Melanin Pigments of Fungi Under Extreme Environmental Conditions (Review) N
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ISSN 00036838, Applied Biochemistry and Microbiology, 2014, Vol. 50, No. 2, pp. 105–113. © Pleiades Publishing, Inc., 2014. Original Russian Text © N.N. Gessler, A.S. Egorova, T.A. Belozerskaya, 2014, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2014, Vol. 50, No. 2, pp. 125–134. Melanin Pigments of Fungi under Extreme Environmental Conditions (Review) N. N. Gesslera, A. S. Egorovaa, and T. A. Belozerskayab Bach Institute of Biochemistry, Russian Academy of Sciences, Moscow, 119071 Russia Department of Biology, Moscow State University, Moscow, 119991 Russia email: [email protected] Received September 2, 2013 Abstract—This review is dedicated to the research on the functions of melanin pigments in fungi. The par ticipation of melanin pigments in protection from environmental factors is considered. Data on the biosyn thetic pathways and types of melanin pigments in fungi are presented. DOI: 10.1134/S0003683814020094 INTRODUCTION (members of the family Teratosphaeriaceae), Dot The study of melanin pigments has over time hideales, Pleosporales, Myriangialis, as well as some shown their importance for the survival of fungi under unidentified groups related to Dothideomycetes [13], extreme environmental conditions, including the pro were identified. When grown under the harsh condi tection of pathogenic fungi from the action of reactive tions of the Antarctic in cracks of rocks, the micro oxygen species (ROS) in host cells. A clear under scopic fungi Cryomyces antarcticus and Cryomyces mint eri showed high resistance to UV radiation (280– standing of the molecular mechanisms of the resis 2 tance of extremophilic fungi and fungal pathogens 360 nm, 3W/m ), which they were able to sustain for allows one to identify targets for new drugs. few hours, whereas nonpigmented Saccharomyces pastorianus cells died after 30 min of exposure [14]. Melanin pigments were found in representatives of all natural kingdoms from bacteria to mammals. They Under natural conditions, extremophylic fungi often color the vestiture of fish, birds, and animals. In often form a community with bacteria, algae, and fungi melanin is an important protective factor against plants [15–16]. More than 80% of endophytic fungi the adverse effects of environmental stresses, such as that exist in the community with the herbaceous plant UV radiation, drying, high concentrations of salts, Deschampsia antarctica Desv. (Poaceae) in Antarctica heavy metals, and radionuclides. The presence of mel produced melanin pigments [17]. These findings were anin allows fungi to exist under the influence of high consistent with earlier comments regarding the bene electromagnetic radiation, for example, in high fits of melanized fungi under the conditions of high mountain regions, desert soils, and on plant surfaces. insolation, drought, and low temperatures. Under extreme conditions, the proportion of mela Melanized fungi also exhibit improved resistance to nized fungi in mycobiota usually increases, for exam high concentrations of salts. Hortaea werneckii, ple, in ecotopes contaminated with radionuclides [1–4]. Phaeotheca triangularis, Trimmatostroma salinum, In aerial environments, the amount of melanized Aureobasidium pullulans, and Cladosporium spp. live in spores is higher than in the soil [5]. It was shown salterns and are able to tolerate high (close to satura experimentally that darkcolored spores of many fungi tion) salt concentrations [18]. For some types of these are resistant to UV irradiation [6, 7]. The presence of fungi (H. werneckii, R. triangularis, and T. salinum), melanin pigments ensures a high survival rate during hypertonic sodium chloride solutions are their natural high levels of UV radiation, while nonpigmented environment [19]. It was suggested that the presence forms die within a few minutes. Microcolonial yeast of melanin in the cell wall of H. werneckii reduces the like fungi growing on rocks under the conditions of flow of salt into the cell [19]. extreme temperatures, high insolation, drought, and The presence of melanin ensures the survival of low concentrations of organic compounds are strongly microscopic fungi under the conditions of techno melanized [8–10]. Viable cells of these fungi were genic pollution. In industrial and roadside areas, an found in the Antarctic [11, 12]. A genetic analysis of increase in the proportion of darkcolored melanin microcolonial melanized fungi growing on the surface containing fungi, which were more resistant to con of stones allowed to classify many of them as the Dot tamination in urban areas by heavy metals and unsat hideomycetes (including Eurotiomycetes) and related urated hydrocarbons, was observed [20, 21]. In urban Arthoniomycetes