Photosynthesis and Sulfur Oxidation in Microbial Mats

PHOTOSYNTHESIS AND SULFUR OXIDATION IN MICROBIAL MATS UNRAVELLING THE ROLE OF VERSATILE CYANOBACTERIA IN ANCIENT OCEAN ANALOGUES Dissertation Zur Erlangung des Grades eines Doktors der Naturwissenschaften Ͳ Dr. rer. nat. Ͳ dem Fachbereich Biologie der Universität Bremen Judith M. Klatt Bremen, August 2015 Die vorliegende Arbeit wurde am Max-Planck-Institut für Marine Mikrobiologie in Bremen angefertigt. 1. Gutachter: Prof Dr. Friedrich Widdel 2. Gutachter: Dr. Dirk de Beer 3. Gutachter: Prof. Dr. Michael Kühl Colloquium date: December 14, 2015 Content SUMMARY 1 ZUSAMMENFASSUNG 3 I. Introduction 1. PAST AND PRESENT PHOTOSYNTHESIS 9 1.1. Earth’s oxygenation – An overview 10 1.2. Modules involved in photosynthesis and their evolutionary origin 14 1.2.1. Photosynthesis – An overview ………………………………. 14 1.2.2. Light absorption and Light-Harvesting Antennas …..…........... 16 1.2.3. Electron transport ……………………………………………. 17 1.2.4. Electron donors ……………………………………………… 19 1.2.5. CO2 fixation …………………………………………………. 20 1.2.6. (No) Clues about the evolutionary origin ……………….…… 20 1.3. Microbial mats 22 1.3.1. Microbial mats as analogues of ancient ecosystems ……….. 22 1.3.2. Photosynthesis in microbial mats …………………………... 24 1.4. Motivation and Outline 28 1.5. References 30 II. Manuscripts Overview of Chapters 39 2. STRUCTURE AND FUNCTION OF NATURAL SULPHIDE OXIDIZING MICROBIAL MATS UNDER DYNAMIC INPUT OF LIGHT AND CHEMICAL ENERGY 41 3. ASSESSMENT OF THE STOICHIOMETRY AND EFFICIENCY OF CO2 FIXATION COUPLED TO REDUCED SULFUR OXIDATION 85 4. HYDROGEN SULFIDE CAN INHIBIT AND ENHANCE OXYGENIC PHOTOSYNTHESIS IN A CYANOBACTERIUM FROM SULFIDIC SPRINGS 145 5. ANOXYGENIC PHOTOSYNTHESIS AND 2-METHYL HOPANOID PRODUCTION: AMODEL CYANOBACTERIUM ISOLATED FROM A PROTEROZOIC OCEAN ANALOG 173 6. ANOXYGENIC PHOTOSYNTHESIS CONTROLS OXYGENIC PHOTOSYNTHESIS IN A CYANOBACTERIUM FROM A SULFIDIC SPRING 215 7. REGULATION OF THE PARTITIONING BETWEEN OXYGENIC AND ANOXYGENIC PHOTOSYNTHESIS IN A CYANOBACTERIUM DOMINATING SULFIDIC SPRING MICROBIAL MATS 253 III. Perspectives 8. DISCUSSION 271 8.1. The advantage of photosynthetic versatility 272 8.1.1. “Detoxification” hypothesis ………………………………. 272 8.1.2. “Energetics” hypothesis ……………………………………. 273 8.1.3. “Direct competition” hypothesis …………………………… 275 8.1.4. “Modulation” hypothesis …………………………………… 275 8.2. Specific adaptations strategies among cyanobacteria to sulfidic conditions 288 8.2.1. Effects of H2S on cyanobacterial photosynthesis – an overview ……………………………………………… 289 8.2.2. Specific adaptation strategies and their advantage in the environment ……………………………...…………. 292 8.3. Implications 297 8.3.1. Stromatolites and oxygenic photosynthesis? ……………….. 297 8.3.2. The importance of sulfur oxidation intermediates in the Proterozoic C-, S- and O-cycle ……………………… 298 8.4. Outlook 299 8.5. References 301 IV.Contributed work HYPERSPECTRAL IMAGING OF BIOFILM GROWTH DYNAMICS 304 SPATIAL PATTERNS AND LINKS BETWEEN MICROBIAL COMMUNITY COMPOSITION AND FUNCTION IN CYANOBACTERIAL MATS 305 EFFECT OF HIGH ELECTRON DONOR SUPPLY ON DISSIMILATORY NITRATE REDUCTION PATHWAYS IN A BIOREACTOR FOR NITRATE REMOVAL 306 LOW-LIGHT ANOXYGENIC PHOTOSYNTHESIS AND Fe-S-BIOGEOCHEMISTRY IN A MICROBIAL MAT 307 Acknowledgements 308 SUMMARY The capability to perform oxygenic photosynthesis likely evolved in a cyanobacterial ancestor, probably in microbial mats. The cyanobacterial photosynthetic repertoire is not limited to oxygenic photosynthesis. In fact some specialized cyanobacteria can switch to using H2S as an electron donor instead of H2O in a process termed anoxygenic photosynthesis. Such photosynthetic versatility of cyanobacteria might have been an important adaptation strategy to sulfidic conditions in ancient microbial mats. Furthermore, cyanobacterial anoxygenic photosynthesis might have contributed to sustaining ocean euxinia in Proterozoic oceans. Therefore, studying the activity of modern day sulfide-adapted cyanobacteria and the competitiveness of oxygenic with anoxygenic photosynthesis has broad implications. The aim of this thesis was to gain insights into the activity of sulfide-adapted cyanobacteria in microbial mats that represent ancient Earth analogues. In Chapter 2 we describe the interaction between photosynthetically versatile cyanobacteria and chemolithoautotrophic sulphide oxidizing microorganisms in such an analogue system; the Frasassi sulphidic spring microbial mats. Dependent on the availability of O2 in the water column, two distinct end members of mat structure form; one type with cyanobacteria on top of chemolithotrophs and another type with an inverted structure, which we studied in situ using microsensors. To be able to evaluate the importance of the magnitude of the available and conserved