Research Collection. Analysis of Frankia populations by in situ hybridization with 23S rrna targeted oligonucleotide probes.
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1 Research Collection Doctoral Thesis Analysis of Frankia populations by in situ hybridization with 23S rrna targeted oligonucleotide probes Author(s): Zepp, Kornelia Publication Date: 1996 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 Diss. ETH No Analysis of Frankia populations by in situ hybridization with 238 rrna targeted oligonucleotide probes A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH for the degree of DOCTOR OF NATURAL SCIENCES presented by KORNELlA ZEPP Dipl, Biologin, University of Giessen (FRG) born December 14, 1964 in Neustadt a.d. Weinstrasse (FRG) accepted on the recommendation of Prof. Dr. Joseph Zeyer, examiner Prof. Dr. Jeffrey O. Dawson, co-examiner Dr. Dittmar Hahn, co-examiner 1996
3 Summary Zusammenfassung
4 2 Summary Summary The actinomycete Frankia can live in symbiosis with more than 200 woody plants and can be differentiated into host-infection groups. The symbiotic interaction between Frankia strains and actinorhizal plants leads to the tormatten of root nodules in which molecular nitrogen is assimilated. Up to now, however, the analysis of Frankia populations in root nodules has been hampered by the lack of a reliable methodology for the detection and identification of uncultured Frankia populations. Today, molecular biological techniques are available that have the potential to solve some of the problems encountered with the detection and identification of Frankia adequately. These techniques are based on nucleic acid hybridization reactions, which can be applied either ex situ, i.e. after the extraction of target molecules from the sampie, or in situ, l.e, by the whole cell hybridization technique. Reliable analysis of Frankia populatlons therefore requires specific probe/target systems and adequate detection protocols. A highly variable insertion, located in domain 1II of the 238 rrna, which is specific for gram-positive bacteria with a high DNA G+C content was evaluated as probe/target system for the specific detection of Frankia. Comparative sequence analysis of cloned insertions after PCR assisted sequence retrieval from representative Frankia strains confirmed the differentiation of these strains into host infection groups. The Casuarina and Elaeagnus host infection groups (groups 11 and VI) were characterized by no or only small sequence variation. The AInus host infection group could be separated into four subgroups, three containing typical nitrogen-fixing strains (groups lila, IIlb and IV) and a fourth one containing non-nitrogen-fixing strains (group I). The results of hybridization experiments with oligonucleotides as probes indicated a sufficient ratlo of variability and stability within this 238 rrna insertion to serve as target for subgroupspecific detection of Frankia within the AInus group. Uncultured Frankia populations in root nodules of AInus glutinosa could be characterized ex situ by these probes after PCR assisted sequence retrieval of the 238 rrna insertion and cloning into E. coli. A promising alternative to the ex situ analysis of Frankia populations in root nodules by methods based on rrna extraction or on DNA extraction followed by the polymerase chain reaction (PCR) was the whole cell hybridization technique. This technique is based on the microscopic detection of labeled probes hybridized to specific target sequences on rrna in fixed cells. Fluorescent, Cy3-labeled oligonucleotide probes enabled detection of filaments and vesicles without permeabilization of the cells whereas detection of spores required a previouspermeabilization with lysozyme. The signal intensity obtained on spores, however, remained quite low and their detection was not quantitative. Digoxigenin-Iabeled probes also allowed the detection of filaments, vesicles and spores of Frankia. However, for all cell types a previous
5 Summary 3 permeabilization with SOS/OTT and an additional incubation with lysozyme was necessary. The optimized permeabilization protocol allowed the analysis of Frankia populations in nodule homogenates of different alders (AInus glutinosa, A. incana, A. viridis and A. nepalensis) on subgroup-ievel by whole cell hybridization with oligonucleotide probes. The analysis revealed the presence of only one Frankia population in every nodule homogenate. Filaments and vesicles in nodules of the spore (-) type as weil as filaments, vesicles and spores in nodules of the spore (+) type always belonged to the same group. Populations in nodules of the spore (-) type were usually identified as Frankia population belonging to group IV of the AInus host infection group, with the exception of the Frankia population in nodules of A. nepalensis which belonged to group lila. Nodules of the spore (+) type contained Frankia populations either belonging to group lila or to group IV. The feasibility of using the 23S rrna insertion as a target was further demonstrated in studies on the fate of introduced Frankia strains into soil containing indigenous Frankia populations. This study clearly showed the applicability of the whole cell hybridization technique for the analysis of uncultured Frankia populations in nodule homogenates. For the first time, questions on the ecology of Frankia populations in root nodules could be addressed without the drawbacks of isolation or the biases concerned with per detection. However, up to now, the detection was only reliably achieved in enrichments of Frankia, l.e. in root nodules. Therefore, studies on the applicability of the whole cell hybridization technique will have to be expanded to allow a reliable analysis of Frankia populations in other environments, e.g. such as bulk soil.
