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Rock-Inhabiting Fungi Studied with the Aid of the Model Black Fungus Knufia Petricola A95 and Other Related Strains

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Rock-Inhabiting Fungi Studied with the Aid of the Model Black Fungus Knufia Petricola A95 and Other Related Strains M.Sc. Corrado Nai Rock-inhabiting fungi studied with the aid of the model black fungus Knufi a petricola A95 and other related strains BAM-Dissertationsreihe • Band 119 Berlin 2014 Die vorliegende Arbeit entstand an der BAM Bundesanstalt für Materialforschung und -prüfung. Impressum Rock-inhabiting fungi studied with the aid of the model black fungus Knufi a petricola A95 and other related strains 2014 Herausgeber: BAM Bundesanstalt für Materialforschung und -prüfung Unter den Eichen 87 12205 Berlin Telefon: +49 30 8104-0 Telefax: +49 30 8112029 E-Mail: [email protected] Internet: www.bam.de Copyright © 2014 by BAM Bundesanstalt für Materialforschung und -prüfung Layout: BAM-Referat Z.8 ISSN 1613-4249 ISBN 978-3-9816380-8-0 Rock-inhabiting fungi studied with the aid of the model black fungus Knufia petricola A95 and other related strains Inaugural dissertation to obtain the academic degree Doctor rerum naturalium (Dr. rer. nat.) Submitted to the Department of Biology, Chemistry and Pharmacy of the Freie Universität Berlin by CORRADO NAI from Wallisellen (Switzerland) April 2014 First reviewer Prof. Dr. Rupert Mutzel Second reviewer Prof. Dr. Anna A. Gorbushina Day of disputation 11 July 2014 To Pia & Marco and Emilia & Oscar, without whom I would not be writing this. To Sissi, – always. Considerate la vostra semenza: Fatti non foste a viver come bruti, Ma per seguir virtute e canoscenza. Dante, Inferno XXVI, 118-120 ACKNOWLEDGMENTS ACKNOWLEDGMENTS This work was primarily conducted at the Federal Institute for Materials Research & Testing (BAM) in Berlin, Germany, in the framework of its Ph.D. Programme, between August 2010 and February 2014. While I hope to have made an interesting contribution to the Black Yeast Community, this would not have been possible without many persons. Thank you to Prof. Dr. Anna Gorbushina for giving me the chance to write the Ph.D. Thesis in an exciting research subject at the Department “Materials & Environment” of the BAM, Research Group “Model Biofilm in the Material Sciences,” as well as for her supervision and the scientific discussions. Thank you to Prof. Dr. Rupert Mutzel at the Freie Universität Berlin for being the Erstgutachter and allowing me to graduate at the Department of Biology, Chemistry and Pharmacy, and for the excellent chili con carne at the Lange Nacht der Wissenschaften. Dr. Francesc X. Prenafeta-Boldú hosted me as research student in autumn 2012 in his group at the Institute of Agrifood Research & Technology (IRTA) in Torre Marimon (Catalonia, yet Spain). Parts of this thesis could only be developed due to his skilled supervision and sharp observations. I was amazed by the friendliness and open-heartedness of the Catalan people. Gràcies, Francesc. Science is a community effort, and I am indebted to Nicole Knabe, Pedro Martin-Sanchez, Annette Naumann, Steffi Noack-Schönmann, Franz Seiffert and Jörg Toepel at the BAM for their collaboration, their constructive criticism and the collegial working atmosphere. Thank you to Dr. Barry Bochner from Biolog Inc. (United States) for his professional and friendly support with the Biolog System and for being a kind host at the 2013 Biolog Conference in San Francisco. A valuable part of the experimental results was produced by several undergraduate students whom I was fortunate enough to supervise, in particular Leoni Lang, Annette Pannenbecker, Michael Riddermann, Marco Tosi and Helen Y. Wong. I hope they learned from me as much as I learned from them thanks to their curiosity and enthusiasm. Thank you to Prof. Dr. Regine Hengge for the participation at her Science&Theatre seminar at the Freie Universität Berlin and her insights on science and its social and cultural implications, for which I am truly grateful. Thank you to my brother Alessandro for being a conspicuous role model. I suspect that if I wouldn’t have chosen to study another discipline this thesis became a faded blueprint of yours. A sincere thanks to Sissi and all my family and friends scattered throughout many locations for their continuous support, friendship, patience – and love. If I don’t mention you by name here, be sure than exclusively word savings – not oblivion – gained the upper hand. IX ACKNOWLEDGMENTS Halfway through this work I stopped cutting my hair, and besides the fact that it appealed my girlfriend it had two further advantages. Firstly, it was a tangible morning reminder of the efforts spent so far; and, secondly, it was a growing incentive for a swift graduation – if anything just for the sake of savings in shampoo. A Berliner barber will hopefully be pleased soon. Without you he must have waited way longer. Thank you. Danke. Grazie. спасибо. Gràcies. Gracias. 