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Co-Existence and Niche Differentiation of Sulfur Oxidizing Bacteria in Marine Environments

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Co-Existence and Niche Differentiation of Sulfur Oxidizing Bacteria in Marine Environments Co-existence and niche differentiation of sulfur oxidizing bacteria in marine environments Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften - Dr. rer. nat. - dem Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von Petra Pjevac Bremen März 2014 Die vorliegende Arbeit wurde in der Zeit von April 2011 bis März 2014 in der Abteilung für Molekulare Ökologie am Max-Planck-Institut für Marine Mikrobiologie in Bremen angefertigt. 1. Gutachter: Prof. Dr. Rudolf Amann 2. Gutachter: Dr. Timothy G. Ferdelman Tag des Promotionskolloquiums: 09. Mai 2014 ‘A philosopher is a person who knows less and less about more and more, until he knows nothing about everything. A scientist is a person who knows more and more about less and less, until he knows everything about nothing.’ John M. Ziman Table of contents Summary 3 Zusammenfassung 4 List of abbreviations 6 I Introduction 7 1.1 The sulfur cycle 8 1.1.1 Sulfur cycling in coastal sediments 10 1.1.2 Sulfur cycling at hydrothermal vent and cold seep sites 12 1.1.3 Sulfur cycling in the water column 12 1.2 Sulfur-oxidizing prokaryotes 13 1.2.1 Phototrophic sulfur oxidation 13 1.2.1.1 Chlorobi – the GSB 15 1.2.1.2 Chromatiales – the PSB 16 1.2.2 Chemotrophic sulfur oxidation 17 1.2.2.1 Alphaproteobacteria 18 1.2.2.2 Betaproteobacteria 18 1.2.2.3 Gammaproteobacteria 19 1.2.2.4 Epsilonproteobacteria 20 1.2.2.5 Aquificae 22 1.2.2.6 Sulfolobales (sulfur-oxidizing Archaea) 22 1.3 Co-existence and niche differentiation of sulfur-oxidizing microorganisms 22 1.4 Exploration of sulfur oxidation and carbon assimilation pathways in sulfur oxidizing prokaryotes 24 1.4.1 Cultivation-based approaches 26 1.4.2 Molecular approaches 28 1.4.3 Stable- and radioisotope approaches 30 1.4 Thesis aims and motivation 32 II Microbial consumption of zero-valence sulfur in marine benthic habitats 35 1 III Community shift from phototrophic to chemotrophic sulfide oxidation during holomictic conditions in a shallow stratified sea-water lake 69 IV Microbial lipids reveal carbon assimilation patterns on hydrothermal sulfide chimneys 119 V Identification and activity of acetate-assimilating microorganisms in diffuse fluids venting from two hydrothermal systems 170 VI Sulfur-oxidizing Epsilonproteobacteria in S0-rich tidal pools 215 VII General Discussion and Outlook 221 7.1 General discussion 222 7.1.1 Epsilonproteobacteria and S0 – substrate specificity as niche differentiation mechanism among SOPs 222 7.1.2 Life in a sulfide gradient – the influence of sulfide concentration on niche differentiation among chemotrophic SOPs 224 7.1.3 Thiotrophy and carbon assimilation in hydrothermal environments 228 7.1.3.1 CO2 fixation by SOPs at hydrothermal vents 228 7.1.3.2 Organic carbon assimilation by SOPs at hydrothermal vents 230 7.2 Conclusion 231 7.3 Outlook 232 7.4 References 234 Acknowledgements 258 Appendix 259 2 Summary Reduced sulfur compounds and sulfur-oxidizing prokaryotes (SOP) are widely distributed in the marine environment. Diverse microbial lineages thrive on the oxidation of reduced sulfur. They co-exist successfully by the adaptive radiation into different physiological and ecological niches. However, the factors determining this differentiation and SOP distribution are largely unknown. Environmental factors, like pH, temperature and salinity, as well as the physiological capabilities of different SOPs for sulfur-oxidation and carbon assimilation likely govern the niche-differentiation. Therefore, as part of multiple collaborative studies, I studied the influence of substrate quality and availability on structuring sulfur-oxidizing microbial communities in different marine habitats. 0 First, the role of elemental sulfur (S ), in particular cyclooctasulfur (S8), as substrate for SOPs in marine benthic habitats was examined (Chapter II). We observed a specific association between Sulfurimonas/Sulfurovum-related Epsilonproteobacteria 0 and S /S8 regardless of the habitat. We propose that substrate quality effects SOP diversity and niche differentiation, and the capability to oxidize S8 probably provides a competitive advantage to the Sulfurimonas/Sulfurovum-group. Moreover, we investigated the diversity and distribution SOPs along gradients of a sulfide, oxygen and light in a highly sulfidic marine karst lake (Lake Rogoznica, Chapter III). The comprehensive analysis of microbial diversity revealed a community shift from phototrophic to chemotrophic sulfur oxidation during holomixis and tight coupling between sulfide and oxygen concentration and the sulfur-oxidizing microbial community in Lake Rogoznica. In two further studies, we explored different aspects of carbon