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Microbial Diversity and Community Structure in Deadwood of Fagus

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Microbial Diversity and Community Structure in Deadwood of Fagus Microbial diversity and community structure in deadwood of Fagus sylvatica L. and Picea abies (L.) H. Karst Inaugural-Dissertation zur Erlangung der Doktorwürde der Fakultät für Umwelt und Natürliche Ressourcen der Albert-Ludwigs-Universität Freiburg i. Brsg. vorgelegt von Dipl.-Forstwirt Björn Hoppe Freiburg im Breisgau Dekan: Prof. Dr. Tim Freytag Referent: Prof. Dr. François Buscot Korreferent: Prof. Dr. Siegfried Fink Disputationsdatum: 03.02.2015 ii Zusammenfassung Zusammenfassung Totholz wird im Rahmen forstwirtschaftlicher Aktivitäten zunehmend größere Bedeu- tung zuteil. Die Forstwirtschaft hat unlängst realisiert, dass die Förderung und der Er- halt natürlicher Totholzvorkommen von immenser Wichtigkeit für Ökosystemdienst- leistungen sind, nicht zuletzt, weil Totholz ein Reservoir für biologische und funktionel- le Diversität darstellt. Das Hauptziel dieser umfassenden Studie bestand zum einen in der Untersuchung des Einflusses unterschiedlicher Waldbewirtschaftungsstrategien auf die mikrobielle Diver- sität an Totholz zweier in Deutschland forstlich relevanter Baumarten Fagus sylvatica and Picea abies. Zum anderen sollte der Zusammenhang zwischen baumartspezifischen physikalischen und chemischen Parametern und den damit verbundenen Veränderungen der mikrobiellen Diversität aufgeklärt werden. Ein nicht unerheblicher methodischer Fokus lag hierbei in der Verknüpfung moderner molekularbiologischer Techniken („Next-generation sequencing“) mit klassischer, auf Observation basierender Feldmyko- logie. Die vorliegende Arbeit umfasst drei unabhängige, sich aber ergänzende Kapitel. Kapitel 2 umfasst eine Studie, die die Diversität und Artenzusammensetzung von Pilz- gemeinschaften an und im Totholz der beiden oben genannten Baumarten beschreibt. Des Weiteren wurde untersucht, inwieweit sich holzphysikalische und -chemische Ei- genschaften und pilzliche Diversität bedingen und ob eine erhöhte Diversität zu erhöh- ter Enzymaktivität und somit schnelleren Holzabbauraten führt. Hierfür wurden mole- kularbiologische Methoden (454-Pyrosequenzierung) zur Identifikation der Pilze mit Enzymassays und umweltanalytischen Verfahren (Massenspektrographie) zur Elemen- tenanalyse kombiniert. Diese Arbeit stellt die erste umfassende Gegenüberstellung von iii Zusammenfassung Totholz-(„ökosystemen“) der zwei in Deutschland forstwirtschaftlich relevantesten Laub- und Nadelbaumarten dar. Das Ergebnis der Studie stellt klar, dass Pilze spezi- fisch auf Totholz der entsprechenden Baumarten vorkommen. Dies lässt sich entschei- dend von der festgestellten Spezifität der physikalischen und chemischen Substrateigen- schaften ableiten. Darüber hinaus beeinflusst die ausgeübte Waldbewirtschaftung (Na- turwald versus Altersklassenbewirtschaftung) die Zusammensetzung der Artengemein- schaft. Beide Baumarten weisen auch unterschiedliche Sukzessionsmuster1 („dyna- mics“) auf. So tritt z.B. der Weißfäulepilz Resinicium bicolor dominant an Fichten- stämmen aller Zersetzungsstufen auf, wobei Vertreter der Xylariaceae das initiale Zer- setzungsstadium der Buchen dominieren und im weiteren Verlauf von Polyporaceae wie Fomes formentarius abgelöst werden. In Kapitel 3 ist die Untersuchung zur Diversität von nifH-Genen im Totholz beschrie- ben. Stickstoffverfügbarkeit im Totholz ist stark beschränkt und seit den 1960er Jahren wird vermutet, dass Pilze, die genau den Stickstoff zur Fruktifikation benötigen, Asso- ziationen mit Bakterien eingehen, die unter großer Energieaufwendung in der Lage sind, atmosphärischen Stickstoff zu spalten/ binden und somit biologisch verfügbar machen. Das hierbei untersuchte nifH-Gen, welches für das Enzym Dinitrogenase-Reduktase kodiert, fungiert als etabliertes Markergen für stickstofffixierende Bakterien in ver- schiedensten Umweltkompartimenten und Ökosystemen. Unsere auf „clone library se- quencing“ basierenden Untersuchungen konnten zeigen, dass die von uns identifizierten nifH-Gene spezifisch im Totholz vorkommen und bisher nicht in anderen Substraten verschiedener Ökosysteme (z.B. Meere, Flüsse, Seen, Böden, Ölfelder u.v.m.) detektiert wurden. Außerdem ließ sich die Artengemeinschaft Artenzusammensetzung auch zwi- 1 Von Sukzession im eigentlichen Sinne, kann nicht gesprochen werden, da keine Zeitreihen untersucht wurden. iv Zusammenfassung schen den beiden untersuchten Baumarten auftrennen und differenzieren. Darüber hin- aus zeigen die Ergebnisse einen signifikanten Zusammenhang zwischen Diversität der nifH-Gene und fruktifizierender Pilze. Zusätzlich konnte durch aufwendige Netzwerka- nalysen bestätigt werden, dass Interaktionen (sogenannte „Co-occurrence patterns“) zwischen bestimmten Stickstofffixierenden Bakterien und