Black fungal extremes - CBS

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Yu r l o va e t a l.10090807060504030201004% MEA4% MEA + TRCzACzA + TR4% MEA4% MEA + TRCzACzA + TR4% MEA4% MEA + TRCzACzA + TR4% MEA4% MEA + TRCzACzA + TR4% MEA4% MEA + TRCzACzA + TRA.pullulans VKMF-2205A.pullulans VKMF-2204A.pullulans VKPMF-370H.macrosporumVKM F-2452H.dematioidesVKM F-2836The intensity of growth, %The intensity of pigmentation,%Fig. 6. The influence of tricyclazole on growth and pigmentation of strains belonging to the fourth group.Y-axis: intensity of growth, intensity of pigmentation, %.X-axis: 4 % MEA = 4 % malt extract agar; 4 % MEA + TR = 4 % malt extract agar with 20 μL/mL tricyclazole; CzA = Czapek agar; CzA + TR = Czapek agar with 20 μL/mLtricyclazole.VKM F-179 and A. pullulans var. aubasidani VKPM F-448 did notsecrete 2-HJ and flaviolin both in the presence of tricyclazole andwithout tricyclazole (Table 3).DISCUSSIONThree out of four black yeast genera analysed (Aureobasidium,Hormonema and Kabatiella) (Table 1) belong to the ascomycetousorder Dothideales, while Exophiala is an anamorph ofChaetothyriales (de Hoog et al. 1999). Many authors (Siehr 1981,Taylor et al. 1987, Butler & Day 1998, Butler et al. 2004, Kogejet al. 2004) indicated that both types of fungi synthesise a DHNtypemelanin. Details of the DHN-type melanin pathway havebeen elucidated using a number of different fungi. Much of what isknown about the pathway and its enzymes has come from the useof melanin-deficient strains and compounds, such as tricyclazole,which inhibit specific enzymes in the pathway (Bell & Wheeler1986, Butler & Day 1998).The systemic fungicide tricyclazole [5-methyl-1,2,4-thiazolo(3,4,b)-benzothiazile] (TR) is an inhibitor of biosynthesis ofmelanins, which form via the pentaketide pathway (Bell & Wheeler1986). For example, it is known to strongly inhibit the enzymaticreduction (reductase enzymes) of 1,3,8-trihydroxynaphthalene(1,3,8-THN) to vermelone. Tricyclazole has also been shown toweakly inhibit the reduction of 1,3,6,8-tetrahydroxynaphthalene(1,3,6,8-THN) to scytalone (Wheeler & Greenblatt 1988).Flaviolin and 2-hydroxyjuglone (2-HJ) are known as autoxidativeproducts of 1,3,6,8-THN and 1,3,8-THN, respectively (Fig. 7). Thepresence of flaviolin and 2-HJ in fungal cultures, treated withtricyclazole, is usually accepted as proof that 1,3,6,8-THN and1,3,8-THN were involved in the synthesis of DHN-melanin (Butler& Day 1998). Once produced, 1,3,8-DHN is reduced to vermelone,which in turn is dehydrated to 1,8-dihydroxynaphthalene (DHN)(Bell & Wheeler 1986, Taylor et al. 1987) (Fig. 7). In most cases,these two reactions are carried out by the same reductase anddehydratase enzymes that produce 1,3,8-THN from 1,3,6,8-THN.DHN appears to be polymerised to melanin via a laccase (Butler& Day 1998).In the present investigation we demonstrated, that the DHNmelanininhibitor, tricyclazole, inhibited melanin biosynthesis only insome black yeast strains. Four groups were distinguished, differingby their ability to produce pigment with o- and p-diphenoloxidasesubstrates and to be inhibited by tricyclazole (Table 4).The effect of tricyclazole on pigment production proved to bemore pronounced when strains were grown on CzA. On this medium53.3 % of the strains were inhibited by tricyclazole, whereas only26.6 % of the strains decreased their intensity of pigmentation46
