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Struktur Und Räumliche Verteilung Mikrobieller Gemeinschaften Im Verdauungstrakt Ausgewählter Boden-Invertebraten

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Struktur Und Räumliche Verteilung Mikrobieller Gemeinschaften Im Verdauungstrakt Ausgewählter Boden-Invertebraten Struktur und räumliche Verteilung mikrobieller Gemeinschaften im Verdauungstrakt ausgewählter Boden-Invertebraten Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) dem Fachbereich Biologie der Philipps-Universität Marburg vorgelegt von Markus Gundolf Georg Egert aus Göttingen Marburg/Lahn 2003 Die Untersuchungen zur folgenden Arbeit wurden von Dezember 2000 bis November 2003 am Max-Planck-Institut für terrestrische Mikrobiologie in Marburg unter Anleitung von Priv.-Doz. Dr. Michael W. Friedrich durchgeführt. Vom Fachbereich Biologie der Philipps-Universität Marburg als Dissertation angenommen am: 15.12.2003 Erstgutachter: Priv.-Doz. Dr. Michael W. Friedrich Zweitgutachter: Prof. Dr. Rudolf K. Thauer Tag der Disputation: 19.12.2003 „Jeder dumme Junge kann einen Käfer zertreten, aber alle Professoren der Welt können keinen herstellen.“ aus China Meinen Eltern, und meiner lieben Frau Dorit Die in dieser Dissertation beschriebenen Ergebnisse sind in folgenden Originalpublikationen veröffentlicht bzw. zur Veröffentlichung eingereicht: 1. Egert, M. und M.W. Friedrich (2003) Formation of pseudo-terminal restriction frag- ments, a PCR-related bias affecting terminal restriction fragment length polymorphism analysis of microbial community structure. Appl. Environ. Microbiol. 69:2555-2562. 2. Egert, M., T. Lemke, B. Wagner, A. Brune und M.W. Friedrich (2003) Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl. Environ. Microbiol. 69: 6659-6668. 3. Lemke, T., U. Stingl, M. Egert, M.W. Friedrich und A. Brune (2003) Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Appl. Environ. Microbiol. 69: 6650- 6658. 4. Egert, M., S. Marhan, B. Wagner, S. Scheu und M.W. Friedrich. Molecular profiling of 16S rRNA genes reveals diet-related differences of microbial communities in soil, gut, and casts of Lumbricus terrestris L. (Oligochaeta: Lumbricidae). Zur Veröffentlichung eingereicht bei FEMS Microbiol. Ecol. Folgende Manuskripte werden als Entwürfe präsentiert: 5. Egert, M., U. Stingl, L. Dyhrberg Bruun, B. Wagner, A. Brune und M.W. Friedrich. Physicochemical gradients and microbial diversity in the intestinal tract of the phyto- phagous larva of Melolontha melolontha (Coleoptera: Scarabaeidae). Einreichung geplant bei Appl. Environ. Microbiol. 6. Egert, M., L. Dyhrberg Bruun, B. Wagner, A. Brune und M.W. Friedrich. Analysis of microbial community structure and topology in the intestinal tract of the larva of Mel- olontha melolontha (Coleoptera: Scarabaeidae) reveals an enrichment of Desulfovibrio- related bacteria at the hindgut wall. Einreichung geplant bei Appl. Environ. Microbiol. Inhaltsverzeichnis Inhaltsverzeichnis Abkürzungen III Zusammenfassung IV-V 1 Einleitung 1 1.1 Die Bedeutung der Bodenfauna für den Umsatz organischer Substanz im Boden 1 1.2 Transformation organischer Substanz im Termitendarm 2 1.3 Scarabaeidenlarven und Regenwürmer als weitere Modellsysteme für die