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Functional Compartmentation of the Gut in Wood-Feeding Higher Termites (Nasutitermes Spp.)

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Functional Compartmentation of the Gut in Wood-Feeding Higher Termites (Nasutitermes Spp.) TITLE PAGE ECOLOGICAL AND EVOLUTIONARY DRIVERS OF MICROBIAL COMMUNITY STRUCTURE IN TERMITE GUTS Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) am Fachbereich Biologie der Philipps-Universität Marburg, vorgelegt von Carsten Dietrich aus Erfurt. Universitätsstadt Marburg, 2015 Die Untersuchungen zur folgenden Arbeit wurden von Oktober 2011 bis Februar 2015 am Max-Planck- Institut für terrestrische Mikrobiologie in Marburg in der Forschungsgruppe von Prof. Dr. Andreas Brune durchgeführt. Vom Fachbereich Biologie der Philipps-Universität Marburg als Dissertation angenommen am: 11.05.2015 Tag der Disputation: 27.05.2015 Erstgutachter: Prof. Dr. Andreas Brune Zweitgutachter: Prof. Dr. Roland Brandl Drittgutachter: Prof. Dr. Stefan Rensing III IV Publications Folgende Publikationen sind aus dieser Dissertation entstanden: Brune A und Dietrich C (2015). The termite gut microbiota: Digesting the diversity in the light of ecology and evolution. Ann. Rev. Microbiol. 69. Dietrich C und Brune A (2014). The complete mitogenomes of six higher termite species reconstructed from metagenomic datasets (Cornitermes sp., Cubitermes ugandensis, Microcerotermes parvus, Nasutitermes corniger, Neocapritermes taracua, and Termes hospes). Mitochondr. DNA. Dec 4:1-2. Dietrich C*, Köhler T* und Brune A (2014). The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 80:2261-2269. Dietrich C*, Nonoh J*, Lang K, Mikulski L, Meuser K, Köhler T, Boga HI, Ngugi DK, Sillam-Dussès S und Brune A (eingereicht). Habitat selection and vertical inheritance drive archaeal community structure in arthropod guts. Köhler T, Dietrich C, Scheffrahn RH und Brune A (2012). High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl. Environ. Microbiol. 78:4691–4701. Li H*, Dietrich C*, Zhu N, Mikaelyan A, Ma B, Pi R, Liu Y, Yang M, Brune A und Mo J (eingereicht). Age polyethism drives community structure of the bacterial gut microbiota in the fungus-cultivating termite Odontotermes formosanus. Mikaelyan A, Dietrich C, Köhler T, Meuser K, Sillam-Dussès D und Brune A (eingereicht). Dietary and phylogenetic determinants of bacterial gut community structure in higher termites. Zheng H, Dietrich C, Thompson CL, Meuser K und Brune A (2015). Population structure of Endomicrobia in single host cells of termite gut flagellates (Trichonympha spp.). Microb. Environ. 30: 92–98. Folgende Publikationen aus dieser Dissertation sind in Vorbereitung: Dietrich C, Rossmassler K und Brune A (in Vorbereitung). Genome sequences of Fibrobacteres and TG3 obtained by marker-assisted compositional binning of multiple metagenomes. Rossmassler K, Dietrich C, Thompson C, Mikaelyan A und Brune A (in Vorbereitung). Comparative metagenomics reveal bacterial functional profiles in the hindgut compartments of higher termites. Folgende Publikationen sind nicht in dieser Dissertation enthalten, aber während meiner Studien entstanden: Guichard P, Desfosses A, Maheshwari A, Hachet V, Dietrich C und Brune, A, Ishikawa T, Sachse, C und Gönczy P (2012). Cartwheel architecture of Trichonympha basal body. Science 337:553–554. Meyer BH, Peyfoon E, Dietrich C, Hitchen P, Panico M, Morris HR, Dell A und Albers SV (2013). Agl16, a thermophilic glycosyltransferase mediating the last step of N-glycan biosynthesis in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius. J. Bacteriol. 195:2177–2186. Zheng H, Dietrich C, Radek R and Brune A (eingereicht). Endomicrobium proavitum, the first isolate of Endomicrobia class. nov. (phylum Elusimicrobia) – an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase. Weiterhin sind folgende Beiträge während meiner Studien entstanden: Lang K, Mikulski L, Dietrich C, Meuser K und Brune A (2014). Methanogenic community structure in the digestive tracts of tropical millipedes. In Lang K. Diversity and ultrastrcuture of the seventh order of methanogens. Doctoral Thesis. University of Marburg. Nonoh JO, Dietrich C und Brune A (2013). Distribution of archaeal populations and methanogenic potentials in the highly compartmented gut of soil-feeding termites (Cubitermes ugandensis and Ophiotermes sp.). In Nonoh JO. Archaeal diversity and community structure in the compartmented gut of higher termites. Doctoral Thesis. University of Marburg. Nonoh JO, Dietrich C und Brune A (2013). Microenvironment and community structure of Archaea and Bacteria in the highly compartmented gut of Amitermes sp. (Isoptera: Termitinae). In Nonoh JO. Archaeal diversity and community structure in the compartmented gut of higher