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Prospecting the Biodiversity of the Fungal Family Ustilaginaceae for The Geiser et al. Fungal Biology and Biotechnology 2014, 1:2 http://www.fungalbiolbiotech.com/content/1/1/2 RESEARCH Open Access Prospecting the biodiversity of the fungal family Ustilaginaceae for the production of value-added chemicals Elena Geiser, Vincent Wiebach, Nick Wierckx* and Lars M Blank Abstract Background: Ustilaginaceae (belonging to the smut fungi) are commonly known for their plant pathogenicity. Although these microbes lead to yield reduction of cereal production, they can also have an economically positive side. Ustilaginaceae naturally produce a versatile range of value-added chemicals with potential applications in the food, pharmaceutical, and chemical industry. Results: In this study 68 Ustilaginaceae of 13 species were screened for the production of organic acids, polyols, and glycolipids from glucose to characterize their biodiversity and identify potential novel strains for biocatalysis of these valuable chemicals. Ustilago cynodontis, Ustilago maydis, Ustilago avenae, and Sporisorium exsertum were identified as promising production organisms for itaconate, malate, succinate, and erythritol, respectively. The influence of buffer concentration (pH) on acid production was investigated. Selected strains with best itaconate and malate production were characterized in more detail in bioreactor experiments obtaining total acid concentrations of up to 47 ± 1 g L−1. Conclusion: The identification and detailed characterization of these producers of valuable chemicals highlights the potential of these unicellular smut fungi for industrial applications and is a further step towards the biotechnological utilization of Ustilaginaceae. Keywords: Ustilago maydis, Ustilaginaceae, Organic acid, Polyole, Glycolipid, Itaconate, Malate, Succinate, Erythritol Background also non-pathogenic Ustilaginomycetes, such as Pseudo- The family Ustilaginaceae belongs to the order Ustilagi- zyma antarctica and Pseudozyma tsukubaensis. nomycetes (true smut fungi) and contains 17 genera, Although these plant diseases lead to a considerable such as Macalpinomyces, Sporisorium, Ustanciosporium, yield reduction of cereal production, smut fungi also have Pseudozyma, and Ustilago [1]. The entire family has an economically positive side. They naturally produce a described 607 species, including the model organism wide range of value-added chemicals (e.g. secondary Ustilago maydis, which is mostly studied in relation to metabolites, TCA cycle intermediates) with growing bio- its plant pathogenicity. Members of the Ustilaginaceae technological interest. Reported metabolites are polyols, can infect economically important crops including organic acids, extracellular glycolipids, iron-chelating side- corn, barley, wheat, oats, sorghum, sugarcane, and rophores and tryptophan derivatives [5,6]. Polyols, such forage grasses [2]. Symptoms they cause are tumor for- as erythritol (ery) and mannitol, for example, have large mation (Ustilago maydis) and phyllody in the inflores- markets as sweeteners for diabetics and as facilitating cences (Sporisorium reilianum) [3,4]. However, there are agents for the transportation of pharmaceuticals in medicine [7,8]. Itaconic (ita), L-malic (mal), succinic (suc), l-itatartaric (itt), and l-2-hydroxyparaconic (hp) acid are organic acids produced by many Ustilaginomycetes [6,9]. * Correspondence: [email protected] Applications for itaconic acid are for example the produc- Chair of Applied Microbiology, iAMB – Institute of Applied Microbiology, ABBt – Aachen Biology and Biotechnology, Worringerweg 1, D-52074 tion of resins, plastics, adhesives, elastomers, coatings, and Aachen, Germany nowadays itaconate is discussed as a platform chemical in © 2014 Geiser 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/2.0), 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. Geiser et al. Fungal Biology and Biotechnology 2014, 1:2 Page 2 of 10 http://www.fungalbiolbiotech.com/content/1/1/2 the production of biofuels [10,11]. Malic acid is used in species U. maydis, the acid concentration differed highly, many food products, primarily as an acidulant [12]. although the different strains generally produced the same Succinic acid is utilized as a precursor to pharmaceutical products (Additional file 1, Figure 1). However, there ingredients, such as additives, solvents, and polymers, but were strains which stood out by their relatively high also as a food additive and dietary supplement [13]. An- acid production. U. cynodontis 2217 was identified as the − other category of metabolites produced