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Sulfur Oxidation State of The Molecular Ecology of Key Organisms in Sulfur and Carbon Cycling in Marine Sediments Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften - Dr. rer. nat. - Dem Fachbereich für Biologie und Chemie der Universität Bremen vorgelegt von Sabine Lenk Bremen, März 2011 Die vorliegende Arbeit wurde in der Zeit von Februar 2007 bis Dezember 2010 am Max-Planck-Institut für Marine Mikrobiologie in Bremen angefertigt. 1. Gutachter: Prof. Dr. Rudolf Amann 2. Gutachter: Dr. Heide Schulz-Vogt 1. Prüfer: Prof. Dr. Michael Friedrich 2. Prüfer: Dr. Marc Mußmann Tag des Promotionskolloquiums: 30.3.2011 Abstract The World’s oceans host a variety of sulfidic habitats. Yet, microorganisms oxidizing reduced inorganic sulfur compounds have mostly been studied at hydrothermal vents, in anoxic basins, conspicuous microbial mats and symbioses but rarely in coastal sediments. In this thesis sulfur-oxidizing prokaryotes (SOP) of a eutrophic intertidal sand flat in the German Wadden Sea were investigated by molecular techniques. The diversity, abundance and activity of SOP were analyzed in particular among the Gammaproteobacteria. Comparative sequence analysis of the 16S rRNA and three genes involved in sulfur oxidation revealed a high diversity of mainly gammaproteobacterial SOP. Most of them were closely related to thiotrophic symbionts, including those of the tubeworm genus Oligobrachia. A group of free-living relatives accounted for up to 4% of all cells (~1.3 × 108 cells ml-1). Consistent with a presumed chemolithoautotrophic utilization of inorganic sulfur compounds, these and 14 numerous other members of the Gammaproteobacteria incorporated CO2 as revealed by microautoradiography (MAR). The findings demonstrate that non-filamentous Gammaproteobacteria are important catalysts of sedimentary sulfur oxidation and contribute to CO2-fixation in coastal surface sediments. Similarly, Roseobacter clade bacteria (RCB) accounted for unexpectedly high abundances of up to 10% of all cells in surface sediments (~2.5 × 108 cells ml-1). A RCB-related genome fragment of 35 kb was recovered from a metagenomic fosmid library. It encoded genes of the SOX multienzyme system including the sulfur dehydogenase SoxCD, but also the complete rDSR pathway, a gene arrangement that is unique among SOP. Gene-targeted FISH confirmed the presence of the gene dsrA in sedimentary RCB enriched in anaerobic sulfidic medium. In addition, a novel gene, which encodes a putative dioxygenase, designated as dsrU, was identified in the rDSR pathway. Protocols were developed for application of MAR and nano-scale secondary ion mass spectroscopy (nanoSIMS) to marine sediment samples to follow assimilation of acetate in single cells. Members of the Gammaproteobacteria appeared to assimilate slightly more acetate than RCB, whereas sulfate-reducing bacteria showed no significant incorporation. Particularly the combination of flow cytometry and nanoSIMS proved to be powerful for up-scaling of the analysis of substrate uptake by sediment bacteria enabling an efficient, high-resolution profiling of single cells from complex microbial communities. Zusammenfassung Die Weltmeere umfassen ein Vielzahl sulfidischer Habitate. Mikroorganismen, welche reduzierte inorganische Schwefelverbindungen oxidieren, wurden bisher intensiv an Hydrothermalquellen, in anoxischen Becken, mikrobiellen Matten und Symbiosen erforscht, wenig aber in küstennahen Sedimenten. In dieser Studie wurden schwefeloxidierende Prokaryoten (SOP) einer eutrophen Sandwattfläche des deutschen Wattenmeeres mit molekularbiologischen Techniken untersucht. Es wurde deren Artenvielfalt, Anzahl und Aktivität analysiert. Ein Fokus lag auf der Gruppe der Gammaproteobacteria. Vergleichende Sequenzanalyse der 16S rRNA und dreier Gene der Schwefeloxidation zeigte eine hohe Diversität vorrangig gammaproteobakterieller SOP. Viele waren nahverwandt zu thiotrophen Symbionten, unter anderem zu jenen der Röhrenwurmgattung Oligobrachia. Eine Gruppe freilebender Verwandter umfasste bis zu 4% aller Zellen (~108 Zellen ml-1). Wie Mikroautoradiographie (MAR) zeigte, 14 inkorporierten diese und viele andere Gammaproteobakterien CO2, was auf eine chemolithoautrotrophe Nutzung inorganischer Schwefelverbindungen hindeutet. Die Resultate verdeutlichen, dass auch nicht-filamentöse Gammaproteobakterien wichtige Katalysatoren der sedimentären Schwefeloxidation sind und zur CO2-Fixierung in küstennahen Sedimenten beitragen. Bakterien der Roseobacter Gruppe (RCB) erreichten ebenso hohe Abundanzen von bis zu 10% aller Zellen im Oberflächensediment (~2.5 ×108 Zellen ml-1). Aus einer Metagenombank konnte ein 35 kb langes, RCB-verwandtes Genomfragment identifiziert werden. Jenes kodierte Gene des SOX Multienzymsystems mitsamt der