谢谢 Merci. X ABSTRACT ABSTRACT Black fungi are recently described microorganisms and amongst the most stress-tolerant eukaryotes currently known. They are a taxonomically diverse, but morphologically similar group of filamentous fungi that share two distinct signature characteristics, i.e. melanisation of the cell wall and compact colony morphology, which confer them passive, constituent extremotolerance. Albeit morphologically undifferentiated, black fungi show extensive phylogenetic and ecological diversity. Due to their persistence in unfavourable niches, they are ubiquitous on deserts and in glaciers and are permanent settlers of rock and other atmosphere-exposed material surfaces as well as man-made environments like salterns, humidifiers and dishwashers, and thus widespread in temperate regions worldwide. Some members are devastating opportunistic pathogens of invertebrates or vertebrates, including humans; others show symbiotic potentials with co-occurring microorganisms in extreme ecosystems. Beside their interest for fundamental biology, black fungi are important for several applied applications, e.g. in biotechnology, astrobiology, bioremediation and material preservation. Despite recent advances in the study of these fungi, many biological questions remain to be clarified regarding the molecular mechanisms underlying persistence, their physiology and nutritional modes, and their specific interactions with putative symbiotic partners. Models for pathogenic and halotolerant black fungi are established; however, no model was yet available for rock- and material-inhabiting ones. This thesis introduces the strain Knufia petricola A95 as a suitable model to study rock- inhabiting lifestyle. For this purpose, the strain was characterised at the physiological and molecular levels by phenotype microarrays, growth experiments and genome analyses as well as further methods. Cell-wall mutants of K. petricola A95 isolated during the course of this study were described and included in the comparative analysis to investigate effect of melanisation on physiology and stress tolerance. Direct comparisons were also performed between the model strain and the phylogenetically distant but ecologically, biogeographically and morphologically highly similar rock inhabitant Coniosporium apollinis. Preliminary observations of a model biofilm of K. petricola A95 and the photosynthetic cyanobacterium Nostoc punctiforme ATCC 29133 are introduced to study symbiotic interactions of rock-inhabiting microorganisms. Data presented here are a contribution to the understanding of ecophysiology and extremotolerance of rock-inhabiting black fungi. XI ZUSAMMENFASSUNG ZUSAMMENFASSUNG Schwarze Hefen sind jüngst beschriebene Mikroorganismen und zählen zu den widerstandsfähigsten derzeitig bekannten Eukaryonten. Diese taxonomisch sehr unterschiedlichen, jedoch morphologisch undifferenzierten filamentösen Pilze teilen zwei Hauptcharakteristika, nämlich die Melanisierung der Zellwand und die kompakte, blumenkohlartige Koloniebildung, was den Organismen passive und konstitutive Extremotoleranz verleiht. Obwohl morphologisch meist ununterscheidbar, weisen Schwarze Hefen eine ausgeprägte phylogenetische und ökologische Diversität auf. Aufgrund ihrer Beständigkeit in widrigen ökologischen Nischen, sind solche Mikroorganismen sowohl ubiquitär in Wüsten und auf Gletschern als auch dauerhafte Ansiedler von Stein- und weiteren umgebungsexponierten Oberflächen sowie anthropogenen Umgebungen wie Salzwerken, Luftbefeuchtungsanlagen und Geschirrspülern, und sind daher in der gemäßigten Klimazone weltweit verbreitet. Einige Mitglieder dieser Gruppe sind verheerende opportunistische Pathogene von Wirbellosen oder Wirbeltieren, einschließlich Menschen; für weitere Mitglieder, weisen einige Beobachtungen auf eine symbiotische Lebensweise mit gleichzeitig auftretenden Mikroorganismen an extremen Standorten hin. Neben ihrem Interesse in der Grundlagenforschung, sind Schwarze Hefen wichtig für zahlreiche angewandte Bereiche wie z.B. in der Biotechnologie, Astrobiologie, Bioremediation und im Materialschutz. Trotz neuerlicher Fortschritte in der Untersuchung solche Pilze, sind viele biologische Fragestellungen zurzeit noch abzuklären, wie z.B. hinsichtlich der molekularen Mechanismen ihrer Stresstoleranz, ihrer Physiologie und Ernährungsweise, und ihrer spezifischen Wechselwirkungen mit vermeintlichen symbiontischen Partnern. Modellorganismen für pathogene und salztolerante Schwarze Hefen sind bereits beschrieben; allerdings war noch kein passendes Modell für stein- und materialbesiedelnde Pilze vorhanden. Diese Doktorarbeit führt den Stamm Knufia petricola A95 als geeigneten Modellorganismus zur Untersuchung gesteinsbesiedelnder Lebensweise ein. Unter dieser Zielsetzung, wurde der Stamm auf physiologischer und molekularbiologischer Ebene anhand phänotypischer
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