Se l b m a n n e t a l.Table 1. (Continued).Species Strain no. Source Geography ITS ReferenceTeratosphaeria mexicana <strong>CBS</strong> 110502 (CMW 14461) E. globulus Manjimup, Darling View, Plantation, Western Australia AY725558 Crous et al. 2007Teratosphaeria microspora <strong>CBS</strong> 110890 (CPC 1832) Protea leaf South Africa AY260097 Taylor et al. 2003Teratosphaeria molleriana <strong>CBS</strong> 111164 (CMW 4940; STE-U 1214) E. globulus Abrantes, Portugal AF309620 Crous et al. 2007CPC11842 Eucalyptus sp. Portugal DQ302989 Crous et al. 2006CPC11845 Eucalyptus sp. Portugal DQ302990 Crous et al. 2006<strong>CBS</strong> 116370 (CPC 10397) E. globulus Spain AY725561CPC 12056 DQ302991 Crous et al. 2006Teratosphaeria nubilosa <strong>CBS</strong> 116005 E (CMW 3282; CPC 937) E. globulus Austria AY725572 Crous et al. 2007CPC 4661 E. globulus Spain AY725570 Crous et al. 2004<strong>CBS</strong> 111445 (CPC 4660) E. globulus Spain AY725569 Crous et al. 2004CPC 3722 E. globulus Spain AY725568 Crous et al. 2004CPC 1099 E. globulus Tanzania AY725567 Crous et al. 2004<strong>CBS</strong> 111969 (CPC 1078) E. globulus Kenia AY725563 Crous et al. 2004CPC 4663 E. globulus Spain AY725571 Crous et al. 2004CPC 11882 E. globulus Portugal DQ302999 Crous et al. 2006CPC 11723 –CPC 11487 E. globulus Spain DQ302994 Crous et al. 2006CPC 11249 E. globulus Spain DQ302993 Crous et al. 2006CPC 11246 E. globulus Spain DQ302992 Crous et al. 2006<strong>CBS</strong> 114419 (CPC 10497) Eucalyptus globulus (Myrtaceae) New Zealand AY725574 Crous et al. 2007TC 0.42 E. globulus Australia DQ665659 –TC 0.40 E. globulus Australia DQ665657 –TC 0.47 E. globulus Australia DQ665658 –<strong>CBS</strong> 116283 (CPC 10495) E. globulus New Zeland AY725573 Crous et al. 2004Teratosphaeria nubilosa ( CPC 11885 E. globulus Portugal DQ303000 Crous et al. 2006Teratosphaeria ohnowa CPC 1005 – – AF309605 Crous et al. 2001<strong>CBS</strong> 112896* (CMW 4937; CPC 1004 ) E. globulus South Africa AF309604 Crous et al. 2001– – AF173299 –CMW 9103 – – AF468881 –<strong>CBS</strong> 110949 (STE-U 1006) E. grandis (Myrtaceae), leaves Hazyview, South Africa AY725575 –Teratosphaeria toledana <strong>CBS</strong> 113313 H (CMW 14457) Eucalyptus sp., leaves Toledo, Spain AY725580 –CPC 10840 Eucalyptus sp. Spain AY725581 Crous et al. 2004Abbreviations used: ATCC – American Type Culture Collection, Manassas, VA, U.S.A.; <strong>CBS</strong> – Centraalbureau voor Shimmelcultures, Utrecht, The Netherlands; dH – GS de Hoog private collection, <strong>CBS</strong>, Utrecht, The Netherlands; CCFEE – CultureCollection of Fungi From Extreme Environments, Università degli Studi della Tuscia, Viterbo, Italy; CMW – Culture collection of the Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa; CPC – Culturecollection of P Crous, housed at the <strong>CBS</strong>; IMI – International Mycological Institute, U.K.; MC – Collection of Istituto di Microbiologia di Messina, Italy; MZKI – Microbiological Culture Collection, National Institute of Chemistry, Ljubljana, Slovenia; STE-U –University of Stellenbosch <strong>fungal</strong> culture collection, Stellenbosch, South Africa; TRN – T Ruibal private collection; UAMH – The University of Alberta Microfungus Collection and Herbarium, Edmonton, AB, Canada.*Ex-type cultures.4
Dr o u g h t m e e t s a c i d2003/2004, and from rock samples collected in Mount Aconcagua,Andes, Argentina, and Monte Rosa in the Alps, Italy, as reportedin Table 1. The samples were collected using a sterile chisel,sterlilised in the field before each sampling, and preserved in sterilebags at –20 °C. To remove potential contaminants, rocks collectedin other environments than Antarctica were washed 15 min insterile physiological solution added with 0.1 % Tween 20 (Sigma- Aldrich, Munich, Germany) and rinsed 4 times with physiologicalsolution to remove any trace of the detergent. Isolations from rockswere performed by powdering the samples and seeding fragmentsin triplicate Petri dishes filled with 2 % malt extract agar (MEA,AppliChem, GmbH) and dichloran-rose bengal agar (DRBC, OxoidLtd., Basingstoke, Hampshire, U.K.). Media were supplementedwith chloramphenicol 100 ppm to prevent bacterial growth. Fungifrom lichens were isolated as follows: small fragments of thalli weresterilised by washing with H 2O 2(8 %) for 5 min, washed with steriledeionised water to remove any trace of H 2O 2and finally seededon MEA and DRBC. Plates were incubated at 5 and 15 °C andinspected every 15 d until no new colonies appeared. Colonieswere transferred to MEA slants and incubated at 15 °C. Strainsanalysed for comparison are listed in Table 1; they were taken fromreference collections of the Culture Collection of Fungi from ExtremeEnvironments (CCFEE, Viterbo, Italy) and the Centraalbureau voorSchimmelcultures (<strong>CBS</strong>, Utrecht, The Netherlands), including alarge set of strains sampled by P.W. Crous from plants with leatheryleaves in a semi-arid climate.MorphologyHyphal maturation and conidiogenesis were studied using bothlight and scanning electron microscope (SEM). Slide cultureswere seeded