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Fifteen New Species of Penicillium Persoonia 36, 2016: 247–280 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE http://dx.doi.org/10.3767/003158516X691627 Fifteen new species of Penicillium C.M. Visagie1,8, J.B. Renaud 2, K.M.N. Burgess2, D.W. Malloch3, D. Clark4, L. Ketch5, M. Urb6,7, G. Louis-Seize1, R. Assabgui1, M.W. Sumarah2, K.A. Seifert1,8 Key words Abstract We introduce 15 new species of Penicillium isolated from a diverse range of locations, including Canada, Costa Rica, Germany, Italy, New Zealand, Tanzania, USA and the Dry Valleys of Antarctica, from a variety of habitats, beta-tubulin including leaf surfaces in tropical rain forests, soil eaten by chimpanzees, infrabuccal pockets of carpenter ants, calmodulin intestinal contents of caterpillars and soil. The new species are classified in sections Aspergilloides (1), Canescentia internal transcribed spacer rDNA region (2), Charlesia (1), Exilicaulis (3), Lanata-Divaricata (7) and Stolkia (1). Each is characterised and described using Trichocomaceae classical morphology, LC-MS based extrolite analyses and multigene phylogenies based on ITS, BenA and CaM. Significant extrolites detected include andrastin, pulvilloric acid, penitrem A and citrinin amongst many others. Article info Received: 28 January 2016; Accepted: 12 March 2016; Published: 9 May 2016. INTRODUCTION species might actually function in nature. It was easy to assume that most species are generalists found wherever we care to Because of the standardised approach to delineating species of make isolations. Penicillium now available, with ex-type or representative strains In this paper, 15 species are described that originated from and barcode sequences designated for almost all described several studies in three Canadian laboratories over the past species, including those considered synonyms (Visagie et al. 20 years, which are now recognised as novel taxa because of 2014b), routine description of new species can now be ap- the more complete reference data. Three species were isolated proached with reasonable confidence. The exact set of genes from soil of termite mounds selectively eaten by chimpanzees used for multi-locus sequence typing (MLST) or Genealogical (Pan troglodytes) in the Mahale Mountains and Gombe areas of Concordance Phylogenetic Species Recognition (GCPSR) is Tanzania (Ketch 1998). Thirty-one genera were identified from not standardised among different laboratories, but most tend these termitarium soils and surrounding control soils. The most to use a similar core set of loci. Phenotypes such as irregular commonly isolated genus was Penicillium with over 42 species conidiophore branching, culture sectoring, and the relative recovered, the most common of which was Penicillium citrinum. abundance of conidia, sterile mycelium, soluble pigments or Clark (2002) isolated microfungi from the infrabuccal pockets of exudates can be interpreted as phylogenetically informative carpenter ants, especially Camponotus pennsylvaticus. These characters or artefacts of culture degeneration according to sac-like organs in the mouths of ants filter solids from their their correlation with robustly analysed DNA sequence data. liquid foods to be expelled later, and thus capture fungal mate- The historical focus of Penicillium taxonomy on strains isolated rial collected during feeding and grooming. About 60 strains of from food, soil and the indoor environment is understandable Penicillium were isolated from extracted infrabuccal masses given the importance of these fungi as spoilage agents, produc- from ants collected in New Brunswick (Canada), Germany and ers of potent mycotoxins, and sources of valuable antibiotics. the Netherlands, representing six morphospecies; three are de- Much of the expansion of the number of species in Penicillium scribed as new species here. A US National Science Foundation and its sister genus Talaromyces can be traced to the antibiotic Microbial Observatory study of caterpillar intestines from Costa revolution and the ease with which soil could be collected by Rica previously yielded two undescribed species, P. mallochii travellers and used to isolate new strains upon return to the and P. guanacastense that clearly were significant components laboratory. This practise, however, obscured how Penicillium of that niche, along with P. citrinum (Rivera et al. 2012). An ad- ditional new species, represented as a single strain among the 1 Biodiversity (Mycology), Ottawa Research and Development Centre, 88 isolated, is described here. Other new species described in Agriculture & Agri-Food Canada, 960 Carling Ave., Ottawa, Ontario, K1A this paper were isolated from leaf surfaces of tropical plants, 0C6, Canada; corresponding author e-mail: [email protected]. nuts in temperate hardwood forests, peat bogs and soil remote 2 London Research & Development Centre, Agriculture & Agri-Food Canada, London, Ontario, N5V 4T3, Canada. from agricultural regions. 