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From Multi-Omics to Single Function in Hyperthermophilic Archaeon Sulfolobus Solfataricus

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From Multi-Omics to Single Function in Hyperthermophilic Archaeon Sulfolobus Solfataricus Zooming in: from multi-omics to single function in hyperthermophilic archaeon Sulfolobus solfataricus Pawel Sierocinski Thesis committee Promotor Prof. Dr J. van der Oost Personal chair at the Laboratory of Microbiology Co-promotor Prof. Dr W. de Vos Distinguished Professor Microbiology Other members Prof. Dr W van Berkel Wageningen University & Research Dr SJJ Brouns UHD Delft University of Technology Dr D Swarts UD Wageningen University & Research Dr Nico Claassens, PostDoc Max Planck Institute of Molecular Plant Physiology, Potsdam The research was conducted under the auspices of the Graduate School VLAG ( Advanced studies in Food Technology, Agrobiotechnology, Nutrition and Health Sciences). Zooming in: from multi-omics to single function in hyperthermophilic archaeon Sulfolobus solfataricus Pawel Sierocinski Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Monday 26th August 2019 at 11 a.m. in the Aula Pawel Sierocinski Zooming in: from multi-omics to single function in hyperthermophilic archaeon Sulfolobus solfataricus, 210 pages PhD thesis, Wageningen University, Wageningen, the Netherlands (2017) With references, with summary in English ISBN 978-94-6343-974-9 DOI https://doi.org/10.18174/476997 Table of contents Chapter 1: Introduction and Outlook 6 Chapter 2: Hot Transcriptomics 19 Chapter 3: “Hot standards” for the thermoacidophilic archaeon Sulfolobus solfataricus 46 Chapter 4: Quantitative Proteomic Analysis of Sulfolobus solfataricus Membrane Proteins 108 Chapter 5: Temperature promoter motif regulates gene expression in S. solfataricus 132 Chapter 6: Evolution of S. solfataricus in fluctuating temperature Conditions 148 Chapter 7: Summary, discussion and general conclusions 159 Appendices 179 References 180 About the author 203 Acknowledgements 204 List of publications 207 Overview of completed training activities 208 Hot Transcriptomics 6 Chapter 1 Introduction and Outlook Pawel Sierocinski Till the 1960s life as we knew it occupied a comfortable niche that overlapped with the human temperature range. Even though the earliest reports of life at temperatures above 80°C were published back in 1897 (Davis 1897) they were generally discarded as artefacts. Temperatures reaching over 80°C were considered too high for any living creature to survive, let alone to thrive. In 1963 Kempner speculated, based on the analysis of hot springs in Yellowstone National Park that 73°C is the upper temperature limit for life (Kempner 1963). This paradigm shifted soon thereafter when Brock and Freeze managed to isolate and cultivate Thermus aquaticus, a bacterium with a temperature range from 40°C to 79°C (Brock & Freeze 1969). This opened the doors for further investigation of environments previously assumed hostile for life, resulting in the discovery of a great diversity of thermophiles and hyperthermophiles, both marine and terrestrial. Hyperthermophiles, defined as organisms that thrive at elevated temperatures with optimal growth at or above 80°C (Stetter 2006), occupy diverse sets of environments – from the submarine black smokers, though terrestrial and marine hot springs to high temperature compost heaps. This diversity of ecosystems allows for multiple life strategies. Hyperthermophiles include both aerobic and anaerobic life forms. Most are autotrophic, using hydrogen as the electron donor and a range of electron acceptors, including CO2, sulphur, and nitrate. Their autotrophy is not obligatory and a majority has been classified Hot Transcriptomics 7 as opportunistic heterotrophs capable of metabolising a wide range of organic compounds either by aerobic respiration or fermentation. One key feature that all the hyperthermophiles share is the presence of the reverse gyrase enzyme (Forterre et al. 1995). Although it can be occasionally found in regular thermophiles as well, it has never been observed in mesophiles. The reverse gyrase enzyme is present in bacterial hyperthermophiles but it is of archaeal origin, suggesting it was evolved in HT Archaea and subsequently transferred to HT Bacteria through a horizontal gene transfer event shortly after the two domains split. The enzyme is responsible for positive supercoiling of DNA and knock out strains of hyperthermophiles lacking it are viable, but thermosensitive (Atomi et al. 2004), most likely causing deficient strains to lose competition with the gyrase possessing organism in the hyperthermophilic conditions. Archaea Even though hyperthermophiles share multiple similarities, they span two groups separated by the oldest rift in phylogenetic