Pilzen nicht zufälliger Natur sind, sondern determiniert sind, also bestimmten Abhängigkeiten unterliegen. Während in Kapitel 2 die pilzliche Diversität an Totholz beschrieben wird, präsentiert Kapitel 4 die Ergebnisse zur gesamtbakteriellen Diversität. Auch hierbei wurde 454- pyrosequenciert, um Bakterien in den jeweiligen Totholzstämmen verschiedener Zerset- zungsstadien zu identifizieren. Alphaproteobacteria, Acidobacteria and Actinobacteria waren die dominanten taxonomischen Gruppen in beiden Totholzsubstraten. Interessan- terweise war ein signifikanter Anstieg von Bakterien der Ordnung Rhizobiales an Fa- gus-Stämmen der Zersetzungsstufe 3 zu verzeichnen (25% der Gesamtdiversität). Ein Großteil der Vertreter dieser Ordnung „besitzt“ das nifH-Gen, welches die Expression der Dinitrogenase-Reduktase ermöglicht. Des Weiteren veranschaulichen die Ergebnis- se, dass es auch im Falle der Artenzusammensetzung der Bakterien ähnliche und starke Korrelationen zu den holzphysikalischen und –chemischen Parametern gibt, wie sie in Kapitel 2 für Pilze identifiziert wurden. Außerdem konnte ein negativer Einfluss inten- siver Waldbewirtschaftung auf die bakterielle Diversität nachgewiesen werden. Insgesamt tragen alle Ergebniskapitel zum Nachweis einer bisher unbekannten Vielfalt von Pilzen und Bakterien bei, die potentiell am Totholzabbau beteiligt sind. Dass diese Gemeinschaften nicht unabhängig voneinander leben, sondern untereinander interagie- ren und eine Dynamik im Zusammenhang mit Baumart, Zersetzungsstufe, aber auch mit externen Variablen wie Waldbewirtschaftung aufweisen, zeigt, dass sie integraler und funktioneller Bestandteil der Biodiversität im Wald sind, und genau wie auffälligere v Zusammenfassung Gruppen der Waldbiozönose (z.B. Pflanzen, Insekten und Vertebraten) bei Untersu- chungen zur Waldfunktionen und -dienstleistungen, zu berücksichtigen sind. Die neuen Sequenzierungsmethoden ermöglichen es erst seit kurzer Zeit, diese Blackbox rational zu erforschen. vi Summary Summary Deadwood is gaining greater importance in the context of forestry activities. The forest- ry sector meanwhile has realized that the promotion and preservation of natural dead- wood occurrences is of immense importance for ecosystem services, since it serves as a reservoir for biological and functional diversity. An important objective of this compre- hensive study/ thesis was to explore the impact of different forest management intensi- ties on the microbial diversity in deadwood of the two in Germany silviculturally im- portant tree species Fagus sylvatica and Picea abies. Furthermore, the relationship be- tween tree species-specific physico-chemical properties and the associated changes of microbial diversity and species composition should be elucidated. A significant meth- odological focus was on the combination of modern molecular techniques ("Next- generation sequencing") together with classical field (-observation) mycology. This recent thesis comprises three independent but complementary chapters. Chapter 2 encompasses a study on the diversity and structure of fungal communities in the deadwood of the two above mentioned tree species Fagus sylvatica and Picea abies. This study further investigates the relation between physico-chemical properties and fungal diversity and whether an increase in diversity refers to higher lignin-modifying enzyme activities and increased wood decomposition rates, respectively. The study combines 454 pyrosequencing (to identify the fungal community), enzyme assays and chemical elements analyses (mass spectrography). The work presents the first compari- son of the deadwood (-ecosystems) of these two economically relevant coniferous and deciduous tree species. The results revealed that the fungal communities strongly corre- spond to the specific deadwood substrate, which occurred to be independently from the vii Summary surrounding habitat. This fact clearly relates to the specific substrate properties. The results further revealed that forest management type (age class managed beech and spruce forests versus extensively managed beech forests) significantly impacts the fun- gal community structure on the according forest plots. Both tree species also displayed distinct fungal successional patterns (dynamics). White-rot causing Resinicium bicolor, for example, occurred to be dominant on Picea abies deadwood logs of all decay stages, whereas members of the Xylariaceae were dominating the initially decayed logs of Fagus sylvatica and then were substituted by Polyporaceae (e.g. Fomes formentarius). Chapter 3 describes the investigations of the distribution of nifH genes in the same deadwood logs described in chapter 2. N-availability is highly restricted in deadwood and since the 1960s, it is assumed that fungi meet their N requirements for forming fruiting bodies by associating with bacteria which
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