Mobilization of sulfur by green sulfur bacteria – Physiological and molecular studies on Chlorobaculum parvum DSM 263
DISSERTATION Zur Erlangung des Grades eines Doktors der Naturwissenschaften Dr. rer. nat.
Fachbereich Biologie / Chemie der Universität Bremen
vorgelegt von
Clelia Donà
Bremen, Mai 2011
Mobilization of sulfur by green sulfur bacteria – Physiological and molecular studies on Chlorobaculum parvum DSM 263
Clelia Donà
Bremen, May 2011
A thesis submitted in partial fulfilment
of the requirements for the degree of
Doctor of Philosophy in Natural Sciences
Dr. rer. nat. –
Faculty of Biology and Chemistry
University of Bremen, Germany
RR
Datum des Promotionskolloquiums: 07/07/2011
1. Gutachter: Prof. Dr. Ulrich Fischer 2. Gutachter: Dr. Timothy Ferdelman
1. Prüfer: Prof. Dr. Barbara Reinhold-Hurek 2. Prüfer: Prof. Dr. Friedrich Widdel
RR TABLE OF CONTENTS
ABSTRACT ...... 5
ZUSAMMENFASSUNG ...... 6
Chapter 1: GENERAL INTRODUCTION ...... 8 1.1 Green Sulfur Bacteria: photosynthesis and oxidation of sulfur compounds ...... 10 1.2 The sulfur cycle ...... 29 1.3 Focus of the PhD work ...... 32 1.4 Bibliography of Chapter 1 ...... 35
Chapter 2: THIOSULFATE OXIDATION BY THE GREEN SULFUR BACTERIUM CHLOROBACULUM PARVUM DSM 263 – The Sox system studied in vivo ...... 47
Chapter 3: ELEMENTAL SULFUR MOBILIZATION BY THE GREEN SULFUR BACTERIUM CHLOROBACULUM PARVUM DSM 263 ...... 75
Chapter 4: SULFUR OXIDATION BY THE GREEN SULFUR BACTERIUM CHLOROBACULUM PARVUM DSM 263 ...... 99
Chapter 5: CONCLUDING REMARKS ...... 109
RR ABSTRACT
Green sulfur bacteria are photolithotrophs that use inorganic sulfur compounds as electron donors for photosynthesis. Elemental, solid sulfur is one of the electron donors used. Sulfur is produced by green sulfur bacteria during the oxidation of sulfide to sulfate, and during the oxidation of thiosulfate to sulfur and sulfate. Green sulfur bacteria have been known for long, and the genomes of 12 strains have been sequenced. Yet, it is not clear how green sulfur bacteria can access elemental sulfur, which is practically insoluble at the temperatures at which most of them grow. The present work has been done using pure cultures of the mesophilic strain Chlorobaculum parvum DSM 263. By studying the dynamics of inorganic sulfur compounds in growing cultures of Cla. parvum DSM 263, it was shown that the sulfur produced during thiosulfate oxidative disproportionation can be either oxidized immediately to sulfate, or released outside the cells. Extracellular sulfur oxidation needs a dedicated system, which is not synthesised in the presence of thiosulfate. Experiments conducted at low light intensities revealed that thiosulfate is not consumed exclusively via the Sox multienzymatic system, known thus far as the only thiosulfate oxidizing system present in green sulfur bacteria. It is not clear yet if this additional pathway for thiosulfate consumption allows strain DSM 263 to obtain electrons for thiosulfate, or if it is used by bacteria to consume the reducing power that cells might have in excess. Physiological studies conducted on Cla. parvum DSM 263 fed with sulfur furnished evidence that the oxidation of elemental sulfur to sulfate is accompanied by the formation of yet unidentified sulfur compound(s). Similarly to what commented for thiosulfate consumption, these compounds could be intermediates in the oxidation of sulfur to sulfate, or could be side products of sulfur consumption. Essential elements for the utilisation of elemental sulfur were shown to be present in the membranes of Cla. parvum DSM 263. Differential membrane proteomic studies were thus performed on cells of Cla. parvum DSM 263 grown on sulfur or on sulfide. Seven proteins were found to be overexpressed in sulfuric conditions, revealing that bacteria do possess different proteomic equipment for oxidizing the insoluble sulfur rather than the soluble sulfide. Identification of these overexpressed proteins and of their interaction partners will probably help revealing the cellular apparatus of extracellular solid sulfur mobilization.
