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Saksenaea Dorisiae Sp. Nov., a New Opportunistic Pathogenic Fungus from Europe

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Saksenaea Dorisiae Sp. Nov., a New Opportunistic Pathogenic Fungus from Europe Hindawi International Journal of Microbiology Volume 2019, Article ID 6253829, 11 pages https://doi.org/10.1155/2019/6253829 Research Article Saksenaea dorisiae sp. nov., a New Opportunistic Pathogenic Fungus from Europe Roman Labuda ,1,2 Andreas Bernreiter,2,3 Doris Hochenauer,3 Christoph Schu¨ller,2,3 Alena Kuba´tova´,4 Joseph Strauss,2,3 and Martin Wagner1,2 1Department for Farm Animals and Veterinary Public Health, Institute of Milk Hygiene, Milk Technology and Food Science, University of Veterinary Medicine Vienna, Veterin¨arplatz 1, 1210 Vienna, Austria 2Research Platform Bioactive Microbial Metabolites (BiMM), Konrad Lorenz Strasse 24, 3430 Tulln a.d. Donau, Austria 3Department of Applied Genetics and Cell Biology, Fungal Genetics and Genomics Laboratory, University of Natural Resources and Life Sciences, Vienna (BOKU), Konrad Lorenz Strasse 24, 3430 Tulln a.d. Donau, Austria 4Charles University, Faculty of Science, Department of Botany, Culture Collection of Fungi (CCF), Bena´tska´ 2, 128 01 Prague 2, Czech Republic Correspondence should be addressed to Roman Labuda; [email protected] Received 5 April 2019; Revised 25 May 2019; Accepted 18 June 2019; Published 22 September 2019 Academic Editor: Barbara H. Iglewski Copyright © 2019 Roman Labuda et al. +is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. A new species, Saksenaea dorisiae (Mucoromycotina, Mucorales), isolated from a water sample originating from a private well in Manastirica, Petrovac, in the Republic of Serbia (Europe), is described and illustrated. +e new taxon is well supported by multilocus phylogenetic analysis that included the internal transcribed spacer (ITS) region, domains D1 and D2 of the 28S rRNA gene (LSU), and translation elongation factor-1α gene (tef-1α), and it is resolved in a clade with S. oblongispora and S. trapezispora. +is fungus is characterized by its moderately slow growth at 15 and 37°C, sparse rhizoids, conical-shaped sporangia, and short- cylindrical sporangiospores. Saksenaea dorisiae is a member of the opportunistic pathogenic genus often involved in severe human and animal mucormycoses encountered in tropical and subtropical regions. Despite its sensitivity to several conventional antifungals (terbinafine and ciclopirox), the fungus can potentially evoke clinically challenging infections. +is is the first novel taxon of the genus Saksenaea described from the moderately continental climate area of Europe. 1. Introduction mode of infection by this fungus from contaminated soil or water [2–4]. In addition to these traumatic implantations, +e genus Saksenaea S. B. Saksena is a mucoralean mi- infections through inhalation of spores and the use of in- croscopic fungus (Mucoromycotina, Mucorales, Sakse- dwelling catheters have been reported [5]. Species in this naeaceae) comprising of species often causing severe human genus are responsible for skin infections and are charac- and animal cutaneous mucormycoses in both immuno- terized by rapid progression and invasion of neighboring compromised and immunocompetent hosts [1, 2]. +e ge- tissues. Infection of the Saksenaea spp. is diagnosed by nus was first described from a forest soil in India in 1953. angioinvasion leading to tissue necrosis with cutaneous and Saksenaea vasiformis S. B. Saksena is the only species of the subcutaneous involvement. Furthermore, rhino-orbito-ce- genus (nowadays considered as S. vasiformis species com- rebral and disseminated infections have been reported [1, 2]. plex) for more than 50 years reported in soil, drift-wood, and Classic management of the infection site usually includes a grains [1]. Interruption of skin integrity, such as needle combination of broad, aggressive and repeated surgical sticks, insect stings or spider bites, and burn and accident debridement (which may lead to amputation), and long- wounds (up to 95% of cases), represents the most common term systemic therapy with appropriate antifungals, 2 International Journal of Microbiology preferably liposomal amphotericin B and/or posaconazole transferred (one agar block grown on CYA, ca 5 × 5 mm, in [6–9]. Antifungal therapy alone seems to be inadequate to the middle) on potato dextrose agar (PDA, Fluka), malt control infection [2]. extract agar (MEA, Merck), corn meal agar (CMA, Oxoid), Recent revisions by Alvarez et al. [1] and Crous et al. Sabouraud 4% dextrose agar (SDA, VWR), water agar 1% [10, 11] applied a polyphasic approach, which includes (WA), oatmeal agar (OA), synthetic nutrient-poor agar multilocus (ITS, LSU, and tef-1α), revealed that the (SNA), Czapek’s agar (CZA), Czapek yeast extract agar monotypic genus Saksenaea is genetically heterogeneous (CYA), and yeast extract sucrose (YES) agar as described by and encompassed more species, namely, S. erythrospora, Samson et al. [17] and incubated for 5–30 