Publikationsserver der Universitätsbibliothek Marburg
Titel:Evolution von Zwei-Komponenten-Systemen in Shewanella oneidensis MR-1. Die Histidinkinase ArcS und der Antwortregulator SO_4444,Zwei Komponenten, Zwei Modelle.
Autor:Lassak, Jürgen
Weitere Beteiligte: Buckel, Wolfgang (Prof. Dr.)
Veröffentlicht:2011
URI:https://archiv.ub.uni-marburg.de/diss/z2011/0053
DOI: https://doi.org/10.17192/z2011.0053
URN: urn:nbn:de:hebis:04-z2011-00536
DDC: Biowissenschaften, Biologie
Titel (trans.):Evolution of two component systems in Shewanella oneidensis MR-1
Publikationsdatum:2011-02-09
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
SO_0577, Evolution, Sauerstoff, Zwei-Komponenten-Systeme, Two component signal transduction, Evolution, Sauerstoff, Arc, Evolution, Arc, SO_0577, SO_0577, Zwei-Komponenten-Systeme, Arc

Zusammenfassung:
Die Eroberung neuer Lebensräume und die Anpassung an verschiedenste Umweltbedingungen können durch Organismen ein und derselben Familie erfolgen. Die entstehende Artenvielfalt resultiert primär nicht auf Grund von Veränderungen im genetischen Bauplan sondern vielmehr aus der Diversifikation der regulatorischen Signaltransduktionssysteme welche diesen Bauplan umsetzten. Unter diesen Systemen ist die Zwei-Komponenten-Signaltransduktion (TCS) von zentraler Bedeutung für die koordinierte Antwort auf umweltbedingte Veränderungen nicht nur in Bakterien sondern auch in Archaeen, Protisten und Pilzen. Prototypischerweise reagiert eine Rezeptorhistidinkinase auf ein extrazelluläres Signal und leitet dieses durch Transphosphorylierung auf einen zytoplasmatischen Antwortregulator weiter, welcher seinerseits als Transkriptionfaktor agiert. Dabei können orthologe Transkriptionsfaktoren für die Expression völlig unterschiedlicher Gene verantwortlich sein und es eröffnen sich Spielräume für die Anpassung an unterschiedlichste Umweltbedingungen. Shewanella Spezies sind Gram-negative, fakultativ anaerobe Alteromonaden. Die 48 bisher bekannten Arten haben nicht nur marine und limnische Habitate erobert, sondern man findet sie auch als Symbionten und Pathogene vor allem von Fischen. Die Besiedlung so unterschiedlicher ökologischer Nischen schlägt sich auch in der Diversität der Regulationssysteme nieder. So variieren allein die bekannten Zahlen von TCS-Proteinen innerhalb der Shewanellaceae von 67 in S. denitrificans OS217 bis 116 in S. sediminis HAW-EB3. Der Antwortregulator SO_4444 gehört dabei zu den TCS-Proteinen, die sich ausschließlich in einigen wenigen Shewanellen finden (S. baltica OS223 und S. oneidensis MR-1). Phylogenetische Untersuchungen des genetischen Kontextes von SO_4444 legen den Schluss nahe, dass der Antwortregulator zusammen mit einer Hybrid-Histidinkinase SO_4445 und weiteren fünf Genen durch lateralen Gentransfer aus Aermonas sp. aquiriert wurde. Deletionen und Insertionen in SO_4444 führen, verglichen mit dem Wildtyp, zu einer Beeinträchtigung der Biofilmbildung sowohl unter statischen Bedingungen als auch in einem hydrodynamischen Flusskammersystem. Eine Erhöhung des intrazellulären Levels an an zyklischem Guanosinmonophosphat (c-di-GMP) durch das Einbringen einer Guanylatzyklase aus Vibrio cholerae (VCA_0956) und die resultierende partielle Wiederherstellung des Wildtypphänotyps deuten auf eine Abhängigkeit des ∆SO_4444-Biofilmphänotyps von dem Signalmolekül. Darüber hinaus zeigen weitere Untersuchungen im genetischen Kontext von SO_4444 ebenso für die Hybrid-Histidinkinase SO_4445 einen deutlichen Einfluss auf den Biofilm. Interessanterweise unterscheidet sich dieser sowohl in Quantität und