Pi gm e n t f o r m at i o n in b l a c k y e a s t-l i k e f u n g iTable 3. Melanin metabolites analysed by TLC in control cultures and in tricyclazole-inhibited cultures ofA. pullulans VKM F-179, VKM F-370, VKPM F-371 and A. pullulans var. aubasidani VKPM F-448.Accession no. Tricyclazole 1 Metabolites 22-HJ flaviolin 3,3 ’ -biflaviolinVKM F-179 − − − −+ − − −VKM F-370 − − − −+ + + −VKPM F-371 − − − −+ + − +VKPM F-448 − − − −+ − − −1Tricyclazole concentration in the medium was 0 μg mL -1 (−) or 20 μg mL -1 (+).2“+ “ = metabolite was observed; “− “ = metabolite was not observed.VKM/VKPM = Russian Collection of microorganisms, Puschuno, Russia.Table 4. Subdivision of the strains into pigmentation groups.Strains Pigmentation on substrates of Influence of tricyclazole on intensity ofo-diphenoloxidases p-diphenoloxidases pigmentation growth4 % MEA CzA 4 % MEA CzAGroup 1 (12/12) 1Exophiala nigra VKM F-2137 + + - + - -Exophiala. prototropha CBS 534.94 + + + + - -Group 2 (8-10/12) 2A. pullulans SPChPhA 129(11) + + - - - +K. lini CBS 125.21 + + - + + +Group 3 (5-7/12) 3A. pullulans VKPM F-371 + + - - + -A. pullulans CBS 105.22 + + - + + -A. pullulans VKM F-1125 + + - + - -A. pullulans var. aubasidani VKPM F-448 + + + + - -A. pullulans SPChPhA 2320 + + - + - -Group 4 (1-3/12) 4A. pullulans VKM F-2204 + + - - - -A. pullulans VKM F-2205 + + - - + -A. pullulans VKM F-370 - + + - - -H. dematioides VKM F-2836 - + - * + *H. macrosporum VKM F-2452 + + + - + +* H. dematioides F-2836 did not grow at all on CzA.Abbreviations used: “+ “ = characteristic was observed; “− “ = characteristic was not observed.1Strains produced black pigments when they were cultivated on all 12 aromatic substrates used: both on o-diphenoloxidases and on p-diphenoloxidases substrates;2Strains produced dark pigments when they were cultivated on 8–10 aromatic substrates from 12 used: both on o-diphenoloxidases and on p-diphenoloxidases substrates;3Strains produced dark pigments when cultivated on 5–7 aromatic substrates from 12 used: both on o-diphenoloxidase and p-diphenoloxidase substrates;4Strains produced dark pigments when cultivated on 1–3 aromatic substrates from 12 used: both on o-diphenoloxidases and on p-diphenoloxidases substrates.when they were cultivated on 4 % MEA with tricyclazole (Table4). Metabolites from ethyl acetate extracts of biomass from A.pullulans VKM F-179 = CBS 105.22, VKM F-370, VKPM F-371 andA. pullulans var. aubasidani VKPM F-448 were analysed by thinlayerchromatography to determine if DHN-melanin precursors orrelated metabolites were present. Flaviolin and 2-HJ were detectedonly in the extracts of 14-d-old cultures of A. pullulans VKM F-370,A. pullulans VKPM F-371, when they were grown on CzA with 10and 20 μg/mL tricyclazole. However, flaviolin and 2-HJ were notfound in acetone extracts of biomasses of these strains, whenthey were grown in CzA without tricyclazole (Table 3). Strains A.pullulans VKM F-179, A. pullulans var. aubasidani VKPM F-448did not secrete 2-HJ and flaviolin, neither in the presence of norwithout tricyclazole (TR) (Table 3) and even when they werewww.studiesinmycology.org47
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Studies in Mycology 61 (2008)Black
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On o f r i e t a l.2005). The abili
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De n g e t a l.Table 1. Strains use
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De n g e t a l.10098CBS 157.67 Exop
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homogentisate 165, 171, 173Hortaea
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CBS Biodiversity SeriesNo. 6: Alter
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Studies in Mycology (ISSN 0166-0616
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Satow MM, Attili-Angelis D, Hoog GS
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Black fungal extremes - CBS

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