Transformation organischer Substanz 5 1.4 Molekulare Diversitätsanalysen im Intestinaltrakt von Boden-Invertebraten 7 1.5 Fragestellungen und Ziele der Arbeit 8 2 Material und Methoden 10 2.1 Chemikalien und Gase 10 2.2 Versuchstiere und ihre Präparation 10 2.2.1 Scarabaeidenlarven 10 2.2.2 Regenwürmer 12 2.3 Chemisch-physikalische Analysen 13 2.3.1 Gaschromatographie (Methan) 13 2.4 Molekularbiologische Untersuchungen 14 2.4.1 DNA-Extraktion 14 2.4.2 PCR-Amplifikation von 16S rRNA-Genen 15 2.4.3 Erstellung von 16S rRNA-Gen Klonbibliotheken 16 2.4.4 Sequenzanalyse 17 2.4.5 T-RFLP-Analyse 18 2.4.6 FISH 20 2.5 Bioinformatische Analysen 24 2.5.1 Sequenzverarbeitung 24 2.5.2 Phylogenetische Analyse von 16S rRNA-Genen 24 2.5.3 Entwicklung und Testen von Oligonukleotidsonden 25 2.5.4 Analyse der Sekundärstruktur von DNA-Fragmenten mit mfold 25 I Inhaltsverzeichnis 2.6 Statistische Methoden 26 2.6.1 Ökologische Indizes 26 2.6.2 Multivariate Statistik zur Analyse von T-RFLP-Profilen 28 3 Ergebnisse 30 3.1 Physiko-chemische Bedingungen und mikrobielle Aktivitäten im stark alkalischen Darm humivorer Rosenkäferlarven 30 3.2 Struktur mikrobieller Gemeinschaften in Mittel- und Enddarm humivorer Rosenkäferlarven 40 3.3 Weitere Untersuchungen zur mikrobiellen Besiedlung des Darms von Rosenkäferlarven 51 3.4 Physiko-chemische Gradienten und mikrobielle Diversität im Darm phytophager Maikäferlarven 54 3.5 Zusammensetzung und räumliche Verteilung mikrobieller Gemeinschaften im Enddarm phytophager Maikäferlarven 77 3.6 Direkte Visualisierung Desulfovibrio-verwandter Bakterien an der Enddarmwand von Maikäferlarven 107 3.7 Analyse mikrobieller 16S rRNA-Genprofile in Boden, Darm und Losung von Regenwürmern unter verschiedenen Fütterungsbedingungen 109 3.8 Pseudo-T-RFs: PCR-Artefakte mit Auswirkungen auf die T-RFLP-Analyse mikrobieller Gemeinschaften 133 3.9 Einsatz von Klenow-Fragment zur Vermeidung von pseudo-T-RFs 142 4 Zusammenfassende Diskussion 147 4.1 Struktur und räumliche Verteilung mikrobieller Gemeinschaften im Darm von Scarabaeidenlarven 147 4.2 Die Darmflora des Regenwurms – ein Vergleich mit anderen Boden-Invertebraten 160 4.3 Die Bedeutung von pseudo-T-RFs für die T-RFLP-Analyse mikrobieller Gemeinschaften 163 4.4 Ausblick: Integration von Struktur und Funktion mikrobieller Gemeinschaften im Intestinaltrakt von Scarabaeidenlarven 167 5 Literaturverzeichnis 169 II Abkürzungen Abkürzungen apsA: Gen für die α-Untereinheit der Adenosin-5´-Phosphosulfat-Reduktase CFB: Cytophaga-Flavobacterium-Bacteroides CLSM: Konfokales Laser-Scanning-Mikroskop DAPI: 4´,6-Diamidino-2-phenylindol DFA: discriminant function analysis DGGE: Denaturierende-Gradienten-Gel-Elektrophorese FAM: 6´-Carboxyfluorescein FG: Frischgewicht FISH: Fluoreszenz in-situ Hybridisierung ITS: internal transcribed spacer L1-3: Entwicklungsstadien der Scarabaeidenlarven MDS: multi-dimensional scaling OTU: operative taxonomische Einheit PCR: Polymerase Kettenreaktion PBS: phosphate buffered saline PFA: Paraformaldehyd RT: reverse Transkriptase T-RF: terminales Restriktionsfragment T-RFLP: terminaler Restriktionsfragment-Längen-Polymorphismus Alle weiteren Abkürzungen wurden entsprechend der „Information for authors“ des Euro- pean Journal of Biochemistry