientific and practical research.
However, there are collections, one of the tasks of which is to support fungi of rare taxa and to preserve biological diversity in general. They keep species that are poorly studied or new to science. This group also includes fungi isolated from extreme habitats. These may be micromycetes with a high adaptive potential capable of active metabolism under unfavorable environmental conditions [14]. Such fungi are stored mainly in large bioresource centers such as CBS, MUCL, DAOMC, VKM, and others (Appendix A). It is in these poorly studied organisms that the potential of the kingdom of Fungi is concentrated, which has yet to be revealed.
The Metabolites of Fungi database was constructed on ChEBI (Chemical Entities of Biological Interest, (https://www.ebi.ac.uk/chebi/) and FungalMet (http://www.fungalmet.org/it/) databases.
The acronym ChEBI literally means “chemicals of biological interest database”. It provides all researchers with open access to information on low-molecular-weight chemical compounds produced by fungi and reflects the relationships between individual chemicals, their families, and classes [15]. All this database information is of public access (Creative Commons license, CC BY 4.0). All the data presented have links to their sources. The main data sources for the ChEBI database are the databases: IntEnz, ChEMBL, KEGG COMPOUND, PDBeChem. Among the Life Sciences databases interacting with ChEBI, we found the following: ArrayExpress, EAWAG-BBD, BioModels, BRENDA, ChEMBL, ChemIDplus, COMe, DDBJ, DrugBank, EMBL, ENA, Enzyme Portal, Expression Atlas, GenBank, GMD, IEDB, IntAct, IntEnz, IUBMB, KEGG, KEGG DRUG, KEGG GLYCAN, LIPID MAPS, LMPD, LMSD, nmrshiftdb, NURSA, PDBe, PIR, PubChem, Reactome, RESID, Rhea, SABIO-RK, wwPDB, and UniProtKB.
The manual and default keyword search for fungal organisms in ChEBI provides comprehensive information on diverse fungal taxa and their metabolites.
FungalMet stores information on secondary metabolites of fungi that were addressed and correlated with fungal sources in scientific publications. Metabolites can be found using the search with various parameters, such as the microorganism-producer and the name of the compound or the chemical formula. Currently, the database contains more than 3000 metabolite names. When the new information comes, the database is updated with the new substances of the fungal origin. Information on all of its fungal taxa and on all the metabolite names was extracted from FungalMet. Interestingly, in the process of analyzing the data obtained, it turned out that these two bases largely complement each other, with very little overlap (Table 4).
Table 4 shows that these two databases together contain the information on more than 7400 metabolites. At the same time, 6397 of them are unique, that is, they are found only in one of them.
These metabolites are produced by 304 fungal genera, of which approximately 10% generate 20 or more metabolites and 35% produce a single metabolite. Several fungal taxa, however, as shown in Table 5, produce hundreds of beneficial compounds.
The yeast Saccharomyces cerevisiae, which has played an important role in food and beverage fermentation for centuries and has been extensively studied (Table 6), maintains a special place on the fungal list.
As not all strains of the same species are equally active in the production of a particular metabolite, the substrate from which the strain was isolated, the duration and methods of its conservation in the collection, etc., are of high importance in research. In this regard, many scientific journals in their rules for authors indicate as compulsory the information on the number (designation) of the strain used in the study. For example, Journal of Microbiology in Instructions to Authors “strongly encourages authors to deposit important strains in publicly accessible culture collections and to refer to these collections and strain numbers in the manuscript”.
Nevertheless, not all the Metabolites of Fungi database records with metabolites produced by micromycetes are accompanied by specific strain numbers. Additionally, only a very small part of them keep the records with the strain numbers of the known culture collections. As a result, only 1176 database records present the strains, the rest do not indicate it at all. Of these, there are 325 records with numbers of known collections (Table 7), they make 129 unique collection strains only. Some collections are excluded from the database because neither their catalogues nor their WDCM numbers are available.
The results of the comparative analysis on the diversity of the world collection fungal strains on one side with the diversity of fungi with the metabolites studied and presented in the most famous Life Sciences databases on the other side, are presented in Table 8.

4. Discussion

The analysis of the integrated data made it possible to assess the extent to which fungi from different taxa have been studied in relation to their ability to produce metabolites and to understand in which collections of the world one or another known producer of certain chemical compounds should be sought.
The main interest in fungal metabolites is associated with the discovery of new drugs, since among the substances produced by fungi, most exhibit antibacterial, antifungal, or antitumor activity [16]. According to the literature data, these biologically active substances are found in certain taxa of fungi, mainly in the representatives of the Pezizomycotina subphylum and in several classes of basidiomycetes (for example, Agaricomycetes and Exobasidiomycetes) [17]. Our analysis of the database showed that, among the fungal genera whose representatives produce the maximum number of metabolites (more than 20), the greatest number actually belongs to the four classes of Pezizomycotina and Agaricomycetes of Agaricomycotina (Figure 2).