energy for mat stratification, a theoretical background knowledge describing the energy conservation efficiency of sulfur-chemolithoautotrophs was needed, the derivation of which is described in Chapter 3. This showed that mats driven by chemosynthesis conserved substantially less energy than photosynthesis-driven mats, although similar amounts of light and chemical energy were available. The ecosystem does therefore not necessarily develop towards optimal energy usage and the dynamics of energy availability are more important for mat stratification and function than the mere magnitude. During the studies described in Chapter 2, it became apparent that obligate anoxygenic phototrophs are almost entirely absent in the Frasassi sulfidic spring mats. To elucidate the selective advantage of sulfide-adapted cyanobacteria, several physiological studies with cyanobacterial isolates were performed in Chapter 4, 5 and 6. In Chapter 7 similar studies were done on natural mats. In all Chapters we studied the combinatory effect of H2S and light on oxygenic photosynthesis and, if present, on anoxygenic photosynthesis. The study of cyanobacteria isolated from mats is challenging because classical approaches in microbiology, such as growth in a bioreactor, are not always suitable. Benthic 1 cyanobacteria tend to form biofilms, which creates physico-chemical microenvironments. We therefore developed a microsensor-based incubation system, which enabled us to simulate the steep and fluctuating gradients of light, sulfide and O2 occuring in the cyanobacterias’ natural environment (Chapter 4 and 5). In Chapter 4 the activity of an obligately oxygenic phototrophic cyanobacterium isolated from the Frasassi sulfdic springs was studied in the novel setup. We found several stimulatory or inhibitory effects of H2S on its photosynthetic activity. To get insights into the possible mechanisms causing these effects, we developed a model of the photosynthetic redox reactions, which also helped understanding how an obligate oxygenic phototrophic bacterium is so well adapted to diurnally fluctuating light and H2S concentrations. In Chapter 5 similar studies were performed on a cyanobacterium isolated from the Little Salt Spring mats, another ancient Earth analogue. We showed that the cyanobacterium performs both oxygenic and anoxygenic photosynthesis. Dependent on light intensity rates of anoxygenic photosynthetic CO2 fixation were up to twice as high as rates during oxygenic photosynthesis. The two photosynthetic modes were, however, never performed simultaneously. In contrast, Chapter 6, a bioreactor-based study of another cyanobacterial strain obtained from the Frasassi sulfidic springs, showed an elegant transition between oxygenic and anoxygenic photosynthesis, which we explain based on a simple kinetic regulation mechanism controlled by the affinity to H2S. Similar observations were made in Chapter 7, a study of natural mats dominated by a single cyanobacterial morphotype sampled from the Frasassi sulphidic springs. The very high apparent affinity to H2S allows for simultaneous oxygenic and anoxygenic photosynthesis over an astonishingly wide range of H2S concentrations and irradiances. Overall, this thesis highlights the wide spectrum of adaptations to sulfidic conditions among cyanobacteria. A crucial factor determining success in the environment is the specific effect of the local dynamics of light and H2S on activity. The most successful cyanobacteria ancient Earth analogues are photosynthetically versatile. As exposure to sulphidic conditions is like a red line through the history of cyanobacteria, it seems intuitive that cyanobacterial anoxygenic photosynthesis might be an ancient trait. However, there is currently no robust evidence supporting this hypothesis. This thesis highlights that photosynthetically versatile cyanobacteria might, however, have had an important impact on the ancient biogeochemical cycling. Deeper knowledge concerning the timeline of the emergence of anoxygenic photosynthesis among cyanobacteria has the potential to explain major shifts on the global oxygen budgets and redox state of Earth through history. 2 ZUSAMMENFASSUNG Der evolutive Ursprung oxygener Photosynthese, und damit der einzigen natürlichen Quelle Sauerstoffs unseres Planeten, liegt wahrscheinlich in einem Vorfahren der heutigen Cyanobakterien. Ausgehend von mikrobiellen Matten begann der Siegeszug dieses Prozesses in Form der Cyanobakterien, der die Entwicklung unseres Planeten maßgeblich geprägt hat. Nebst der einzigartigen Fähigkeit H2O als Electronendonor zu verwenden, sind bestimmte spezialisierte Cyanobakterien zusätzlich zur photosynthetischen H2S-Oxidation, einer Form der anoxygenen Photosynthese, befähigt. Diese Vielseitigkeit könnte eine wichtige Rolle in der

Load more