Black fungal extremes - CBS

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Za l a r e t a l.the type species of Aureobasidium. The genus was circumscribedusing criteria of conidiogenesis, i.e., synchronous holoblasticconidium production. This feature is also known in sporodochialKabatiella species forming defined leaf spots on specific host plants.When these fungi are cultured, the sporodochia fall apart, and themicromorphology becomes very similar to that of Aureobasidiumpullulans. For this reason, Hermanides-Nijhof (1977) classified allKabatiella species in Aureobasidium, even though most Kabatiellaspecies have not been cultured and are only known from thesporodochial anamorph on the host plant. LSU sequences of thefew species thus far available for study indeed show affinity to A.pullulans.Kabatiella zeae Narita & Y. Hirats. (Hermanides-Nijhof 1977)is found in isolated positions away from other aureobasidia (deHoog et al. 1999, Yurlova et al. 1999). Synchronous conidiationis thus polyphyletic. However, in addition to molecular differencesfor some species, morphological distinctions may also be possible,since most Kabatiella species have sickle-shaped conidia, suchas K. caulivora, K. harpospora (Bres. & Sacc.) Arx, K. phoradendri(Darling) Harvey f. umbellulariae Harvey, and K. zeae. In Kabatiellalini, a species clustering within A. pullulans (Fig. 2), the conidiahave similar shape, but are slightly larger than in the var. pullulans.Kabatiella microsticta, K. caulivora and another, related pycnidialfungus, Selenophoma mahoniae deviate in all of the genes studiedat the variety level. Thus, they might be regarded as separatevarieties of A. pullulans, but the possibility cannot be excluded thatunintentially the ubiquitous phyllosphere fungus A. pullulans wasisolated instead of the pathogen. It appears likely that the plantinvading,host-specific pathogens are consistently different fromA. pullulans, which on host plants colonises surfaces only, butunambiguously identified strains are needed to prove this.Our multilocus analysis shows that Aureobasidium pullulansconsists of three robust main groups, two of which have highstatistic support in LSU and show the same topology with all of thegenes sequenced. The ex-neotype of the species, CBS 584.75,is in group 1, A. pullulans var. pullulans. This group also containsCBS 146.30, the ex-type strain of Dematoideum nigrescens Stautz,CBS 701.76, the ex-type strain of Candida malicola D.S. Clark &R.H. Wallace, and CBS 100524, the ex-type strain of A. pullulansvar. aubasidani Yurlova, which should thus be regarded assynonyms. The production of aubasidan rather than pullulan as themain extracellular exopolysaccharide (Yurlova & de Hoog 1997) isapparently strain dependent. Although the production of EPS andother previously described diagnostic characters for this varietywere not evaluated in this study, we believe that used multilocusapproach as molecular diagnostic tool would show the difference ofvar. aubasidani to other varieties. The ex-type strain of Dematoidiumnigrescens (CBS 146.30) was the only initially darkly pigmentedstrain in group 1, which is probably due to its degeneration. Thevar. pullulans, which is newly defined, is phenetically characterisedby rapidly expanding, pinkish cultures that can develop radial darkbrown sectors due to the local presence of thick-walled, melanisedhyphae. Most isolates attributed to this variety originate fromsugary or osmotically fluctuating habitats, such as saline waterin the salterns, tree slime flux, fruit surfaces and phyllosphere(Table 1). This well supported variety was obtained pan-globallyfrom temperate to tropical habitats, and was also found trapped inSpitsbergen glaciers and in ice released from these glaciers intothe sea water. Its distribution is wide, ranging from the Arctic tothe Mediterranean coast. Given the small degree of diversity withTUB, ELO and EF1α, the taxon can be regarded as being relativelyrecent.Group 2, A. pullulans var. melanogenum contains CBS 105.22,the ex-type strain of this variety, and an authentic strain, CBS 123.37with the invalid description of Torula schoenii Roukhelman. Earlierdata (Yurlova et al. 1995) suggested that this taxon cannot bedistinguished from var. pullulans, but current sequence data showthat the groups are strictly concordant. Cultures are characteristicallyblack from the beginning. They produce an abundance of dark,ellipsoidal conidia, which can either originate from disarticulatinghyphae (arthroconidia) or transfer from hyaline conidia. The hyalineconidia are ellipsoidal and emerge from inconspicuous scarsalongside undifferentiated hyphae; the process of conidiogenesisis synchronous in addition to percurrent, the latter being identical tothat in the anamorph genus Hormonema. The sources of isolationof the strains of this variety, as far as is known, are low-nutrient,mostly low-strength environments, such as moist metal and glasssurfaces, showers, fountains, as well as ocean water. Only onestrain of this variety was retrieved from a human patient, but it isalso possible that this was a culture contaminant, since it is oftenreported