history of life, i.e. the split between the Bacteria and the Archaea. Their similarities, from both morphological and physiological perspective, caused that initially they were all classified as bacteria. For example, Sulfolobus solfataricus, the subject of this thesis, has been initially classified as an atypical member of the genus Pseudomonas. It was only in 1977 when Carl Woese established a novel method of determining phylogeny that was based on similarities of conserved regions of the ribosomal genes (Woese & Fox 1977). His results suggested that, although morphologically identical, some microorganisms show a genetic divergence indicating an ancient split from the rest of the prokaryotes. Hot Transcriptomics 8 Initially it was the methanogens that did not fit in the prokaryotic puzzle, but soon after it turned out that the majority of thermophiles cluster closer to the methanogens than to bacteria. The idea did not catch quickly in the morphology dominated field of phylogenetics, but in 1990 it was proposed, again by Woese, that life should be reorganised into three domains (Woese et al. 1990) and since then this classification has become a new paradigm on how the life on earth has evolved, and should be organised. Archaea are distinct from the rest of the nucleus-free life not only due to their 16S RNA sequences. They have a unique composition of their cell membrane, consisting of ether-linked isoprenoid lipids (Kates 1977) a trait that allows them to thrive in environments where other microorganisms fail (Gliozzi et al. 2002). They are the only group of organisms that can perform metabolic processes that are key to the nutrient cycling on our planet. Main example is methanogenesis, a key process in anaerobic conditions that allows removal of acetate, CO2 and hydrogen thus protecting the microbial communities from accumulation of harmful by-products of fermentation. Annually 500 billion tons of methane are produced by methanogens making it a truly planetary scale process fully facilitated by Archaea (Conrad 2009). Archaea are also responsible for recently discovered processes of anaerobic methane oxidation (Raghoebarsing et al. 2006) and anaerobic ammonia oxidation (Schmidt et al. 2002) that play a key role in the stability of nutrient cycles of the planet. One of the most interesting features of Archaea is their DNA processing machinery. Even though they are similar to prokaryotes in terms of the metabolism, their processing of DNA resembles the one of eukaryotes. They have similar regulatory proteins and sequences, similar tRNA genes and, at Hot Transcriptomics 9 least in some cases, their replication starts, unlike bacterial one, from multiple origins of replication. This has led to Archaea becoming a model system for preliminary studies of eukaryote replication, transcription and translation, combining a relatively homologous mechanism and the ease of growing and manipulating the genetics in comparison with the eukaryotes. This similarity resulted with a novel concept of the origin of Eukaryotic cell as a fusion between an archaeon and a prokaryote, changing the tree of life into a ring- like structure (Rivera & Lake 2004). Archaea are also a key element of studying the origins of life on the planet, with multiple hypotheses suggesting that it might have required hot environments for the first cellular replicators to kick off. Archaea were originally divided into two major kingdoms: Euryarchaeota, containing halophilic Archaea, methanogens and some of the (hyper)thermophiles and Crenarchaeota, harbouring most of the known (hyper)thermo (acido)philes. This has been challenged by the more recent discoveries of multiple novel groups of Archaea, including Nanoarchaeota, Thaumarchaeota, Lokiarchaeota and Korarchaeota, which makes the current phylogeny of Archaea a work in progress (Huber et al. 2003; Brochier- Armanet et al. 2008; Petitjean et al. 2015; Spang et al. 2015). The new discoveries, greatly facilitated by the cheaper sequencing technology, also put a dent in the long held belief that Archaea are mainly involved in the extreme environments. Archaeal sequences are ubiquitous in all the sampled environments, and make up a significant part of mesophilic strata. The initial abundance of extremophiles was probably an artefact; the extreme environments where Archaea are predominant were disproportionally sampled, while mesophilic Archaea were too rare to be readily discovered and cultivated. Yet since typical mesophilic environments are vastly bigger than Hot Transcriptomics 10 the extreme ones, a large diversity of Archaea from those environments still outnumbers the extremophiles. Thermophiles and Sulfolobus solfataricus That said, thermophiles are still one of the hallmarks of Archaea and are among the
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