The most inspected fungi belong to the order Eurotiales (Eurotiomycetes), including the genera Aspergillus, Penicillium, Paecilomyces, and Paecilom. Several dozen taxa are utilized in biotechnological research but are not supported in collections for yces, as well as certain fungal genera from the order Hypocreales (Sordariomycetes).
The last group has representatives of the genera Fusarium, Trichoderma, Acremonium, and others that have been constantly researched and studied over the years. Among the producers, there are also representatives of other phyla—Mucoromycotina, Taphrinomycotina, Pucciniomycotina, etc., but their number is disproportionately small. This is largely due to the insufficient use of the collection fund available for researchers.
Taxonomic diversity comparison in FungalDC and Fungal Metabolite database revealed only 70 fungal species known to be producers but not present in the culture collections.
Most of them are fungi whose metabolites were studied directly in the investigation of natural objects—a total of 50 species. These are difficultly cultivated basidiomycetes of the class Pucciniomycetes (Glomospora and Uromyces), pathogens of rust on cereal plants, lichenized ascomycetous fungi Ramalina capitata and Pertusaria sp., as well as representatives of the genera Cytonaema and Smardaea that form stromas on woody plants. This also includes the fungus Plasmodiophora brassicae, the causative agent of diseases of cruciferous plants, currently a representative of the Protozoa kingdom (Plasmodiophoromycota, Plasmodiophoromycetes). Most of the taxa of this group belong to the class Agaricomycetes (23 genera, 41 species), a characteristic feature of which is the presence of rather large fruiting bodies, in the study of which metabolites were detected. Examples: the genera Agaricus, Amanita, Boletus, Chlorophyllum, Clitocybe, Conocybe, Favolaschia, Ganoderma, Inocybe, Polyporus, Psilocybe, Tylopilus, and others. Among ascomycetes, truffles Tuber liyuanum and Tuber magnatum, morel Morchella importuna can be included into this group.
The remaining 20 species are represented by cultivated micromycetes that are not maintained in collections according to the FungalDC database. Among them, the species with type strains not currently available and the species descriptions in the literature not sufficient to confirm the uniqueness of the taxon (for example, Alternaria oryzae [18], Microascus tardifaciens [19]), as well as taxa not represented in collections with available catalogs, such as Pestalotiopsis fici, Pestalotiopsis oenotherae, Phomopsis paspali, Guanomyces polythrix, Cercospora coffeicola, and Sordaria araneosa.
Several dozen taxa are utilized in biotechnological research but are not supported in collections for multiple reasons, as confirmed by the data obtained. On the other hand, the number of fungal taxa with the strains maintained in collections and with the known metabolites production is less than 3% of the total diversity of the total repository list of collections (Table 8).
On the one side, the diversity of the entire world fungal collection fund was compared to the diversity of the list of species traditionally utilized in scientific research. On the other side, it was demonstrated that the scientific community continues to underestimate the possibility of obtaining new promising strains from collection repositories.
The database FungalDC developed in VKM is available to users on various portals—www.vkm.ru and www.mycobank.org in online mode could possibly help with this issue. Perhaps its use will considerably expand the range of strains studied and lead to new scientifically significant data.

Author Contributions

Conceptualization, S.O. and A.V.; methodology, S.O. and A.V.; software, A.V.; validation, G.K. and N.I.; formal analysis, S.O.; investigation, A.V.; resources, S.O.; data curation, S.O., G.K. and N.I.; writing—original draft preparation, S.O., G.K. and N.I.; writing—review and editing, G.K. and N.I.; visualization, S.O.; supervision, S.O.; project administration, S.O. All authors have read and agreed to the published version of the manuscript.

