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New Penicillium and Talaromyces Species from Honey, Pollen and Nests of Stingless Bees Downloaded from orbit.dtu.dk on: Oct 07, 2021 New Penicillium and Talaromyces species from honey, pollen and nests of stingless bees Barbosa, Renan N.; Bezerra, Jadson D.P.; Souza-Motta, Cristina M.; Frisvad, Jens C.; Samson, Robert A.; Oliveira, Neiva T.; Houbraken, Jos Published in: Antonie van Leeuwenhoek: Journal of Microbiology Link to article, DOI: 10.1007/s10482-018-1081-1 Publication date: 2018 Document Version Publisher's PDF, also known as Version of record Link back to DTU Orbit Citation (APA): Barbosa, R. N., Bezerra, J. D. P., Souza-Motta, C. M., Frisvad, J. C., Samson, R. A., Oliveira, N. T., & Houbraken, J. (2018). New Penicillium and Talaromyces species from honey, pollen and nests of stingless bees. Antonie van Leeuwenhoek: Journal of Microbiology, 111(10), 1883-1912. https://doi.org/10.1007/s10482-018- 1081-1 General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. Users may download and print one copy of any publication from the public portal for the purpose of private study or research. You may not further distribute the material or use it for any profit-making activity or commercial gain You may freely distribute the URL identifying the publication in the public portal If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Antonie van Leeuwenhoek (2018) 111:1883–1912 https://doi.org/10.1007/s10482-018-1081-1 (0123456789().,-volV)(0123456789().,-volV) ORIGINAL PAPER New Penicillium and Talaromyces species from honey, pollen and nests of stingless bees Renan N. Barbosa . Jadson D. P. Bezerra . Cristina M. Souza-Motta . Jens C. Frisvad . Robert A. Samson . Neiva T. Oliveira . Jos Houbraken Received: 15 January 2018 / Accepted: 31 March 2018 / Published online: 13 April 2018 Ó The Author(s) 2018 Abstract Penicillium and Talaromyces species have and six in Talaromyces, including seven new species. a worldwide distribution and are isolated from various These new species were studied in detail using a materials and hosts, including insects and their polyphasic approach combining phenotypic, molecu- substrates. The aim of this study was to characterize lar and extrolite data. The four new Penicillium the Penicillium and Talaromyces species obtained species belong to sections Sclerotiora (Penicillium during a survey of honey, pollen and the inside of nests fernandesiae sp. nov., Penicillium mellis sp. nov., of Melipona scutellaris. A total of 100 isolates were Penicillium meliponae sp. nov.) and Gracilenta obtained during the survey and 82% of those strains (Penicillium apimei sp. nov.) and the three new belonged to Penicillium and 18% to Talaromyces. Talaromyces species to sections Helici (Talaromyces Identification of these isolates was performed based on pigmentosus sp. nov.), Talaromyces (Talaromyces phenotypic characters and b-tubulin and ITS sequenc- mycothecae sp. nov.) and Trachyspermi (Talaromyces ing. Twenty-one species were identified in Penicillium brasiliensis sp. nov.). The invalidly described species Penicillium echinulonalgiovense sp. nov. was also isolated during the survey and this species is validated Electronic supplementary material The online version of here. this article (https://doi.org/10.1007/s10482-018-1081-1) con- tains supplementary material, which is available to authorized Keywords Aspergillaceae users. 8 new taxa Á Á Fungal ecology Á Polyphasic approach Á Taxonomy Á R. N. Barbosa Á R. A. Samson Á J. Houbraken (&) Trichocomaceae Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands e-mail: [email protected] R. N. Barbosa Á J. D. P. Bezerra Á C. M. Souza-Motta Á Introduction N. T. Oliveira Departamento de Micologia Prof. Chaves Batista, Stingless bees comprise a diverse group of highly Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, Centro de Biocieˆncias, Cidade Universita´ria, eusocial insects occurring throughout the tropical CEP: 50670-901 Recife, PE, Brazil regions in the world. They are important honey producers and pollinators of several plants (Ramı´rez J. C. Frisvad et al. 2010; Brown and Oliveira 2014). An example of Department of Biotechnology and Biomedicine, Technical University of Denmark, 2800 Kongens Lyngby, a stingless bee species is Melipona scutellaris Denmark 123 1884 Antonie van Leeuwenhoek (2018) 111:1883–1912 (Hymenoptera: Apidae: Meliponini), an indigenous 2014). The genera Aspergillus, Penicillium, Mon- species occurring in the North-eastern part of Brazil ascus and Mucor are commonly associated with bees and considered to be one of the first species to be or their products (Egorova 1971; Gilliam et