3 New Brunswick Museum, 277 Douglas Avenue, Saint John, New Brunswick, Extrolite profiling brought a new dimension to Penicillium taxo- E2K 1E5, Canada. nomy about 25 years ago (Filtenborg et al. 1990), accompanied 4 268 Gledhill Ave, Toronto, Ontario, M4C 5L2, Canada. 5 Precision BioLogic Inc., 140 Eileen Stubbs Ave, Dartmouth, Nova Scotia, by a hypothesis that different isolates of a single species should B3B 0A9, Canada. produce a consistent profile of core extrolites. With the availabili- 6 Department of Biology, University of Western Ontario, London, Ontario, ty of a new generation of LC-MS-MS technology, we generated N6A 5B7, Canada. extrolite profiles for all the new species described in this paper. 7 Centre de Recherche en Cancérologie de Lyon, INSERM U1052, 165 Chemin du petit Revoyet - BP 12, 69921 Oullins Cedex, France. Although reports are unavailable for the metabolites produced 8 Department of Biology, University of Ottawa, 30 Marie-Curie, Ottawa, by many species related to our new taxa, these observations Ontario, K1N 6N5, Canada. will be useful for future comparative chemotaxonomic studies. © 2016 Naturalis Biodiversity Center & Centraalbureau voor Schimmelcultures You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 248 Persoonia – Volume 36, 2016 Materials AND METHODS Newly generated sequences were submitted to GenBank under accession numbers KT887760–KT887876. Strains Gene sequences of the new species were compared with a Cultures were isolated either by direct or dilution plating from reference sequence dataset (Visagie et al. 2014b), with phylo- various substrates or niches as indicated in the species de- genies calculated for the relevant taxonomic sections in the scriptions, usually on 2 % malt extract agar with antibacterial system of Houbraken & Samson (2011). Datasets were aligned antibiotics. Strains were recovered from the working collections using MAFFT v. 7.221 (Katoh & Standley 2013), with the L-INS-i of Keith Seifert (Agriculture and Agri-Food Canada, Ottawa) algorithm selected for ITS and G-INS-i for BenA and CaM. and David Malloch (formerly University of Toronto), the latter Aligned datasets were adjusted and trimmed manually in Ge- now maintained in the Seifert laboratory. Ex-type and other neious. Datasets were subsequently analysed using Maximum representative strains were deposited into the Canadian Collec- Parsimony (MP) and Bayesian tree Inference (BI). MP heuristic tion of Fungal Cultures (DAOMC) and the CBS-KNAW Fungal searches were performed in PAUP v. 4.0b10 (Swofford 2003). Biodiversity Centre (CBS) in the Netherlands. BI analyses were run in MrBayes v. 3.2.5 (Ronquist & Huelsen- beck 2003). Model selections were made using MrModeltest v. Morphology 2.3 (Nylander et al. 2004) based on the lowest Akaike informa- tion criterion (AIC) value. Aligned datasets with the respective Colony characters were recorded from various media incu- command blocks for MP and BI were uploaded onto TreeBASE bated for 7 d, including Czapek yeast autolysate agar (CYA), (www.treebase.org) with accession no. S18638. Trees were Blakeslee’s (1915) malt extract agar (MEAbl), yeast extract prepared for publication in Adobe Illustrator CS6. sucrose agar (YES), oatmeal agar (OA) and creatine sucrose agar (CREA). BactoTM malt extract was used for MEAbl prepa- Extrolites ration. Media preparations, inoculations, incubation conditions and microscopic preparations followed the recommendations For extrolite analyses, all strains were grown in 9 cm polystyrene Petri dishes on YES (Frisvad 1981, Filtenborg et al. 1990) and by Visagie et al. (2014b). Colour names and codes used in de- CYA (Pitt 1980) incubated at 25 °C for 14 d. Strains were also scriptions are from Kornerup & Wanscher (1967). Microscopic grown in 200 mL of CYA broth incubated at 25 °C for 14 d. observations were made on an Olympus SZX12 dissecting Extrolites were extracted from the agar plates using an esta-
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