Funding

This research has received funding from the Ministry of Science and Higher Education of the Russian Federation under grant agreement No. 075-15-2021-1051.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Appendix A. List of Culture Collections (on 2 June 2022)

CountryAcronymWDCM NumberCulture Collection NameNumber of Species
1ArgentinaBGIVWDCM962Banco de Glomeromycota In Vitro (Bank of Glomeromycota In Vitro)8
2CCMWDCM29Coleccion de Cultivos Microbianos28
3CEPWDCM973Entomopathogenic Fungal Culture Collection of Argentina30
4ArmeniaMDCWDCM803Microbial Depository Center (National Microbial Culture Collection of the Republic of Armenia)305
5AustraliaAMMRLWDCM42Australian National Reference Laboratory in Medical Mycology326
6AWRI MCCWDCM22AWRI Microorganism Culture Collection55
7CCWDCM61CSIRO Canberra Rhizobium Collection1
8CSWDCM532CSIRO Collection of Living Micro-algae1
9DE-CSIROWDCM70CSIRO Insect Pathogen Culture Collection14
10DMPMCWDCM454Department of Microbiology20
11DFPWDCM102DFP Culture Collection447
12FRRWDCM18Food Science Australia, Ryde451
13WAITEWDCM35Insect Pathology Pathogen Collection19
14JCTWDCM387James Cook Townsville161
15KEMHWDCM11KEMH/PMH Culture collection33
16ACHWDCM47Mycology Culture Collection123
17WACWDCM77Plant Pathology Culture Collection347
18SBSFUWDCM78School of Biological Sciences3
19SMTWAWDCM90School of Medical Technology Western Australia1
20SAITPWDCM569School of Pharmacy and Medical Sciences, University of South Australia1
21WACCWDCM452Western Australian Culture Collection13
22WMWDCM1205Westmead Medical Mycology Collection366
23DWTWDCM36Wood Technology and Forest Research Division80
24BelarusBIMWDCM909 Belarusian Collection of non-pathogenic microorganisms164
25BelgiumMUCLWDCM308Agro-food and Environmental Fungal Collection4601
26BCCM/IHEMWDCM642BCCM/IHEM—Fungi Collection: Human and Animal Health1855
27CRA-W-Fungi collection, Walloon Agricultural Research Centre11
28GINCO-Glomeromycota in vitro collection7
29LUC-Limburgs Universitair Centrum11
30CLO-Gent-Verticillium chlamydosporium (Fungi) strain collection1
31BrazilIPTWDCM721Agrupamento de Biotecnologia, Culture Collection of Microorganisms4
32ITALWDCM143Banco de Fermentos Lacticos2
33CBMAIWDCM823Brazilian Collection of Microorganisms from the Environment and Industry111
34BCCCpWDCM921Brazilian Culture collection of Crinipellis perniciosa1
35CRM-UNESPWDCM1043Central de Recursos Microbianos do Instituto de Biociencias da UNESP60
36FTIWDCM716Centro de Biotecnologia e Quimica-CEBIQ14
37CCBWDCM713Colecao de Culturas de Basidiomicetos16
38CFAF-Colecao de Culturas de Fitopatogenos e Agentes de Controle Biologico de Fitopatogenos13
39Fiocruz/CCFFWDCM720Colecao de Culturas de Fungos Filamentosos359
40CCTWDCM885Colecao de Culturas Tropical692
41Fiocruz/CFAMWDCM957Colecao de Fungos da Amazonia71
42CFEUnioeste-Colecao de Fungos Entomopatogenicos do Laboratorio de Biotecnologia Agricola5
43CFEOCA-Colecao de Fungos Entomopatogenicos Oldemar Cardim Abre19
44Fiocruz/CFPWDCM951Colecao de Fungos Patogenicos20
45UFPEDAWDCM114Colecao de Microrganismos UFPEDA127
46CICG-Colecao Internacional de Cultura de Glomeromycota24
47CCMA-UFLAWDCM1083Culture Collection of Agricultural Microbiology59
48CCDCAWDCM1081Culture Collection of Microorganisms from the Department of Food Science58
49UFRJIMWDCM725Departamento de Microbiologia Medica2
50DPUAWDCM715Departamento de Patologia/ICB81
51IZWDCM724Departamento de Tecnologia Rural344
52CGWDCM712Embrapa Genetic Resources and Biotechnology Collection of Fungi of Interest to Biological Control42
53CCOCWDCM575Fundacao Oswaldo Cruz-FIOCRUZ45
54CCTWDCM711Fundacao Tropical de Pesquisas e Tecnologia “Andre Tosello”97
55INPAWDCM719Laboratorio de Micologia Medica Divisao de Microbiologia e Nutricao93
56IALMICWDCM717Micoteca do Insituto Adolfo Lutz90
57IMTWDCM718Micoteca do Instituto de Medicina Tropical de Sao Paulo254
58MGSS-Micoteca Prof. Gilson Soares da Silva61
59CMRPWDCM1240Microbiological Collections of Parana Network344
60IALWDCM282Nucleo de Colecao de Micro-organismos3
61ITALSMWDCM723Secao de Microbiologia19