Schwefeldehydrogenase SoxCD sowie des kompletten rDSR Stoffwechselwegs – eine für SOP einzigartige Genkonstellation. Eine Gen-spezifische FISH wies das Gen dsrA in RCB aus Sediment nach, welche anaerob in sulfidischem Medium angereichert wurden. Darüber hinaus wurde eine neues Gen im rDSR Stoffwechselweg entdeckt, das, vorläufig als dsrU bezeichnet, vermutlich eine Dioxygenase kodiert. Es wurden Protokolle zur Anwendung von Mikroautoradiographie und nano-skalierter Sekundärionenmassenspektrometrie (nanoSIMS) auf marine Sedimentproben entwickelt, um die Assimilation von Acetat in einzelnen Zellen zu verfolgen. Gammaproteobakterien assimilierten offenbar mehr Acetat als RCB, während sulfatreduzierende Bakterien keine signifikante Aufnahme zeigten. Die Kombination von Durchflußzytometrie and nanoSIMS erwies sich als besonders zielführend für eine Hochskalierung der Analyse der Substrataufnahme durch Zellen aus Sedimenten, da sie ein effizientes, hochauflösendes Screening von vielen Einzelzellen aus komplexen mikrobiellen Gemeinschaften ermöglicht. Contents 1. Introduction ................................................................................................................................................2 1.1 Role and Fate of Reduced Inorganic Sulfur Compounds in Coastal Sediment .....................................3 1.2. Sulfur-Oxidizing Prokaryotes ...............................................................................................................5 1.3. Molecular Approaches for Characterization of Uncultured SOP ..................................................... 11 1.4. Thiotrophic Carbon Assimilation and Carbon Mineralization in Coastal Sediments ........................ 14 1.5. Molecular Approaches to Study in situ Activities of Uncultured Microorganisms .......................... 17 1.6 The Wadden Sea – An UNESCO World Heritage Site ........................................................................ 18 1.7 Objectives of This Thesis ................................................................................................................... 22 References ............................................................................................................................................... 24 2. Sulfur-Oxidizing Gammaproteobacteria in Coastal Sediments ............................................................... 37 Summary .............................................................................................................................................. 38 Introduction ......................................................................................................................................... 39 Results ................................................................................................................................................. 40 Discussion ............................................................................................................................................ 51 Conclusion ........................................................................................................................................... 53 Experimental Procedures .................................................................................................................... 54 References ........................................................................................................................................... 59 Supporting Information ....................................................................................................................... 65 3. Sulfur-Oxidizing Roseobacter Clade Bacteria in Coastal Sediments ........................................................ 74 Summary .............................................................................................................................................. 75 Introduction ......................................................................................................................................... 76 Results ................................................................................................................................................. 77 Discussion ............................................................................................................................................ 86 Conclusion ........................................................................................................................................... 88 Experimental Procedures .................................................................................................................... 89 References ..........................................................................................................................................
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