assimilation in hydrothermally influenced habitats dominated by thiotrophic Sulfurimonas/Sulfurovum- related Epsilonproteobacteria. We demonstrated the effects of temperature and/or substrate flux on carbon-isotope fractionation during CO2 assimilation in environmental samples (Chapter IV). Furthermore, we showed that these and other hydrothermal vent associated thiotrophs do not incorporate acetate (Chapter V), despite their heterotrophic potential. Other microorganisms, not involved in oxidative sulfur cycling at hydrothermal vents, showed high activity and growth after the input of organic substrate. In summary, this thesis contributes to the general understanding of microbial ecology in sulfur-rich environments by provides novel insights into diversity and niche in sulfur-oxidizing microbial communities. 3 Zusammenfassung Reduzierte Schwefelverbindungen und schwefeloxidierende Prokaryoten (SOP) sind weit verbreitet in marinen Habitaten. Phylogenetisch diverse Mikroorganismen können Schwefel oxidieren. Sie koexistieren erfolgreich, da einzelne Gruppen verschiedenen physiologischen und ökologischen Nischen angepasst sind. Die Faktoren, die diese Differenzierung und die Verbreitung von SOP in marinen Habitaten ermöglichen, sind jedoch weitgehend unbekannt. Umweltfaktoren - wie pH-Wert, Temperatur und Salzgehalt - und die physiologischen Unterschiede zwischen verschiedenen SOP in Bezug auf Schwefeloxidation und Kohlenstoffassimilation beeinflussen wahrscheinlich die Nischendifferenzierung. Daher untersuchte ich im Rahmen mehrerer kollaborativere Studien den Einfluss von Schwefel Form und Verfügbarkeit auf die Diversität in Schwefeloxidierenden mikrobiellen Gemeinschaften in verschiedenen marinen Lebensräumen. Zuerst wurde die Rolle von elementarem Schwefel (S0), insbesondere Cyclooctaschwefel (S8), als Substrat für die SOP in bentischen Lebensräumen (Kapitel II) untersucht. Wir entdeckten eine spezifische, vom Lebensraum unabhängige Verknüpfung zwischen Epsilonproteobacterien aus der Sulfurimonas/Sulfurovum Gruppe 0 und S /S8. Die Form des Schwefelsubstrats scheint Auswirkungen auf die Diversität und Nischendifferenzierung von SOP zu haben. Die Fähigkeit, S8 zu oxidieren, stellt für die Sulfurimonas/Sulfurovum Gruppe einen Vorteil gegenüber anderen SOP da. Darüber hinaus untersuchten wir die Diversität von SOP entlang des Sulfid-, Sauerstoff und Lichtgradienten in einem hoch sulfidischen marinen See (Rogoznica See, Kapitel III). Die umfassende Analyse der mikrobiellen Diversität enthüllte den Umschwung von phototorpher zu chemotropher Schwefeloxidation während einer anoxischen Holomixis und die enge Verknüpfung von Sulfid und Sauerstoffkonzentration und der Komposition von Schwefeloxidierenden mikrobiellen Gemeinschaften in dem Rogoznica See. In zwei weiteren Studien untersuchten wir verschiedene Aspekte der Kohlenstoffassimilation in hydrothermal beeinflussten marinen Lebensräumen. Wir haben gezeigt, dass Temperatur und Substratverfügbarkeit eine Auswirkung auf die Isotopenfraktionierung von Kohlenstoff bei der CO2-Assimilation durch Epsilonproteobacterien der Sulfurimonas/Sulfurovum Gruppe haben (Kapitel IV). Weiterhin zeigten wir, dass diese und andere SOP in hydrothermal beeinflussten Fluiden kein Acetat zu assimilieren scheinen (Kapitel V). Stattdessen reagierten andere 4 Mikroorganismen, die nicht am oxidativen Schwefelkreislauf in Hydrothermalquellen beteiligt sind, mit erhöhter Aktivität und erhöhtem Wachstum auf die Zugabe des organischen Substrats. Diese Arbeit trägt zum allgemeinen Verständnis der mikrobiellen Ökologie in schwefelreiche marinen Habitaten bei, und bietet neue Einblicke zu Diversität und Nischendifferenzierung in Schwefeloxidierenden mikrobiellen Gemeinschaften. 5 List of abbreviations APS adenosine 5’-phosphosulfate reductase ATP adenosine triphosphate BChl bacteriochlorophyll CBB Calvin-Benson-Bassham cycle DMSO dimethyl sulfoxide DMSP dimethyl sulfoniopropionate FISH fluorescence in situ hybridization GNSB green non-sulfur bacteria GSB green sulfur bacteria IPL intact polar lipid MAR microautoradiography NADPH nicotinamide adenine dinucleotide phosphate PHA polyhydroxyalkanoate PNSB purple non-sulfur bacteria PSB purple sulfur bacteria rDSR reverse dissimilatory sulfite reductase system rRNA ribosomal RNA RSS reduced sulfur species rTCA reductive trycarboxylic acid cycle RubisCO ribulose 1,5-bisphosphate carboxylase/oxygenase SI stable isotope SIMS secondary ion mass spectrometry SIP stable isotope probing SOP sulfur-oxidizing prokaryote SOX thiosulfate-oxidizing multi-enzyme system 6 Chapter I Introduction Chapter I: Introduction 1.1 The sulfur cycle Sulfur is among the most abundant elements on Earth (McDonough and Sun, 1995). Besides its elemental form - pure or native sulfur (S0), it can occur is multiple positive and negative stable redox states and therefore reacts with a variety
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