62URMWDCM604Universidade Federal de Pernambuco1144
63BulgariaBTCCWDCM66Bulgarian Type Culture Collection77
64NBIMCCWDCM135National Bank for Industrial Microorganisms and Cell Cultures213
65CanadaDAOMCWDCM150Canadian Collection of Fungal Cultures2716
66CSCC-Cereal Smuts Cultures Collection, Winnipeg Research Centre Agriculture and Agri-Food6
67LSRRW-Department of Crop Sciences and Plant Ecology
University of Saskatchewan
2
68MULWDCM250Department of Microbiology MUL-B 2506
69UWOWDCM91Department of Plant Sciences294
70HERWDCM6Felix d’Herelle Reference Center for Bacterial Viruses1
71DFFWDCM50Forest Pathology Culture Collection, Pacific Forest Research Centre164
72FSCWDCM237Fredericton Stock Culture Collection128
73LYCCWDCM634Lallemand Yeast Culture Collection1
74OCRC-Oat crown rust Collection, Winnipeg Research Centre Agriculture and Agri-Food1
75OSRC-Oat Stem Rust Collection, Winnipeg Research Centre Agriculture and Agri-Food1
76PFCWDCC-PFC Wood Decay Culture Collection, Pacific Forestry Centre8
77CCRCAF-Research Centre Culture Collection of Agriculture and Agri-Food2
78SGSCWDCM338Salmonella Genetic Stock Centre21
79SCCMWDCM920Sporometrics Culture Collection of Microorganisms30
80UAMHWDCM73UAMH Center for Global Microfungal Biodiversity1721
81WLRC-Wheat Leaf Rust Collection, Winnipeg Research Centre Agriculture and Agri-Food1
82WSRC-Wheat Stem Rust Collection1
83ChileCChRGMWDCM1067Chilean Collection of Microbial Genetic Resources21
84ChinaCCTCCWDCM611China Center for Type Culture Collection822
85ACCCWDCM572Agricultural Culture Collection of China300
86CGMCCWDCM550China General Microbiological Culture Collection Center1118
87CCDMWDCM117Culture Collection of Department of Microbiology41
88CMCC(B)WDCM123National Center for Medical Culture Collections34
89Czech RepublicRIBMWDCM655Collection of Brewing Yeasts, Research Institute for Brewing and Malting28
90CMF ISB-Collection of Microscopic Fungi ISB (CMF ISB)280
91DBMWDCM654Collection of Yeasts and Industrial Microorganisms, Institute of Chemical Technology, Department of Biochemistry and Microbiology103
92DMUPWDCM658Collection of Yeasts, Department of Genetics and Microbiology, Faculty of Science, Charles University71
93CCBASWDCM558Culture Collection of Basidiomycetes288
94CCDM-Culture Collection of Dairy Microorganisms16
95CCFWDCM182Culture Collection of Fungi615
96RIFIS-Culture Collection of Microorganisms with Application in the Fodder Industry, Food Research Institute30
97CCC-Czech Collection Clavicipitales31
98CCMWDCM65Czech Collection of Microorganisms513
99CNCTCWDCM130Czech National Collection of Type Cultures78
100DenmarkIBTWDCM758IBT Culture Collection of Fungi103
101SSIWDCM158The International Escherichia and Klebsiella Centre (WHO)1
102FinlandHAMBIWDCM779HAMBI Culture Collection36
103VTTCCWDCM139VTT Culture Collection139
104FranceUMIPWDCM344Collection de Champignons et Actinomycetes Pathogenes229
105CNCMWDCM174Collection Nationale de Cultures de Microorganismes54
106LCPWDCM659Fungal Strain Collection, Laboratory of Cryptogamy588
107UCLAFWDCM552HMR/Romainville34
108GermanyBLWGWDCM264Bayerische Landesanstalt fur Weinbau und Gartenbau41
109DSMZWDCM274DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH1603
110IFAMWDCM145Institut fur Allgemeine Mikrobiologie2
111BBLFWDCM204Institut fur Pflanzenschutz im Forst112
112GreeceATHUMWDCM650ATHens University Mycology203
113BPICWDCM610Benaki Phytopathological Institute Collection127
114NUAWDCM281Department of Microbiology, National University of Athens1
115Hong KongCUHKWDCM68Biology Department, Chinese University of Hong Kong30
116HungaryDACTWDCM496Dept. Agricult. Chem. Technol.256
117NCAIMWDCM485National Collection of Agricultural and Industrial Microorganisms127
118IndiaMPKVWDCM448Biological Nitrogen Fixation Project College of Agriculture13
119CCDMBIWDCM119Culture Collection, Department of Microbiology78
120NTCCIWDCM107Culture Collection, Microbiology and Cell Biology Laboratory48
121DUMWDCM40Delhi University Mycological Herbarium1273
122DBVWDCM173Division of Standardisation1
123DMSRDEWDCM166DMSRDE Culture Collection150
124UMFFTDWDCM562Food and Fermentation Technology Division, University of Mumbai5
