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Aureobasidium Pullulans Varieties: Biotechnological Potential, Stress Tolerance, and Description of New Species Gostinčar Et Al

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Aureobasidium Pullulans Varieties: Biotechnological Potential, Stress Tolerance, and Description of New Species Gostinčar Et Al Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species Gostinčar et al. Gostinčar et al. BMC Genomics 2014, 15:549 http://www.biomedcentral.com/1471-2164/15/549 Gostinčar et al. BMC Genomics 2014, 15:549 http://www.biomedcentral.com/1471-2164/15/549 RESEARCH ARTICLE Open Access Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species Cene Gostinčar1,2*, Robin A Ohm3, Tina Kogej1, Silva Sonjak1, Martina Turk1, Janja Zajc1, Polona Zalar1, Martin Grube4, Hui Sun3, James Han3, Aditi Sharma3, Jennifer Chiniquy3, Chew Yee Ngan3, Anna Lipzen3, Kerrie Barry3, Igor V Grigoriev3 and Nina Gunde-Cimerman1,5 Abstract Background: Aureobasidium pullulans is a black-yeast-like fungus used for production of the polysaccharide pullulan and the antimycotic aureobasidin A, and as a biocontrol agent in agriculture. It can cause opportunistic human infections, and it inhabits various extreme environments. To promote the understanding of these traits, we performed de-novo genome sequencing of the four varieties of A. pullulans. Results: The 25.43-29.62 Mb genomes of these four varieties of A. pullulans encode between 10266 and 11866 predicted proteins. Their genomes encode most of the enzyme families involved in degradation of plant material and many sugar transporters, and they have genes possibly associated with degradation of plastic and aromatic compounds. Proteins believed to be involved in the synthesis of pullulan and siderophores, but not of aureobasidin A, are predicted. Putative stress-tolerance genes include several aquaporins and aquaglyceroporins, large numbers of alkali-metal cation transporters, genes for the synthesis of compatible solutes and melanin, all of the components of the high-osmolarity glycerol pathway, and bacteriorhodopsin-like proteins. All of these genomes contain a homothallic mating-type locus. Conclusions: The differences between these four varieties of A. pullulans are large enough to justify their redefinition as separate species: A. pullulans, A. melanogenum, A. subglaciale and A. namibiae. The redundancy observed in several gene families can be linked to the nutritional versatility of these species and their particular stress tolerance. The availability of the genome sequences of the four Aureobasidium species should improve their biotechnological exploitation and promote our understanding of their stress-tolerance mechanisms, diverse lifestyles, and pathogenic potential. Keywords: Aureobasidium pullulans, Dothideomycetes, Genome, Stress, Haloadaptation, Halotolerance, Polyextremotolerant, New species, Opportunistic mycosis, Pullulan Background applications in medicine, pharmacy, the food industry, Aureobasidium pullulans (de Bary) G. Arnaud is a polyex- and other fields [2,3]. A. pullulans also produces a β- tremotolerant black yeast of considerable biotechnological glucan that shows high reactivity to human IgG anti- importance, and it has exceptional stress tolerance and in- bodies [4] and possible beneficial immunomodulatory creasing medical relevance [1]. A. pullulans is well known effects [5]. A. pullulans has an unusually large spectrum for its production of pullulan, a neutral polysaccharide of extracellular enzymatic activities [6,7]. Several of these of repeating maltotriose units, which has numerous are of biotechnological interest, and include: amylases, cel- lulases, lipases, proteases, xylanases, β-fructofuranosidases, * Correspondence: [email protected] maltosyltransferases, mannanases, and laccases (for review, 1Department of Biology, Biotechnical Faculty, University of Ljubljana, Večna pot 111, Ljubljana SI-1000, Slovenia see [8]). At least some of these appear to have interesting 2National Institute of Biology, Večna pot 111, Ljubljana SI-1000, Slovenia Full list of author information is available at the end of the article © 2014 Gostinčar et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Gostinčar et al. BMC Genomics 2014, 15:549 Page 2 of 28 http://www.biomedcentral.com/1471-2164/15/549 traits that are different from their homologues in other production of extracellular enzymes [36], and by the species [8,9]. pronounced stress tolerance of A. pullulans [1]. AstrainofA. pullulans is used for the production of a Aureobasidium pullulans has evolved an exceptional cyclic peptide that has specific antifungal activity: aureoba- tolerance for a broad range of ecological conditions. It is sidin A [10]. Due to its strong antagonistic activity against considered a polyextremotolerant organism [1,37], and it other microorganisms, A. pullulans is used as a biocontrol can survive hypersaline [17], acidic, basic [38,39], cold and agent in agriculture [11]. Additionally, a recent study oligotrophic [40] conditions. Some of the A. pullulans reported that some strains of A. pullulans can produce an adaptations to stress (and especially to elevated salt con- antibacterial compound, exophilin A, as well as high yields centrations) are associated with rigorous management of of liamocins, and heavy oils with previously unknown ac- intracellular concentrations of alkali-metal cations [41], ylated mannitol structures, which have possible industrial synthesis of compatible solutes [42] and of mycosporines applications as surfactants [12]. [43], and adaptation at the level of the membrane-lipid TheoccurrenceofA. pullulans is widespread in tropical, composition [44,45]. A. pullulans can also mitigate envir- temperate and polar areas. It is frequently found in associ- onmental stress by rapid dimorphic switching from small ation with diverse plants, such as in the phyllosphere colourless yeast cells to thick-walled, heavily melanised, [13,14], as an epiphyte or endophyte, on stored barley grain meristematic forms [46]. [15], and in coconut water [16]. A. pullulans has also been The genus Aureobasidium is a member of the order found in numerous other habitats, some of which are par- Dothideales (Ascomycota, Dothideomycetes; Figure 1), ticularly unusual, such as coastal hypersaline water [17,18], and it comprises 27 taxa (species and varieties), with A. glacial ice [19,20], other polar environments [21,22], pol- pullulans being by far the most studied of these. Although luted water [23], refrigerated, frozen, salt-preserved and the distinction of varieties and forms of A. pullulans has dried foods [24,25], various indoor habitats (e.g., bathroom been suggested, the name A. pullulans is mainly used in surfaces [26], house dust [27], dishwashers [28], tap water research databases. The most recently described species [29]), the surface of human skin [30], aviation fuel tanks of Aureobasidium are A. leucospermi Crous [47], A. [31], and the surface of synthetic polymers [32] and of proteae (Joanne E. Taylor & Crous) Joanne E. Taylor & degrading polyurethane and PVC plastics [33]. A. pullulans Crous 2011 [47], and A. thailandense S.W. Peterson, has been reported to cause a variety of localised infections Manitchotpisit & Leathers [48]. in humans, and even systemic infections, although very Various loci have been sequenced in the past to infer rarely (for review, see [34,35]). It has been suggested that the taxonomy and phylogeny of the taxa in Aureobasi- this infection potential is at least partially supported by the dium, such as internal transcribed spacer (ITS) rDNA, Figure 1 The Aureobasidium pullulans varieties. A. Phylogram showing the phylogenetic relationships of the four A. pullulans varieties and their phylogenetic position, inferred from super alignment of selected fungal proteomes. Chi2-based branch supports are shown, calculated according to the approximate Likelihood-Ratio Test, as implemented in Phyml 3.0. B. Representative images of one-month-old cultures of the four A. pullulans varieties (as indicated) on malt extract agar and microscopy images of cultures after one week of growth on malt extract agar blocks. Gostinčar et al. BMC Genomics 2014, 15:549 Page 3 of 28 http://www.biomedcentral.com/1471-2164/15/549 intergenic spacer 1, translation elongation factor-1α, β- interest); (ii) their exceptional stress tolerance (mainly tubulin, and RNA polymerase II [19,47-49]. Based on a focusing on genes associated with the synthesis of compat- multilocus analysis of a worldwide selection of A. pullu- ible solutes and water management, transport of alkali- lans-like isolates, it was confirmed that the earlier described metal ions and water, the high osmolarity glycerol [HOG] variety A. pullulans var. melanogenum Hermanides-Nijhov pathway, and melanin synthesis); and (iii) evidence in is distinct from A. pullulans (de Bary) G. Arnaud 1918. In favour of describing these varieties as separate species. addition, two new varieties have been described: A. pullu- lans var. subglaciale Zalar, de Hoog & Gunde-Cimerman, Genome properties: sequencing and assembly of the and A. pullulans var. namibiae Zalar, de Hoog & Gunde- genomes Cimerman. A. pullulans var. aubasidani Yurlova (Yurlova The genome assembly sizes of
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