classes. Among them, Capnodiales conditions in air and snow samples, representatives of 105 106 GESSLER et al. the genera Cladosporium and Alternaria were domi development of conidia and their resistance to UV nant [22, 23]. radiation [42]. Melanins in Magnaporthe grisea—a Radionuclide contamination led to a change in pathogen of rice blast—are needed as an antioxidants fungal communities, an increased proportion of mela that protect the fungus from plant ROS [43, 44]. Lov nized fungi, and a reduced diversity of species [3, 4, astatin inhibits the synthesis of melanins in the patho 24]. Most common in contaminated zones were the genic fungi M. grisea, Stagonospora nodorum, Colletotri species Cladosporium, Ulocladium, Stachybotris, and chum atramentarium, and Bipolaris sorokiniana; this Humicola. The species Cladosporium sphaerospermum, inhibition reduces the virulence of the fungi and allows C. herbarum, C. cladosporioides, Alternaria alternata, recommending lovastatin as an indirectaction fungi and Aureobasidium pullulans were widely available [3, cide [45]. 25]. Melanized fungi (mainly Cladosporium spp., Melanins are one of the main factors in the patho A. alternata, A. pululans, and Hormoconis resinae) genesis of Gaeumannomyces graminis, which is a caus were found even in environs of the destroyed reactor in ative agent of the root rot of gramineous. Isolates, Chernobyl [25]. The presence of melanin was also which did not synthesize melanins, were able to colo shown in lightcolored fungi, distributed in the area nize the roots of gramineous, but any visible symptoms around the Chernobyl nuclear power plant: of the disease were not observed [46]. The lack of mel A. versicolor and Purpureocillium lilacinum (Paecilo anin pigments in mutant Alternaria brassicicola strains myces lilacinus, according to the old classification) can not only cause a change in the color and increased [26, 27]. The latter species, along with Chaetomium sensitivity to UV radiation but also reduce the resis aureum, was recognized as a bioindicator of soil con tance to proteolytic and glycolytic enzymes [47]. Mel tamination within the range 3.7 × 106–3.7 × 108 Bq/kg anins protect Rhizoctonia solani from bacterial lysis [3]. In P. lilacinum, strains isolated from contaminated [48]. Transformation of the entomopathogenic fungus areas had a melanin content that was 2–2.5 times Metarhizium anisopliae with melanin synthesis genes higher than in related strains that lived in areas isolated increases the efficiency of the application of this fun from the background level of radioactivity [26, 28]. gus against larvae of the cabbage moth (Plutella xylos The distribution of melanized fungi in areas with high tella) [ 49]. levels of radiation undoubtedly reflects their advantage Localization of melanins in fungi. Melanin pig over lightcolored fungal species; however, a majority ments in fungi may be detected in the cell wall or of the basic mechanisms of radiation resistance of liv secreted into the environment. Melanins can be seen ing organisms are not currently established [29]. as a dark substance in the cell wall during microscopic A majority of melanized fungi that are adapted to examination [19, 50]. Investigations of the micro extreme conditions, phylogenetically are similar to structure of melanins associated with the cell wall of melanized pathogenic fungi, capable of withstanding C. neoformans showed that it is represented by multiple ROS attacks in host cells [30]. Melanized opportunis layers of spherical granules (50–80 nm in diameter), tic fungi have adapted to dishwashers and are able to located under the polysaccharide capsule and adjacent survive elevated temperatures and the presence of to the plasma membrane [54]. In the halophilic fungus detergents [31]. The melanized yeasts Exophiala der H. werneckii with an optimal concentration of salt matitidis and E. phaeomuriformis (Chaetothyriales), (0.86 M NaCl), the melanized dark layer is on the which may cause systemic diseases in humans, were outer part of the cell wall, but the whole cell wall is the fungi most frequently (up to 56% of the detected smelanized when the concentration of salt is increased mycobiota) found in dishwashers. Probably, the high [19]. Dark melanin granules were found in the fibrillar temperature, high humidity, and the alkaline medium matrix on the surface of the cell wall in A. pullulans, in dishwashers provide an alternative environment for Verticillium dahliae, and Phomopsis sp. [51]. In the these pathogenic fungi. presence of a melanin precursor—3,4dihydroxyphe The presence of melanins in pathogenic fungi can nylalanine (DOPA)—melanin granules are formed on have a significant impact on the development of dis the surface of conidia and yeast cells of the dimorphic eases. Thus, it was shown that virulence was signifi pathogenic