by smut fungi con- best itaconate producer with 3.3 ± 0.1 g L 1 itaconate and −1 tains extracellular glycolipids, such as mannosylerythritol a yield of 0.1 ± 0.0 gita gglc (Figure 1A). The best malate − lipids (mel) and ustilagic acid (ua) [14-16]. These lipids have producer was U. maydis 2162 with 11.1 ± 0.0 g L 1 malate −1 biosurfactant properties and can be used in pharmaceutical, and a yield of 0.3 ± 0.0 gmal gglc after 48 h cultivation cosmetic, and food applications and are known for their (Figure 1B). The final malate titer of S. cruentum 2211 − strong fungicidal activity on many species [5]. was in the same range with 11.0 ± 0.0 g L 1 and a yield −1 Besides the production of this broad range of metabo- of 0.3 ± 0.0 gmal gglc.However,theproductionratewas lites Ustilaginaceae have further positive characteristics. lower, because the highest malate titer was reached The haploid form of many strains grows unicellularly, after 96 h. Therefore, U. maydis 2162 was the preferred which is advantageous in comparison to filamentous malate producer. The highest succinate concentration of − fungi where control of fungal morphology is an important 2.5 ± 0.1 g L 1 was reached by U. avenae 2216 correspond- −1 process determinant [17]. Furthermore, the strains are able ingtoayieldof0.1±0.0gsuc gglc (Figure 1C). S. exsertum to metabolize a variety of poly- and monomers with carbo- 2212 produced the highest amount of erythritol, namely −1 −1 hydrate origin derived from renewable non-food biomass 3.8 ± 0.0 g L with a yield of 0.1 ± 0.0 gery gglc (Additional degradation [5,18,19], which are the substrates of choice for file 1, ery). future biotechnological bulk production processes [20]. In addition, the variety and relative ratio of produced These advantages make strains of the family Ustilagi- (glyco-) lipids amongst the tested genera and species dif- naceae promising candidates for industrial production fered considerably (Table 1). Because of the high variety of polyols, acids and lipids. So far large scale erythritol of possible lipids for which no standards are available, production by Pseudozyma tsukubaensis is the only the substances cannot be identified and quantified reported industrial use of Ustilaginaceae, which is also a exactly. Therefore, the relative ratio was estimated by − notable itaconate producer with up to 75 g L 1 itaconate visual inspection of TLCs. [8,9]. While the fundamental biology of these species is An additional screening in MES buffered screening studied in great detail, the biotechnological exploitation is medium was performed. MES is known for its significant still a relatively unexplored field. The production, as well impact on fungal metabolism [22,23]. Therefore, the as the ratio of the different products is strongly influenced influence of MES on growth and acid production of by both the chosen strain and culture conditions [6,21]. To several representative strains of the family of Ustilaginaceae, exploit nature’s biosynthetic capabilities, 68 Ustilaginaceae was investigated using cultures with MES, CaCO3,and of 13 species were screened for their production of itaco- a combination of both buffers. Neither growth nor acid nate, malate, succinate, erythritol, ustilagic acid, and man- production were negatively influenced by the presence nosylerythritol lipids from glucose to characterize their of MES per se (data not shown). Therefore, MES was biodiversity and identify potential novel strains for bioca- considered to be a suitable cultivation buffer. The MES talysis. High performing strains for the best itaconate and buffered screening confirmed the best producer for itaco- malate production were characterized in more detail in nate, malate, and succinate (Additional file 1), although bioreactor experiments. overall concentrations were generally lower than in CaCO3 buffered medium. Furthermore, the different Results and discussion buffer agents had a significant impact, especially on the Screening for best producer of itaconate, malate, succinate, mannosylerythritol lipids and ustilagic acid production. erythritol, ustilagic acid, and mannosylerythritol lipids Additional file 1 (TLC) shows the TLC of extracted For identification of potential novel strains for biocatalysis, lipids produced by different Ustilaginaceae cultivated 68 Ustilaginaceae of 13 species, with special focus on for 96 h in screening medium buffered with MES or 56 U. maydis strains, were cultivated in two different CaCO3 exemplarily for 12 different strains. In cultivations buffered, defined media and screened for their extracellu- with the stronger CaCO3 buffer
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