in air, especially in warmer climates (Punnapayak et al.2003). Strains of this variety have a world-wide distribution, fromthe Arctic to the tropics. Given its marked diversity with TUB, ELOand EF1α, this may be an ancestral taxon, the introns havingaccumulated more mutations than var. pullulans.Group 3, A. pullulans var. subglaciale Zalar et al. is exclusivelyknown from Kongfjorden glacial and subglacial ice and sea water.Its psychrotolerant nature is in line with its active metabolism underconditions of permanently cold in Arctic glaciers.Group 4 consists of a single isolate, CBS 147.97, the ex-typeof the monotypic variety A. pullulans var. namibiae, isolated frommarble in Namibia, Africa. The strain takes an isolated positionwith all sequenced genes, but has not drifted far away from theancestral variety.Other related groups are 5 and 6, which are aureobasidiumlikebut consistently different. Strains of these groups thus far haveonly been recovered from glacial ice in Spitsbergen. The speciesoccurred with very high densities in subglacial ice in microchannels,and in gypsum-rich ice at high pH. During their travel through theglacier, these cells have been subjected to extreme variations ina wdue to ice freezing and thawing. These conditions are highlyselective, for which reason this entity is likely to be restricted tosmall endemic areas, such as Kongsfjorden (Skidmore et al. 2005).The description as novel species will be the subject of a laterpaper.The overall phylogenetic structure of A. pullulans suggests thatthe species is strictly clonal. A possible teleomorph, Discosphaerinafagi, has been suggested on the basis of ITS sequence similarity(de Hoog et al. 2000), but this finding awaits confirmation withmultilocus analysis and re-isolation from single ascospores.The varieties of Aureobasidium pullulans are markedly differentfor melanin production. This can be of biotechnological interest,since the organism is highly significant for its pullulan and aubasidanproduction (Yurlova & de Hoog 1997). Melanin contamination leadsto low pullulan quality. Attempts have been made to grow nonpigmentedyeast cells, e.g. by culturing A. pullulans in a two-stagefermentation process in media with a special nutrient combination(Shabtai & Mukmenev 1995), or with melanin-deficient mutants(Gniewosz & Duszkiewicz-Reinhard 2008). From the presentstudy, it is apparent that the use of strains of the variety pullulansis recommended.36
Ar c t i c Au r e o b a s i d i umACKNOWLEDGEMENTSThe authors would like to thank to Nick Cox (NERC Station) for his logistic supportin our Arctic excursions. We are indebted to Walter Gams, who provided Latindiagnoses. We also thank Fumiyoshi Abe, who donated valuable deep-sea isolates.The work in Kongsfjorden was funded by EU Large Scale Facility Fund. The workwas supported by the Slovenian Ministry of Education, Science and Sport.REFERENCESAbyzov SS (1993). Microorganisms in the Antarctic ice. In: Friedmann EI (ed.):Antarctic Microbiology, Wiley-Liss, New York: 265–297.Andrews JH, Harris RF, Speaer RN, Lau GW, Nordheim EV (1994). Morphogenesisand adhesion of Aureobasidium pullulans. Canadian Journal of Microbiology40: 6–17.Babjeva I, Reshetova I (1998). Yeast resources in natural habitats at polar circlelatitude. Food Technology and Biotechnology 36: 1–5.Bary A de (1884). 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Microbial Ecology 52: 207–216.Tamura K, Dudley J, Nei M, Kumar S (2007). Me g a 4: Molecular evolutionary geneticsanalysis (MEGA) software version 4.0. Molecular Biology and Evolution 24:1596-1599.Urzì C, De Leo F, Lo Passo C, Criseo G (1999). Intra-specific diversity ofAureobasidium pullulans strains isolated from rocks and other habitatsassessed by physiological methods and by random amplified polymorphic DNA(RAPD). Journal of Microbiological Methods 36: 95–105.Viala P, Boyer G (1891). Sur un Basidiomycète inferérieur, parasite des grainsde raisins. Comptes Rendues Hebdomaires des Séances de l’Académie deSciences, Paris 112: 1148–1150.Vishniac HS (2006). A multivariate analysis of soil yeasts isolated from a latitudinalgradient. Microbial Ecology 52: 90–103.www.studiesinmycology.org37
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Ce l l u l a r r e s p o n s e s t
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On o f r i e t a l.Table 1. Test pa
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On o f r i e t a l.2005). The abili
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A r o c k-i n h a b i t i n g a n c
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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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e n v i r o nm e n ta l is o l at i
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Origin o f Ex o p h i a l a d e r m
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s u b s t r at e s p e c i f i c i
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Bi o d i v e rs i t y o f t h e g e
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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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