termites. Doctoral Thesis. University of Marburg. * Diese Authoren haben zu gleichen Teilen beigetragen. V VI Acknowledgements Ich danke… …meinem Doktorvater und Mentor Prof. Dr. Andreas Brune für sein großes Engagement und das Vertrauen, das er mir entgegengebracht hat. Besonders bedanke ich mich für seine Motivation, Ratschläge und stete Diskussionsbereitschaft, die immer wieder neue Impulse für diese Arbeit gab. Ganz besonders danke ich ihm für den Freiraum, den er mir für meine eigenen Ideen ließ und ich mich dadurch immer weiter entwickeln konnte. …Prof. Dr. Roland Brandl, Prof. Dr. Stefan Rensing, Prof. Dr. Uwe Maier und Prof. Dr. Martin Thanbichler für ihre Bereitschaft diese These zu begutachten und für ihre hilfreiche Kritik und anregenden Vorschläge. …Prof. Dr. Ralf Conrad, Prof. Dr. Johann Heider und Dr. Marc Dumont für ihre hilfreiche Kritik in meinem Thesis Advisory Commitee und auch dafür, dass sie mich abseits des TACs immer wieder unterstützt haben. …Prof. Dr. Ute Windisch und Prof. Dr. Harald Platen für deren immer noch anhaltende Unterstützung in meinem Werdegang und deren wertvolle Lehrveranstaltungen, die mich bis heute prägen. …der International Max Planck Research School for Environmental, Cellular and Molecular Microbiology für das Stipendium, das ich erhalten habe. Weiterhin bedanke ich mich bei allen Mitgliedern meines Jahrgangs für die hilfreichen Anmerkungen während der Seminare. …der gesamten AG Brune inklusive der Ehemaligen für ihre Forschungsergebnisse, die die Formulierung der Hypothesen meiner Arbeit erst erlaubt haben. Weiterhin bedanke ich mich für die anregende Kritik im Termiten-Seminar. Insbesondere möchte ich mich noch bei Dr. Claire Thompson, Dr. Tim Köhler, Dr. Jürgen Strassert, Dr. Aram Mikaelyan, Niclas Lampert und Hao Zheng für das tägliche wissenschaftliche Kaffeekränzchen bedanken. Weiterhin bedanke ich mich bei Dr. David Ngugi, der mich neugierig auf die AG Brune gemacht hat. Ich danke zudem der unverzichtbaren Katja Meuser dafür, dass sie meinen überschwänglichen „Ordnungsdrang“ ausgehalten hat und stets jedem hilft. …der gesamten Abteilung der Biogeochemie und deren Ehemaligen. Besonders bedanke ich mich bei Dr. Marcela Hernández und Dr. Marc Dumont für deren Interesse an meiner Arbeit. Mein besonderer Dank gilt Dr. Jennifer Pratscher, die mir in meiner Anfangszeit sehr geholfen hat. … Dr. Jennifer Pratscher, Miriam Runkel und Dr. Aram Mikaelyan und für das Gegenlesen dieser Arbeit. …meiner Familie inbesondere meinen Eltern, meiner Schwester und meiner Großmutter für deren Unterstützung und Glauben an mich. Meiner Partnerin danke ich sehr für die große Unterstützung besonders in der letzten Phase dieser Arbeit. VII VIII […] „Abseits der Straße beginnen die Entdeckungen“ — Hellmut Walters “Nothing in biology makes sense except in the light of evolution” — Theodosius Dobzhansky IX X Zusammenfassung Termiten sind eine Ordnung sozialer Insekten, die sich vermutlich vor 150 Millionen Jahren aus subsozialen Schaben entwickelt hat. Die Fähigkeit Holz zu verwerten erhielten (niedere) Termiten durch die Aufnahme cellulolytischer Flagellaten – eukaryotische Einzeller, die den Großteil des Darmvolumens einnehmen und das wichtigste Mikrohabitat für prokaryotische Mikroorganismen sind. Der Verlust der Flagellaten in der jüngsten Termitenfamilie, der Termitidae oder auch höhere Termiten genannt, führte zu einer ausschließlich prokaryotischen Darmmikrobiota sowie zu beachtlicher Substrat-Diversifizierung und enormem ökologischen Erfolg. Während die Unterfamilie Macrotermitinae eine Symbiose mit holzabbauenden Pilzen der Gattung Termitomyces einging, konnten andere höhere Termiten Substrate mit höherem Humifizierungsgrad verwerten. Vorhergehende Studien zeigten, dass sich die Termitendarmmikrobiota nah verwandter Termiten sehr ähnelt, aber zwischen entfernt verwandten Termiten deutliche Unterschiede zu finden sind. Da in der Literatur allerdings nur äußerst wenige Termiten auf ihre Darmmikrobiota hin untersucht wurden, ist nicht klar ob diese Unterschiede bestimmten Mustern folgen. Daher enthält diese Dissertation Studien, die die archaeelle und bakterielle Diversität der Darmmikrobiota über eine große Bandbreite von Termiten mittels Hochdurchsatzsequenzierung der 16S-rRNA-Gene untersuchen. Während die archaeelle Mikrobiota hauptsächlich aus methanogenen Organismen besteht, zeigt die bakterielle Darmmikrobiota eine deutlich höhere Diversität. Die Phyla Bacteroidetes, Firmicutes, Proteobacteria und Spirochaetes kommen in den Därmen fast aller Termiten vor, allerdings in variabler Abundanz. Dagegen treten andere Phyla wie Elusimicrobia, Fibrobacteres und die Candidatus Division TG3 nur in bestimmen Termiten- gruppen auf. Interessanterweise ändert sich die Abundanz
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