verwendet. III Zusammenfassung Zusammenfassung Boden-Makroinvertebraten sind entscheidend an der Transformation organischer Substanz beteiligt, die für viele Schlüsselfunktionen des Bodens verantwortlich ist. An den Transforma- tionsprozessen, die während der Darmpassage ingestierter organischer Substanz ablaufen, sind intestinale Mikroorganismen beteiligt, die auch für die Ernährung ihrer Wirte von ent- scheidender Bedeutung sind. Über die Zusammensetzung der mikrobiellen Gemeinschaften im Verdauungstrakt der meisten Boden-Invertebraten sowie ihre räumliche Verteilung inner- halb verschiedener Darmabschnitte ist allerdings nur wenig bekannt. Gerade die Topologie mikrobieller Gemeinschaften wird aber als eine wichtige Voraussetzung zum tieferen Ver- ständnis ihrer Funktion in Verdauungstrakten von Invertebraten angesehen, die von ausge- prägten axialen und radialen Gradienten physiko-chemischer Parameter geprägt sind. Im Rahmen dieser Arbeit wurden daher Struktur und räumliche Verteilung mikrobieller Ge- meinschaften im Verdauungstrakt der Larven zweier Scarabaeiden (Pachnoda ephippiata [Kongo-Rosenkäfer] und Melolontha melolontha [Feldmaikäfer]) und von Regenwürmern (Lumbricus terrestris) mit Methoden der molekularen mikrobiellen Ökologie untersucht. Während der Untersuchungen wurde zudem ein neuartiger PCR-Artefakt, die Bildung sog. pseudo-T-RFs, mit bedeutenden Auswirkungen für die T-RFLP-Analyse mikrobieller Ge- meinschaften entdeckt, beschrieben und mögliche Ansätze zu seiner Vermeidung aufgezeigt. In einer T-RFLP-Studie mit Regenwürmern wurde gezeigt, dass sich die Darmmikrobiota die- ser Tiere aus der Nahrung rekrutiert, d.h. ihnen im Gegensatz zu vielen anderen Boden- Invertebraten eine spezifische Darmflora fehlt. Es wurde deutlich, dass die mit dem gefresse- nen Boden aufgenommene mikrobielle Gemeinschaft während der Darmpassage signifikante Veränderungen ihrer relativen Zusammensetzung erfährt und dass die Unterschiede zwischen den mikrobiellen Gemeinschaften von Futter, Darm und Losung stark von der Diät der Re- genwürmer beeinflusst werden. Die hier präsentierten Ergebnisse zur Intestinalmikrobiologie von Scarabaeidenlarven stellen die ersten ihrer Art für Käferlarven und mit die ersten für andere Boden-Arthropoden als Termiten dar. Es konnte gezeigt werden, dass sich die ausgeprägten Unterschiede physiko- chemischer Parameter (pH-Wert, Redoxpotential, Fettsäurespektren), die zwischen den Haupt-Darmabschnitten (Mittel- und Enddarm) der Larven herrschen, in einer deutlich unter- IV Zusammenfassung schiedlichen Besiedlung mit Mikroorganismen widerspiegeln. Im Gegensatz zu den unter- suchten Regenwürmern ist die Darmmikrobiota der Scarabaeidenlarven als spezifische Darm- flora anzusehen, da sie deutlich verschieden zur Mikrobiota der aufgenommenen Nahrung war. Bei beiden Larven war der Mitteldarmabschnitt weniger dicht besiedelt als der als Gär- kammer angesehene Enddarm. Die Methanogenese war stets auf den Enddarm beschränkt; bei den Maikäferlarven wurden Methanobrevibacter-Arten, bei den Rosenkäferlarven zusätzlich Methanomicrococcus-Arten als verantwortliche Methanogene identifiziert. Im Vergleich zu den Bacteria war aber sowohl die Diversität
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