Morphologie. Zudem führt die Deletion beider Gene zu einem der Einzeldeletion ∆SO_4445 vergleichbaren Phänotyp. Damit lassen sowohl die differentiellen Phänotypen in ∆SO_4444 und ∆SO_4445, als auch das Verhalten des Doppel-Dletionsstamms keine offensichtlichen Schlüsse zu, ob oder wie die beiden Komponenten zusammenarbeiten. Jedoch zeigen unsere Untersuchungen deutlich, dass horizontaler Gentransfer von TCS-Elementen Einfluss auf ein bestehendes regulatorisches Netzwerk ausüben kann, und sich damit sowohl die Möglichkeit bietet das sensorische Potential eines Organismus zu erweitern als auch bestehende Regulationsmechanismen zu verfeinern oder neue zu etablieren. Im Gegensatz zu SO_4444 ist die Hybridsensorkinase ArcS (SO_0577) eine Autapomorphie aller Shewanellen und damit Bestandteil des Kernsatzes an TCS-Proteinen. Unsere Untersuchungen in S. oneidensis MR 1 konnten das Protein als korrespondierende Kinase zum Antwortregulator ArcA identifizieren. Die Anoxische Redoxkontrolle (Arc) regelt in Escherichia coli u.a. die Anpassung an einen wechselnden Sauerstoffgehalt in der Umwelt. Hierbei misst die Sensorkinase ArcB den Redox-Status des Chinon-Pools der Membran und leitet die Information über ein Phosphorelaissystem an ArcA weiter. Identifiziert man ein Pendant zum E. coli ArcA in Shewanella leicht durch eindeutige Sequenzähnlichkeiten (81% Sequenzidentität für S. oneidensis), so führt ein Abgleich von ArcB (E. coli) mit dem Shewanella Proteom zu keinem eindeutigen Ergebnis. Nur das Histidin-Phosphotransfer-Protein HptA zeigt signifikante Homologien zum C-Terminus von ArcB. Interessanterweise liegt hptA im gleichen genetischen Kontext wie das E. coli arcB. Diese Tatsache spricht entweder für Deletion oder Translokation des die Kinase kodierenden Genabschnitts. Phänotypische Vergleiche der Deletionstämme ΔarcS, ΔhptA und ΔarcA mit S. oneidensis Wildtyp offenbaren auffällige Übereinstimmungen der Mutanten bezogen auf Wachstum, Biofilmbildung und. Dabei zeigten zugehörige Doppel- und Tripple-Deletionen nie kumulative Effekte. Mehr noch in vitro Interaktionsstudien an aufgereinigten Proteinen zeigen Phosphotransfer zwischen ArcS, HptA und ArcA. Damit rekonstituiert sich das atypische Arc-der Shewanellaceae aus ArcS, HptA und ArcA. ArcS weicht in seiner modularen Struktur stark von der bekannter ArcB-Proteine ab und weist auch keinerlei signifikante Sequenzhomologien zu ArcB auf. Damit bildet ArcS einen phylogenetisch distinkten Arm von „ArcB“-Proteinen. Doch dieser auffälligen strukturellen und phylogenetischen Unterschiede zum Trotz ist es möglich, Deletionen in arcB (E. coli) und arcS und/oder hptA (S. oneidensis MR-1) zu kreuzkomplementieren. Zusammengefasst stützt dies die These einer Trunkierung der sensorischen Komponente ArcB und Rekrutierung der alternativen Sensorkinase ArcS als funktionalen Ersatz. Weiterführende in vitro und in vivo Untersuchungen an den katalytischen Resten ArcS-HKH731, ArcS-RecID1017 und ArcS-RecIID1162 deuten aber darauf hin, dass obwohl ArcS und ArcB funktional konvergieren, der Regulationsmechanismus fundamental unterscheidet. Vergleichende Analysen zwischen ArcB (E. coli)- und ArcS-Sensorik indizieren zudem eine Veränderung im Signalspektrum ebenso wie in der Signalaufnahme und Signalweiterleitung. Das Shewanella Arc-System steht damit ebenso beispielhaft wie der Antwortregulator SO_4444 für den evolutionären Wandel von TCS-Schaltkreisen, der es diesen Bakterien mit ermöglicht in verschiedenste Lebensräume vorzudringen und sich dort erfolgreich zu behaupten.

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