al. 1989; domesticated in the Americas (Kerr 1996; Silva et al. Eltz et al. 2002;Ferrazetal.2008; Barbosa et al. 2013). In this part of Brazil, M. scutellaris is the main 2017). Most fungi associated with bees and nests bee species in meliponiculture (stingless beekeeping). have a saprophytic lifestyle, but fungi can also have a Meliponiculture in the rural areas is a sustainable mutualistic relationship with bees (Menezes et al. activity and the honey from these bees is widely 2015). On the other hand, fungi are also reported to be appreciated as a food source. The composition of the pathogenic to many bee species and cause serious honey of the stingless bees differs from that of bees of problems in honey bee (Apis mellifera) brood. the genus Apis (honey bees) (Vit et al. 2004). The Aspergillus flavus is the primary species responsible honey of stingless bees contains, in comparison to for stonebrood, a disease where dead and mummified honey of honey bees, a more complex mixture of larvae are present in the brood cells, but also other carbohydrates and contains other types of organic Aspergilli such as Aspergillus fumigatus and Asper- acids, proteins, minerals, vitamins, pollen grains and gillus niger are reported as aetiological agents of this enzymes (Almeida-Muradian et al. 2013). Recently, disease (Gilliam and Vandenberg 1988; Foley et al. the interest in honey produced by stingless bees 2014;Lopesetal.2015;Sarwar2016). Though it is increased. Besides being a food source, also several generally accepted that infection only occurs in other functionalities are linked to this type of honey, weakened colonies, the specific conditions predis- such as antiseptic, antimicrobial, anti-inflammatory posing the onset of disease are not fully understood and wound-healing properties (Silva et al. 2013; Rao (Shoreit and Bagy 1995). et al. 2016). Fungi play an important role in many ecosystems; Penicillium and Talaromyces are fungal genera however, only a limited number of studies dealt with classified in the order Eurotiales. In the dual nomen- the association between stingless bees in Brazil and clature era (pre 2012), Talaromyces was known as a filamentous fungi (e.g. Oliveira and Morato 2000; sexual genus related to Penicillium and other genera. Ferraz et al. 2008;Go´is et al. 2010)andyeasts(e.g. In the last decade, the genera Talaromyces and Teixeira et al. 2003;Rosaetal.2003;Danieletal. Penicillium were re-defined due to new taxonomic 2013; Barbosa et al. 2016). In the present study, we insights and the introduction of single name nomen- analysed three different substrates associated with M. clature (Houbraken and Samson 2011; Samson et al. scutellaris bees: bee pollen, nests and honey. In 2011; McNeill et al. 2012; Yilmaz et al. 2014). nature, the M. scutellaris bee nests are mainly located Currently, Penicillium and Talaromyces are separate in tree hollows, and they are kept by beekeepers in genera that contain both sexual and asexual species. artificial wooden hives. The bees use cerumen (a Visagie et al. (2014) accepted 354 Penicillium species mixture of wax and floral resins) for the construction and Yilmaz et al. (2014)88Talaromyces species, and of their nests and this material is also used inside these numbers are rapidly increasing (Houbraken et al. nests in storage pots, brood cells and entrance 2016a). Several of the new species that are being openings (Cortopassi-Laurino et al. 2006;Pianaro discovered are found during ecology and biodiversity et al. 2007). The floral pollen is collected, packed into studies of specific substrates or habitats (Houbraken pollen pellets, and subsequently stored inside the nest et al. 2016a). Describing new species from poorly by worker bees. This stored pollen is referred to as explored substrates and habitats, like those related to ‘bee bread’. The pollen spectrum has been studied in meliponiculture, will add to our knowledge on biodi- the past to get insight in the bee colony’s food versity. With this information, future studies will also requirements, pollinating functions and the plant be able to better understand the ecology of fungi in species visited by the bees (Cortopassi-Laurino et al. these type of environments. 2007). Fungi, such as Penicillium and Talaromyces,can In this paper, we focus on the identification of have a strong association to a specific substrate Penicillium and Talaromyces species isolated from (Peterson et al. 2003; Kobayashi et al. 2008; Visagie three different substrates (bee pollen, nests and honey) 2012,Lietal.2012;Riveraetal.2012;Yilmazetal. associated to M. scutellaris in the Atlantic Rainforest
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