125VPCIWDCM497Fungal Culture Collection60
126GPCK-Germplasm Centre for Keratinophilic Fungi22
127ITCCWDCM430Indian Type Culture Collection746
128MCMWDCM561MACS Collection of Microorganisms8
129MTCCWDCM773Microbial Type Culture Collection and Gene Bank1004
130NCIMWDCM3National Collection of Industrial Microorganisms288
131IndonesiaFNCCWDCM755Food and Nutrition Culture Collection92
132ICBBWDCM842ICBB Culture Collection for Microorganisms and Cell Culture27
133ITBCCWDCM44Institute of Technology Bandung Culture Collection57
134InaCCWDCM769Lembaga Ilmu Pengetahuan Indonesia, Indonesian Institute for Sciences150
135IranIBRCWDCM950Iranian Biological Resource Center288
136PTCCWDCM124Persian Type Culture Collection50
137IrelandIMDWDCM227Industrial Microbiology Dublin104
138ItalyITEM-Agro-Food Microbial Culture Collection92
139CSMAWDCM147Centro di Studio dei Microorganismi Autotrofi—CNR1
140DBVPGWDCM180Industrial Yeasts Collection288
141JapanAHUWDCM635AHU Culture Collection339
142OUTWDCM748Department of Biotechnology220
143ATUWDCM636Dept. of Biotechnology University of Tokyo4
144HUTWDCM195HUT Culture Collection241
145IAMWDCM190IAM Culture Collection509
146IFOWDCM191Institute for Fermentation, Osaka3024
147RIFYWDCM749Institute of Enology and Viticulture15
148TIMMWDCM750Institute of Medical Mycology148
149JCMWDCM567Japan Collection of Microorganisms1984
150TSYWDCM67Laboratory of Mycology, Division of Microbiology5
151MAFFWDCM637NARO Genebank, Microorganism Section777
152NIBHWDCM746National Institute of Bioscience and Human-Technology15
153RIBWDCM640National Research Institute of Brewing14
154NRICWDCM747Nodai Research Institute Culture Collection161
155IFMWDCM60Research Center for Pathogenic Fungi and Microbial Toxicoses, Chiba University394
156MalaysiaSKUKWDCM565Simpanan Kultur Universiti Kebangsaan40
157UKKPWDCM430Universiti Kebangsaan Kultur Perubatan21
158MexicoCENACUMIWDCM757Centro Nacional de Cultivos Microbianos (National Center For Microbial Cultures)277
159CFQWDCM100Cepario de la Facultad de Quimica65
160ITDWDCM99Coleccion de Cepas Microbianas10
161ENCB-IPNWDCM449Coleccion de Cultivos de la Escuela Nacional de Ciencias Biologicas97
162INIFWDCM104Coleccion de Microhongos83
163LIH-UNAMWDCM817CultureCollection of Histoplasma capsulatum Strains from the Fungal Immunology Laboratory of the Department of Microbiology and Parasitology, Faculty of Medicine, UNAM1
164IIBM-UNAMWDCM48Industrial Culture Collection40
165CDBBWDCM500Unidad de Servicios de la Coleccion Nacional de Cepas Microbianas y Cultivos Celulares123
166CISMWDCM95Verticillium dahliae from cotton3
167The NetherlandsCBSWDCM133Centraalbureau voor Schimmelcultures, Fungal and Yeast Collection18,346
168New ZealandNZFSWDCM62Forest Research Culture Collection100
169ICMPWDCM589International Collection of Microorganisms from Plants969
170WARCWDCM376New Zealand Reference Culture Collection1
171NZRDWDCM318New Zealand Reference Culture Collection of Microorganisms, Dairy Section2
172NZRMWDCM457New Zealand Reference Culture Collection, Medical Section5
173PakistanFCBPWDCM859First fungal culture bank of Pakistan119
174PhilippinesITDIWDCM503Industrial Technology Development Institute49
175UPCCWDCM310Natural Sciences Research Institute Culture Collection214
176PNCM-BIOTECHWDCM620Philippine National Collection of Microorganisms144
177PolandLOCKWDCM105Centre of Industrial Microorganisms Collection38
178IAFBWDCM212Collection of Industrial Microorganisms159
179IAW-Research and Development Centre for Biotechnology Culture Collection 17
180LCCWDCM231University of Warmia and Mazury in Olsztyn34
181PortugalMUMWDCM816Micoteca da Universidade do Minho125
182Republic of KoreaEFCC-Entomopatogenic Fungal Culture Collection58
183RomaniaICCFWDCM232Collection of Industrial Microorganisms21
184Russian FederationVKMWDCM342All-Russian Collection of Microorganisms2100
185VIZRWDCM760Collection for plant protection, All-Russian Institute of Plant Protection14
186KMMWDCM644Collection of Marine Microorganisms of the Pacific Institute of Biorganic Chemistry of the Far-Eastern Branch of the RAS48