R R ZUSAMMENFASSUNG
Grüne Schwefelbakterien bilden eine eigene Gruppe von photolithotrophen Bakterien, welche anorganische Schwefelverbindungen als Elektronenquelle für die Photosynthese nutzen. Elementarer Schwefel ist eine dieser Elektronenquellen. Er wird von Grünen Schwefelbakterien bei der Oxidation von Sulfid oder Thiosulfat zu Sulfat gebildet. Grüne Schwefelbakterien sind schon lange bekannt und vor kurzem wurde das Genom von 12 Stämmen sequenziert. Trotzdem ist es bisher nicht gelungen, zu verstehen, in welcher Form der elementare Schwefel zugänglich gemacht wird. Für die vorliegende Arbeit wurde der mesophile Stamm Chlorobaculum parvum DSM 263 verwendet. Die Untersuchung von anorganischen Schwefelverbindungen in wachsenden Cla. parvum DSM 263-Kulturen hat gezeigt, dass der durch Oxidation von Thiosulfat entstehende Elementarschwefel entweder sofort zu Sulfat umgewandelt oder aus der Zelle ausgeschieden wird. Um den elementaren Schwefel, welcher nicht sofort periplasmatisch zu Sulfat umgewandelt wird, oxidieren zu können, würde ein spezielles Schwefeloxidationssystem benötigt, dessen Synthese bisher nie in Gegenwart von Thiosulfat beobachtet wurde. Die Ergebnisse einiger bei niedrigen Lichtintensitäten durchgeführter Experimente lassen deshalb den Schluss zu, dass Thiosulfat nicht ausschließlich durch das Sox-Multienzymsystem verbraucht wird, welches bisher das einzige bekannte Thiosulfatoxidationssystem in Grünen Schwefelbakterien darstellt. Es ist bisher nicht nachgewiesen worden, dass dieser zweite Stoffwechselweg Stamm DSM 263 erlaubt, Elektronen von Thiosulfat zu gewinnen, oder ob er dazu dient Reduktionskraft abzubauen, welche ohnehin in der Zelle im Überfluss vorhanden ist. Physiologische Studien an auf Schwefel gewachsenem Chlorobaculum parvum DSM 263 untermauerten die Vermutung, dass während der Oxidation von elementarem Schwefel zu Sulfat ein oder mehrere nicht identifizierte Zwischenprodukte entstehen. Ähnliches wird auch für die Oxidation von Thiosulfat vermutet. Die entstehenden Substanzen könnten Zwischenprodukte der Oxidation von Schwefel zu Sulfat sein, sie könnten aber auch Nebenprodukte des Schwefelverbrauchs sein. Es konnte gezeigt werden, dass die essentiellen Elemente zur Verwendung von elementarem Schwefel auch in den Membranen von Cla. parvum DSM 263 vorhanden sind. Des Weiteren wurden differentielle Membran-proteomische Experimente an Zellen von Cla. parvum DSM 263 durchgeführt, welche auf Schwefel oder Sulfid gewachsen waren. Es konnte nachgewiesen werden, dass in Umgebung von elementarem Schwefel sieben Proteine überexprimiert wurden. Dieses Ergebnis lässt den Schluss zu, dass die Bakterien unterschiedliche proteomische Ausstattungen R R besitzen, um eher den unlöslichen Schwefel als das lösliche Sulfid zu oxidieren. Die Identifizierung dieser überexprimierten Proteine und ihrer Interaktionspartner wird vermutlich dazu beitragen können, den zellulären Mechanismus aufzuklären, welcher für die Mobilisierung von extrazellulärem ungelöstem Schwefel verantwortlich ist.
R R – Chapter 1 –
GENERAL INTRODUCTION
Green sulfur bacteria (Chlorobi) are primary producers that use light energy to fix carbon dioxide into biomass. They also play a role in the sulfur cycle, oxidizing a variety of reduced sulfur compounds (sulfide, thisoulfate, sulfur) to sulfur or sulfate (Fig. 1). Chlorobi are restricted to anoxic environments where light, carbon dioxide, and reduced sulfur compounds are present. They are present in microbial mats, anoxic sediments, and anoxic water basins, where they might even become numerically preponderant – it is the case of the chemoclines of Black Sea and Lake Cadagno (Manske et al., 2005; Halm et al., 2009).
Fig. 1: Schematic representation of the metabolism of green sulfur bacteria, which reduce CO2 photosynthetically using inorganic sulfur compounds as electron donors. Chlorobaculum parvum DSM 263/NCIB 8327 is the model strain used in the present study.
However, even if not among the most diffused bacteria, green sulfur bacteria possess unique features that renders their metabolism particularly interesting for basic research: they can perform photosynthesis at extremely low light intensities, they possess unique cellular structures – the chlorosomes, and they can use a solid compound (sulfur, S8) as electron donor. The clade of green sulfur bacteria has been known for long: already in the 30s, green sulfur bacteria served as models for Van Niel’s formulation of the general equation of photosynthesis (Barker and Hungate, 1990). They have been studied extensively again in the 80s using biochemical methods (Fischer 1984; Steinmetz and Fischer, 1982 and 1985), and recently by genome analysis (Eisen et al, 2002; works by Bryant, Frigaard, and Hanson). However, part of their sulfur metabolism is still elusive (Fig. 2). R R
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