6 4 Zusammenfassung Zusammenfassung Aktinomyceten der Familie Frankiaceae können mit über 200 Holzpflanzen Symbiosen eingehen. Diese Symbiosen führen zur Bildung von WurzelknöHchen, in denen Frankia molekularen Stickstoff binden kann. Die eindeutige Charakterisierung von Frankia Populationen in Wurzelknöllchen ist bisher nicht möglich gewesen, da zuverlässige Methoden zur Identifizierung von nicht-kultivierten Frankia Stämmen fehlten. In den letzten Jahren sind allerdings molekulargenetische Methoden zum Ex-situ und ln-sltu Nachweis nicht-kultivierter bakterieller Populationen entwickelt worden. Diese Methoden beruhen auf der Bindung von Gensonden ("probe") an Zielsequenzen ("target"), die spezifisch für die nachzuweisenden Mikroorganismen sind. Für die erfolgreiche Anwendung dieser Methoden (Hybridisierung) sind ein zuverlässiges "probe/target"-system und differenzierte Nachweisprotokolle Voraussetzung. Eine hochvariable Insertion der 23S rrna, die typisch für Aktinomyceten mit hohem DNA-(G+C)-Gehalt ist, wurde auf ihre Eignung als "probe/target"-system zur Bestimmung von nicht-kultivierten Frankia Populationen getestet. Die Insertion ausgewählter Frankia Referenzstämme wurde mithilfe der PCR amplifiziert und anschliessend kloniert. Vergleichende Sequenzanalyse der klonierten Insertionen bestätigte die Einteilung der untersuchten Frankia Stämme in Wirtsspezifitätsgruppen. Frankia Stämme mit Casuarina- bzw. Elaeagnus-Wirtsspezifität (Gruppen 11 und VI) wiesen nur sehr geringe Sequenzunterschiede innerhalb dieser Insertion auf. Die Stämme der Alnus-Wirtsspezifitätsgruppe konnten dagegen aufgrund grösserer Sequenzunterschiede in vier Gruppen unterteilt werden. Drei Gruppen umfassen stickstoff-bindende Frankia Stämme (Gruppen lila, IIlb und IV), während ausschliesslich nicht-stickstoffbindende Frankia Stämme die vierte Gruppe bilden (Gruppe I). Hybridisierungen, bei denen Oligonukleotide als Sonden eingesetzt wurden, ermöglichten die Unterscheidung zwischen den Untergruppen der zur Alnus Wirtsspezifitätsgruppe gehörenden Frankia Stämme. Diese Ergebnisse zeigten, dass innerhalb dieser Insertion genügend Sequenzunterschiede vorkommen um die Grundlage für ein zuverlässiges "probe/target"-system für Frankia zu bilden. Anschliessende Hybridiserungsversuche bestätigten dieses Ergebnis, da nichtkultivierte Frankia Populationen in Wurzelknöllchen eindeutig identifiziert werden konnten. Frankia Populationen konnten mithilfe von Ex-situ Techniken, nach der Extraktion von rrna oder DNA und nachfolgender PCR, identifiziert werden. Eine vielversprechende Alternative zu Ex-situ Nachweismethoden ist die ln-situ Ganz-Zell-Hybridisierung. Ganz-Zell-Hybridisierung beruht auf dem mikroskopischen Nachweis von Gensonden, die in fixiertem Zellmaterial an spezifische Zielsequenzen gebunden haben. Frankia Filamente und Vesikel konnten ohne Vorbehandlung mithilfe von fluoreszenten, Cy3 markierten, Sonden nachgewiesen werden. Sporen konnten erst nach einer
7 Zusammenfassung 5 Vorbehandlung mit Lysozym nachgewiesen werden. Trotz Vorbehandlung war die Signalintensität gering und eine Quantifizierung von Sporen nicht durchführbar. Die Hybridisierung mit digoxigenin-markierten Sonden war erst möglich, nachdem alle Zelltypen, d.h. Filamente, Vesikel und Sporen, zuerst mit SDS/DTT und danach mit Lysozym vorbehandelt wurden. Die Optimierung der Zellpermeabilisierung ermöglichte die tn-situ Analyse von Frankia Populationen in Wurzelknöllchen verschiedener Erlenarten (AInus glutinosa, A. tncene, A. viridis, and A. nepalensis). Diese Populationen konnten durch die Verwendung spezifischer Oligonukleotidsonden in die Untergruppen AInus-infizierender Frankia Stämme eingeordnet werden. Die untersuchten Wurzelknöllchen enthielten entweder nur Filamente und Vesikel (Sporen-minus-Typ) oder noch zusätzlich Sporen (Sporenplus-Typ), Die Population eines Knöllchens wurde jeweils von Frankia Stämmen einer Untergruppe gebildet. Populationen in Wurzelknöllchen des Sporen-minus-Typs gehörten immer zur Wirtsspezifitätsgruppe 111. Populationen in Wurzelknöllchen des Sporen-plus-Typs Hessen sich entweder der Gruppe IV oder der Gruppe lila zuordnen. Die Zuverlässigkeit des "probe/target" Systems wurde schliesslich in Untersuchungen bestätigt, bei denen das Dursetzungsvermögen eingebrachter Frankia Stämme bei der Knöllchenbildung an Erlen im Vergleich zu im Boden vorkommender Frankia Populationen bestimmt wurde. Das in dieser Arbeit vorgestellte Referenzsystem und die Nachweisbarkeit gebundener Sonden mithilfe der Ganz-Zell-Hybridisierung ermöglichen erstmals die Bearbeitung ökologischer Fragen zu Frankia Populationen in Wuzelknöllchen, ohne durch Nachteile der Ex-situ Techniken eingeschränkt zu sein. Bisher wurden alle Analysen mit Wurzelknöllchen durchgeführt, die eine natürliche Anreicherung von Frankia Populationen darstellen. Weitere Untersuchungen müssen sich daher auf den Nachweis von nicht-kultivierten Frankia Populationen auch in komplexeren Systemen, wie z.b. dem Boden, richten.
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