187IPP-Collection of Monoxenic Cultures of Arbuscular Mycorrhizal Fungi of the Institute of Plant Physiology RAS4
188VNIISC-Culture Collection of the Institute of Agricultural Microbiology, Russian Academy of Agricultural Sciences143
189IBC-Institute of Cell Biology RAS13
190LE(BIN)WDCM1015Komarov Botanical Institute Basidiomycetes Culture Collection672
191VKPMWDCM588Russian National Collection of Industrial Microorganisms733
192DSB MSU-The Department of Soil Sciences Moscow State University35
193RIAWDCM337The Russia Research Institute for Antibiotics Culture Collection43
194SenegalMAOWDCM53Mircen Afrique Ouest1
195SerbiaISSWDCM375Collection of Bacteria1
196SingaporeDBSWDCM510Department of Biological Culture Collection98
197NUSDMWDCM568Department of Microbiology24
198Slovak RepublicCCWDF-Culture Collection of Wood-destroying Fungi52
199CCYWDCM333Culture Collection of Yeasts394
200RIVEWDCM28Research Institute for Viticulture and Enology96
201SloveniaMZKIWDCM599Microbial Culture Collection of National Institute of Chemistry174
202ZIMWDCM810ZIM Collection of Industrial Microorganisms112
203SpainCECTWDCM412Coleccion Espanola de Cultivos Tipo394
204CCMCUWDCM599Culture Collection of Microorganisms182
205Sri LankaDMBUKWDCM564Department of Microbiology44
206SwedenCCUGWDCM32Culture Collection University of Goteborg92
207FCUGWDCM651Fungal Cultures University of Goteborg507
208UPSCWDCM603Uppsala University Culture Collection of Fungi800
209SwitzerlandCCTMWDCM475Centre de Collection de Type Microbien19
210TaiwanBCRCWDCM59Bioresource Collection and Research Center1545
211ThailandBSMBWDCM491Bacteriology and Soil Microbiology Branch20
212BCCWDCM783BIOTEC Culture Collection399
213NRPSUWDCM679Department of Agro-industry, Faculty of Natural Resources36
214ABKMIWDCM698Department of Applied Biology, Faculty of Science12
215DBKKU1WDCM687Department of Biology, Faculty of Science27
216SWU2WDCM697Department of Biology, Faculty of Science4
217DBMU2WDCM667Department of Biotechnology, Faculty of Science62
218FTCMUWDCM690Department of Food Science and Technology, Faculty of Agriculture10
219DMSTWDCM707Department of Medical Sciences Culture Collection204
220MPSUWDCM492Department of Microbiology2
221DMKKU1WDCM680Department of Microbiology, Faculty of Medicine2
222DMMU3WDCM668Department of Microbiology, Faculty of Medicine Siriraj Hospital66
223DMKUWDCM669Department of Microbiology, Faculty of Science57
224NUWDCM696Department of Microbiology, Faculty of Science2
225PPKU1WDCM670Department of Plant Pathology, Faculty of Agriculture5
226PPKU3WDCM672Department of Plant Pathology, Faculty of Agriculture19
227PPKU4WDCM673Department of Plant Pathology, Faculty of Agriculture18
228PPKU5WDCM674Department of Plant Pathology, Faculty of Agriculture10
229MLMJIWDCM701Department of Plant Protection, Faculty of Agricultural Production7
230CMKKUWDCM684Diagnostic Microbiology Unit Division of Clinical Laboratory Srinagarind Hospital, Faculty of Medicine9
231IFRPDWDCM676Institute of Food Research and Product Development, Kasetsart University35
232KUFCWDCM677Kasetsart University Fungus Collection, Department of Plant Pathology, Faculty of Agriculture18
233KKUWDCM23MICKKU Culture Collection18
234MLLDWDCM702Microbiological Research Laboratory, Soil and Water Section, Department of Land Development3
235CHULAWDCM511Department of Microbiology, Faculty of Science34
236DMCUWDCM663Microbiology Department, Faculty of Science24
237MLRUWDCM695Microbiology Laboratory, Department of Biology, Faculty of Science7
238MSDSWDCM494Microbiology Section, Biological Science Division, Department of Science Services9
239MSCMUWDCM692Microbiology Section, Chiang Mai University (MSCMU)50
240MSPPWDCM704Mycology Section, Plant Pathology and Microbiology Division, Department of Agricultural Science4
241NCSCWDCM664National Center of Streptococcus Collection, Department of Microbiology, Faculty of Medical Science16
242PCUWDCM662Pharmaceutical Sciences Chulalongkorn University Culture Collection10
243PPKMWDCM699Plant Production Technology Department, Faculty of Agricultural Technology5