onto MEA, incubated for 10 wk and mounted in lacticacid. Samples for SEM observations were prepared according tomethods described by Onofri et al. (1980).DNA extraction and sequencingDNA was extracted from mycelial fragments taken from 6-mos-oldMEA slants grown at 10 °C, using Nucleospin Plant kit (Macherey-Nagel, Düren, Germany) following the protocol optimised forfungi. PCR reactions were performed using BioMix (BioLineGmbH, Luckenwalde, Germany). In each 25 µL reaction tube 5pmol of each primer and 40 ng on template DNA were added. Theamplification was carried out using MiniCycler (MJ Research,Waltham, Massachusetts, U.S.A.) equipped with a heated lid.The first denaturation step at 95 °C for 3 min was followed by:denaturation at 95 °C for 2 s, annealing at 55 °C for 30 s, extensionat 72 °C for 30 s. The last three steps were repeated 35 times,with a last extension 72 °C for 5 min. The products were purifiedusing Nucleospin Extract kit (Macherey-Nagel, Düren, Germany).Primers NS1, NS2, NS3, NS4, NS5, NS8, ITS1, ITS4 (White etal. 1990), SR10R (Bruns et al. 1992), ITS5, and ITS4a (Larenaet al. 1999) were employed to amplify SSU and ITS rDNAportions. Sequencing reactions were performed according to thedideoxynucleotide method (Sanger et al. 1977) using the TF BigDye Terminator 1,1 RR kit (Applied Biosystems). Fragments wereanalysed using an ABI 310 Genetic Analyser (Applied Biosystems).Sequence assembly was done using the software Chromas (v. 1.451996–1998, Conor McCarthy School of Health Science, GriffithUniversity, Southport, Queensland, Australia).www.studiesinmycology.orgAlignment and tree reconstructionSSU sequences were aligned with ARB beta-package (v. 22-08-2003, Ludwig et al. 2004; www.mikro.biologie.tu-muenchen.de/pub/ARB). The SSU alignment spanned positions 141–2512,which corresponds to 1515 bp with reference to Saccharomycescerevisiae. Trees based on SSU sequences were reconstructedwith neighbour-joining in ARB.ITS sequences were aligned iteratively with Ward’s averaging(Van Ooyen 2002) in a research data base of black yeasts presentat <strong>CBS</strong> using the BioNumerics package (Applied Maths, Kortrijk,Belgium). Due to gaps necessary for alignment, the ITS1 domainspanned 187 positions (real lengths 147–154 bp), the 5.8S gene156 positions and the ITS2 domain 184 positions (real lengths143–155 bp). The alignments were based on the positions 28–481,the initial and the final parts were cut off to compare fragmentswith the same length. Alignments were exported and the best-fitsubstitution model was determined using Modeltest MrAic.pl 1.4.3(Nylander 2004, program distributed by the author) estimatedusing Ph y m l (Guindon & Gascuel 2003) through hierarchicallikelihood ratio tests. MrAic calculates the Akaike InformationCriterion (AIC), corrected Akaike Information Criterion (AICc)and Bayesian Information Criterion (BIC); Akaike weights fornucleotide substitution model and model uncertainty. All 56 modelsimplemented in Modeltest were evaluated. Phylogenetic trees werereconstructed by Maximum Likelihood, using Tr e e f i n d e r (Jobbet al. 2004) and the resulting tree was displayed using Tr e e v i e wv. 1.6.6 (Page 1996). The robustness of the phylogenetic inferencewas estimated using the bootstrap method (Felsenstein 1985) with100 pseudoreplicates generated and analysed with Tr e e f i n d e r.As alignment over the entire complex was highly ambiguous, analgorithm for tree reconstruction without alignment, the DNA-walkDivergence method (DNAWD, Licinio & Caligiorne 2004; Caligiorneet al. 2005) was used, involving the entire spacer region. DNAwalksare defined by incrementing walk steps for each nucleotide inthe sequence (for example a positive step for purines, and negativefor pyrimidines). It makes simultaneous comparisons of the threedimensionalwalks (representing three composition skews): AG-TC, AC-TG, and AT-CG for each pair of sequences. One sequenceslides against the other until the minimum squared walk difference isfound, corresponding to a global alignment. This is then taken as ameasure of their distance since statistically independent mutationsand indels increase the mean square walk differences linearly. Theresulting distance matrices are then fed into the Kitsch program ofthe Phylip package (v. 3.572c, Felsenstein 1996).Cultural preferencesCultural characteristics and growth rates were recorded onPotato-Dextrose Agar (PDA), MEA, Czapek Dox Agar (CzA) andOatmeal Agar (OA). Strain <strong>CBS</strong> 119434 was incubated at 10 °C,strains <strong>CBS</strong> 122538, 122539 and 122540 at 20 °C and strains<strong>CBS</strong> 899.87, <strong>CBS</strong> 335.97, dH 12881, dH 11526 and dH 13081 at25 °C. The diameter of the colonies was recorded monthly. Testswere performed in triplicate.Temperature preferencesTemperature preferences for the strains <strong>CBS</strong> 119434, 122538,122539 and 122540 were tested by incubating them on MEA,5
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Studies in Mycology (ISSN 0166-0616
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Satow MM, Attili-Angelis D, Hoog GS