days in the dark at S. loutrophoriformis, S. oblongispora, S. trapezispora, and 25°C. Colony size (in mm), colony structure, and charac- S. vasiformis complexes (with more putative cryptic teristics were noted after four days. However, the cultivation species). So far, these species (except S. oblongispora) have was prolonged up to 3 months on all media in order to been reported worldwide from human and animal clinical observe and record changes in pigmentation of the colonies, cases. +ey were encountered in tropical and subtropical as well as to determine the onset of sporangia and zygospore climates and have been reported from Africa (Tunisia), formation. For sporangial development, a recommended Australia, India, the Middle East (Iraq, Israel, and Saudi method of floating agar blocks in yeast extract water Arabia), New Zealand, Sri Lanka, South America according to Padhye and Ajello [18] was used in this study. (Colombia, Ecuador, and French Guiana), +ailand, and In order to determine the optimal and minimal/maximal the USA [1, 12, 13]. In Europe, there are only a few temperatures for growth, the strain was incubated on four published cases available reporting S. vasiformis in- different media (CZA, CYA, PDA, and MEA) at 12, 15, 20, fections, e.g., from Spain [3, 14–16], France [1, 13], and 25, 30, 35, 37, 39, 40, and 42°C(±0.1-0.2°C). Colony di- Greece [2]. Up to now, approximately 45 cases of mostly ameters were measured on the 4th day of cultivation. For cutaneous infections of Saksenaea, have been reported comparative description of the macroscopic and micro- worldwide [2, 4, 5, 10, 11, 13], although the actual number scopic characteristics, CZA was used according to Alvarez of clinical cases is possibly underestimated [4]. Despite its et al. [1] and Crous et al. [10, 11]. association in severe human infections, this genus re- +e capability of three different vegetative forms of the mains a poorly studied mucoralean genus, mainly due to fungus to germinate or grow on more extreme temperatures the lack of sporulation on the mycological culture media was assessed by incubation at 5 ± 0.3°C during 1 to 50 days or (e.g., Sabouraud dextrose agar, malt extract agar, and corn at 40 ± 0.1°C for 24 to 48 hours. For these tests the following meal agar) routinely used in clinical laboratories [1]. procedure was applied: (a) spores: 100 μL of spore sus- During our microbiological survey of water samples, a pension (4.0 ×105 CFU/mL physiologic solution) collected fast-growing nonsporulating mucoralean fungus was re- from CZA (6 days at 30°C) was applied on MEA plate (at covered on a Pseudomonas selective agar plate in a sample 37°C) at defined time intervals (1, 2, 3, 4, 7, 14, 21, 28, 42, and originating from a private well in a rural area of Manastirica 50 d); (b) mycelial pellets: microcolonies of ca 50–200 μm in (the Republic of Serbia) in October 2018. +is isolate was diameter (∼2.0 ×104/mL) after 10–12 d incubation submerse designated BiMM-F232 and further characterized in terms of YES 5%, 140 rpm, 25°C, 100 μL of pellet suspension applied morphology, physiology, molecular phylogeny, and anti- on MEA plate (at 37°C); (c) mycelium: as a nonsporulating fungal susceptibility. Phylogenetically informative sequences colony growing on MEA plate after 4 d incubation (37°C). were obtained from three loci, i.e., internal transcribed spacer Both spores and pellets were exposed to 5°C in physiological region including 5.8S rDNA (ITS), domains D1 and D2 of the or YES broth liquids, respectively, and then transferred 28S rRNA gene (LSU), and the translation elongation factor- (100 μL) onto a plate at 37°C. For exposure to 40°C, they were 1α locus (tef-1α). Overall, the resulting data revealed that this directly applied onto plates and after 24 and 48 hours isolate represents a novel species of the opportunistic path- transferred on a new MEA plate and further incubated at ogenic genus Saksenaea, and it is described and illustrated 37°C. Germination of spores was determined in situ under here as Saksenaea dorisiae sp. nov. low magnification (50–100x). A dried herbarium specimen of the holotype was de- 2. Materials and Methods posited in the herbarium of the Mycological Department, National Museum, Prague, Czech Republic (PRM); the ex- 2.1. Sample Collection and Isolation of the Fungus. A single type cultures were deposited in the Bioactive Microbial sample of water from a private well in Manastirica, Petrovac Metabolites (BiMM), Fungal Collection, UFT-Tulln (AT), (the Republic of Serbia, Europe) was collected in October and in the Culture Collection of Fungi (CCF), Prague (CZ). 2018. A 100 mL aliquot was aseptically filtered through a For determination of microscopic traits, CZA was used filter paper disc (0.45 μm, 47 mm diameter, GN-6 Metricel, after 6–14 days. Sporangiophore structures and sporangia Pall, Mexico) plated on Pseudomonas selective agar amended formation were observed in situ under low magnification with 1% v/v glycerol (Carl Roth, Germany) and incubated (50–100x).
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