244ERAEPWDCM706Radiation Ecology Section, Biological Science Division, Office of Atomic Energy for Peace5
245SSMJIWDCM700Science Section, Department of General Education, Faculty of Agricultural Business9
246TISTRWDCM383TISTR Culture Collection, Bangkok MIRCEN235
247TurkeyKUKENSWDCM101Centre for Research and Application of Culture Collections of Microorganisms83
248RSKKWDCM828Refik Saydam National Type Culture Collection-RSKK22
249UKIMIWDCM214CABI Bioscience Genetic Resource Collection3716
250BEGWDCM777La Banque European des Glomales30
251NCPFWDCM184National Collection of Pathogenic Fungi151
252NCTCWDCM154National Collection of Type Cultures1
253NCWRFWDCM134National Collection of Wood Rotting Fungi296
254NCYCWDCM169National Collection of Yeast Cultures449
255PHBLWDCM508Philip Harris Biological Ltd.27
256DMCCUSWDCM478School of Biological Sciences Culture Collection17
257CCMFWDCM766University of Portsmouth207
258UkraineIBKWDCM1152Culture Collection of Mushrooms195
259UCMWDCM1203Ukrainian Collection of Microorganisms195
260USANRRLWDCM97Agricultural Research Service Culture Collection742
261ATCCWDCM1American Type Culture Collection5585
262ARSEFWDCM112ARS Collection of Entomopathogenic Fungi366
263LMSWDCM530Carolina Biological Supply Company67
264FGSCWDCM115Fungal Genetics Stock Center21
265INVAM-International Culture Collection of VA Mycorrhizal Fungi76
266MCC-Mushroom Culture Collection Department of Plant Pathology, The Pennsylvania State University, USA198
267DM-National Center for Agricultural Utilization Research 54
268NCMAWDCM2Provasoli-Guillard National Center for Marine Algae and Microbiota4
269BMP-Pryor Lab Culture Collection, The University of Arizona, USA119
270RMF-Rocky Mountain Fungus, Wyoming374
271DSCWDCM849The Dicty Stock Center16
272UA-The University of Alabama4
273UBC-University of California at Berkeley1
274UM-University of Maine, Orono, Maine, USA14
275WVDHWDCM411West Virginia Hygienic Laboratory13
276WSF-Wisconsin Soil Fungus183
277UzbekistanNCAMWDCM808National Collection of Agricultural Microorganisms146
278VietnamCNTP-The Industrial Microorganisms Culture Collection39
279ZimbabweBDUZWDCM17Biological Sciences17

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Figure 1. Distribution of fungal species in culture collections on different continents.
Figure 1. Distribution of fungal species in culture collections on different continents.
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Figure 2. A variety of fungi with the greatest number of produced substances (more than 20).
Figure 2. A variety of fungi with the greatest number of produced substances (more than 20).
Diversity 14 00507 g002
Table 1. Volume of information in FungalDC (on 2 June 2022).
Table 1. Volume of information in FungalDC (on 2 June 2022).
CharacteristicsVolume of Information
Number of records84,276
Number of countries53
Number of culture collections279
Number of fungal genera4799
Number of fungal species32,495
Table 2. Location of the collections by country (on 2 June 2022).
Table 2. Location of the collections by country (on 2 June 2022).
CountriesNumber of Culture Collections
Argentina3
Armenia1
Australia19
Belarus1
Belgium6
Brazil32
Bulgaria2
Canada18
Chile1
China5
Czech Republic11
Denmark2
Finland2
France4
Germany4
Greece3
Hong Kong1
Hungary2
India13
Indonesia4
Iran2
Ireland1
Italy3
Japan15
Malaysia2
Mexico9
The Netherlands1
New Zealand5
Pakistan1
Philippines3
Poland4
Portugal1
Republic of Korea1
Romania1
Russian Federation10
Senegal1
Serbia1
Singapore2
Slovak Republic3
Slovenia2
Spain2
Sri Lanka1
Sweden3
Switzerland1
Taiwan1
Thailand36
Turkey2
UK9
Ukraine2
USA17
Uzbekistan1
Vietnam1
Zimbabwe1
Table 3. Fungal genera preserved in the maximum number of collections (on 2 June 2022).
Table 3. Fungal genera preserved in the maximum number of collections (on 2 June 2022).
Fungal GeneraNumber of Culture Collections
Penicillium159
Saccharomyces151
Fusarium150
Candida141
Trichoderma135
Rhizopus131
Mucor127
Cryptococcus124
Cladosporium119
Chaetomium110
Rhodotorula109
Paecilomyces105
Table 4. Data from different sources in the Metabolites of Fungi database (on 26 April 2022).
