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Exploring the Cell Cycle of Archaea

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Exploring the Cell Cycle of Archaea Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 300 Exploring the Cell Cycle of Archaea MAGNUS LUNDGREN ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 UPPSALA ISBN 978-91-554-6881-1 2007 urn:nbn:se:uu:diva-7848 ! " # ! $%%& '( ) * * * + , - . , #, $%%&, / / * 0 , 0 , '%%, & , , 123 4&!54 5))657!! 5 , 0 * * , 1 * . , * * , - * * , . 5 * , " * . * 8 * 5 , 2 . 0 . . , 2 * 0 9 . * 5 , 0 * . , . * * . . , 0 , /7 . . 0 , -. /7 * . * , : . . * , 0 * ; . * / , 0 . . , < ; . * , - . . . 8 * , 1 , ! " 0 / : # / #$ % $ & $ ' ( )* $ $ %+,-./ $ ! = # $%%& 122 7) 57$ 6 123 4&!54 5))657!! 5 ( ((( 5&!6! > (?? ,,? @ A ( ((( 5&!6!B List of papers This thesis is based on the following papers, which are referred to in the text by their roman numerals. I Robinson NP, Dionne I*, Lundgren M*, Marsh VL, Bernander R, Bell SD. Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell, 2004, 116:25-38. II Lundgren M*, Andersson A*, Chen L, Nilsson P, Bernander R. Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proceedings of the National Academy of Sciences USA, 2004, 101:7046-7051. III Majerník AI*, Lundgren M*, McDermott P, Bernander R, Chong JP. DNA content and nucleoid distribution in Methanothermobacter thermautotrophicus. Journal of Bacteriology, 2005, 187:1856-1858. IV Lundgren M, Bernander R. A genome-wide transcription map of an archaeal cell cycle. Proceedings of the National Academy of Sciences USA, 2007, 104:2939-2944 V Lundgren M, Malandrin L, Eriksson S, Huber H, Bernander R. Cell Cycle Characteristics of Crenarchaea: Unity among Diversity. Manuscript *These authors contributed equally Reprints were made with the permission of the publishers Papers by the author not included in this thesis 1. Lundgren M, Bernander R. Archaeal cell cycle progress. Current Opinion in Microbiology, 2005, 8:662-668. 2. Andersson AF, Lundgren M, Eriksson S, Rosenlund M, Bernander R, Nilsson P. Global analysis of mRNA stability in the archaeon Sulfolobus. Genome Biology, 2006, 7:R99 3. Brouns SJ, Walther J, Snijders AP, van de Werken HJ, Willemen HL, Worm P, de Vos MG, Andersson A, Lundgren M, Mazon HF, van den Heuvel RH, Nilsson P, Salmon L, de Vos WM, Wright PC, Bernander R, van der Oost J. Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment. Journal of Biological Chemistry, 2006, 281:27378-27388 Contents Introduction.....................................................................................................7 Focus of this study......................................................................................8 The domain Archaea.....................................................................................10 A brief history of archaea research...........................................................10 Archaeal evolution and diversity..............................................................11 The genus Sulfolobus ...............................................................................13 The cell cycle of Archaea .............................................................................15 General cell cycle features .......................................................................15 Replication ...............................................................................................16 Replication origins in the three domains .............................................16 Replication initiation ...........................................................................18 Replication elongation.........................................................................20 Replication termination .......................................................................24 Genome segregation.................................................................................25 Eukaryotic mitosis ...............................................................................25 Bacterial genome segregation..............................................................26 Archaeal genome segregation..............................................................27 Cell division .............................................................................................28 Eukaryotic cytokinesis.........................................................................28 Bacterial cell division ..........................................................................29 Archaeal cell division ..........................................................................30 Flow Cytometry ............................................................................................31 Principle of flow cytometry......................................................................31 Flow cytometry in cell cycle analysis ......................................................32 Microarray technology..................................................................................33 Principle of microarrays ...........................................................................33 Design of spotted microarrays..................................................................34 Cell cycle studies of the archaea...................................................................36 Physiological analysis of archaeal cell cycles (Paper III and V).............36 Cell cycle features of M. thermautotrophicus .....................................37 Conserved cell cycle characteristics in crenarchaea ............................39 Characterization of replication initiation in Sulfolobus (Paper I and II) ..41 Multiple replication origins in archaea ................................................41 Cdc6 binds to replication origins.........................................................42 Cell cycle specific expression and the different roles of the Cdc6 proteins ................................................................................................43 Comprehensive analysis of cell-cycle dependent transcription in Sulfolobus (Paper IV) ...............................................................................44 Synchronization method ......................................................................44 Cyclic expression.................................................................................45 Concluding discussion and ideas for the future........................................48 Svensk sammanfattning ................................................................................51 Acknowledgements.......................................................................................53 References.....................................................................................................55 Introduction Microorganisms are the foundation of life on Earth; they are present in every environment, from inside Antarctic ice and saline lakes like the Dead Sea to deep inside the Earth’s crust and the superheated anoxic water of hot vents at the bottom of the oceans. They have created, and are maintaining, the environment necessary for organisms like ourselves (Madigan et al., 1997). Our own intestines and skin are also full of microorganisms, vital to our health and well-being, and our bodies harbor a large amount of microbial cells, up to 10 times the number of human cells (Savage, 1977). The exploration of the microbial world is essential to understanding ourselves, our planet and all life upon it. The first microscope, built by Antoni van Leeuwenhoek in 1674, enabled us for the first time to study individual microbial cells, whose existence until then had only been speculated. In the mid 19th century, Louis Pasteur used cultivation methods to convincingly prove that microorganisms were abundant in nature and that they did not arise spontaneously. The study of microorganisms advanced further with the ability to grow microorganisms in pure culture, in particular on solid media, developed by Robert Koch. His work made it possible to separate microorganisms into species that could be studied individually in the same way as e.g. plants and animals. However, the small size and the low number of physiological characteristics of microorganisms limited the study of the microbial world. The study of microorganisms leaped forward with the onset of molecular biology in the 20th century. The identification of DNA, not protein, as the genetic material, was crucial. Avery, MacLeod and McCarty demonstrated that DNA was the “transforming principle”, endowing harmless bacteria with pathogenic capacity by exposing them to DNA from disease-causing bacteria (Avery et al., 1944). Later, Hershey and Chase proved that it was mainly DNA that was transferred to bacteria during phage infection (Hershey and Chase, 1952). In 1953, James Watson and Francis Crick solved the three- dimensional structure of the DNA polymer, using partly
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