Table 4. Data from different sources in the Metabolites of Fungi database (on 26 April 2022).
CharacteristicsTotalChEBIFungalMet
Number of records743740223226
Number of unique metabolite records639736722725
Table 5. Genera of fungi with high production of metabolites (on 26 April 2022).
Table 5. Genera of fungi with high production of metabolites (on 26 April 2022).
Fungal GeneraNumber of Metabolites Produced by Members of the Genus
Saccharomyces1886
Aspergillus1107
Penicillium754
Ganoderma434
Fusarium293
Chaetomium235
Alternaria164
Trichoderma128
Phoma97
Acremonium91
Table 6. Species of fungi with high production of metabolites (on 26 April 2022).
Table 6. Species of fungi with high production of metabolites (on 26 April 2022).
Fungal SpeciesNumber of Metabolites Produced by Members of the Species
Saccharomyces cerevisiae1881
Ganoderma lucidum306
Aspergillus fumigatus143
Aspergillus niger128
Chaetomium globosum108
Aspergillus terreus85
Aspergillus flavus53
Gibberella fujikuroi53
Cordyceps sinensis52
Aspergillus ochraceus48
Claviceps purpurea47
Penicillium citrinum46
Aspergillus nidulans42
Table 7. Strains in Metabolites of Fungi database (on 26 April 2022).
Table 7. Strains in Metabolites of Fungi database (on 26 April 2022).
Acronym of Culture CollectionCountryWebsiteNumber in WDCM/Name of CollectionRecords with the Strain NumberNumber of Unique Strains
ATCCUSAhttp://www.atcc.org/WDCM111534
BCCThailandhttp://www.biotec.or.th/bcc/WDCM7835416
CBMAIBrazilhttps://cbmai.cpqba.unicamp.br/?lang=enWDCM82311
CBSThe Netherlandshttp://www.westerdijkinstitute.nl/WDCM133147
CCTCCChinahttp://www.cctcc.org/WDCM61131
DSMZGermanyhttp://www.dsmz.de/WDCM274113
IBTDenmarkhttp://www.bioengineering.dtu.dk/englishWDCM75842
IFMJapanhttp://www.pf.chiba-u.ac.jp/WDCM6082
IFO (NRBC)Japanhttps://www.nite.go.jp/nbrc/catalogue/?lang=enWDCM191118
IMIUKhttp://www.cabi.org/WDCM2142613
KMMRussiahttp://www.piboc.dvo.ru/WDCM644102
NRRLUSAhttps://nrrl.ncaur.usda.gov/WDCM975430
AJJapanhttps://www.ajinomoto.com/Central Research Laboratories, Ajinomoto Co. Inc., Kawasaki, Japan53
FERMJapanhttps://www.aist.go.jp/index_en.htmlPatent and Bio-Resource Center, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan33
MRCSouth Africawww.samrc.ac.zaNational Research Institute for Nutritional Diseases, Tygerberg, South Africa21
NRCCCanadahttps://nrc.canada.ca/enDivision of Biological Sciences, National Research Council of Canada, Ottawa, Canada11
TUFEstoniahttps://www.natmuseum.ut.ee/en/content/mycological-collectionThe mycological collection of the University of Tartu, Estonia32
Table 8. Diversity of fungi in culture collections and metabolite database (on 2 June 2022).
Table 8. Diversity of fungi in culture collections and metabolite database (on 2 June 2022).
Name of DatabaseNumber of GeneraNumber of Species
FungalDC479932,495
Metabolites of Fungi304899
Share (%)6.32.8
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Vasilenko, A.; Ivanushkina, N.; Kochkina, G.; Ozerskaya, S. Fungi in Microbial Culture Collections and Their Metabolites. Diversity 2022, 14, 507. https://doi.org/10.3390/d14070507

AMA Style

Vasilenko A, Ivanushkina N, Kochkina G, Ozerskaya S. Fungi in Microbial Culture Collections and Their Metabolites. Diversity. 2022; 14(7):507. https://doi.org/10.3390/d14070507

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Vasilenko, Alexander, Natalya Ivanushkina, Galina Kochkina, and Svetlana Ozerskaya. 2022. "Fungi in Microbial Culture Collections and Their Metabolites" Diversity 14, no. 7: 507. https://doi.org/10.3390/d14070507

APA Style

Vasilenko, A., Ivanushkina, N., Kochkina, G., & Ozerskaya, S. (2022). Fungi in Microbial Culture Collections and Their Metabolites. Diversity, 14(7), 507. https://doi.org/10.3390/d14070507

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