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Unique Solutions to Universal Problems: Studies of the Archaeal Cell
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. (Archaea Group)
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Archaea is one of the three domains of life and studies of archaeal biology are important for understanding of life in extreme environments, fundamental biogeochemical processes, the origin of life, the eukaryotic cell and their own, unique biology. This thesis presents four studies of the archaeal cell, using the extremophilic Sulfolobus and ocean living Nitrosopumilus as model systems.

Cell division in crenarchaea is shown to be carried out by a previously unknown system named Cdv (cell division). The system shares homology with the eukaryotic ESCRT-III system which is used for membrane reorganization during vesicle formation, viral release and cytokinesis. Organisms of the phylum Thaumarchaeota also use the Cdv system, despite also carrying genes for the euryarchaeal and bacterial cell division system FtsZ.

The thaumarchaeal cell cycle is demonstrated to be dominated by the prereplicative and replicative stage, in contrasts to the crenarchaeal cell cycle where the cell at the majority of the time resides in the postreplicative stage. The replication rate is remarkably low and closer to what is measured for eukaryotes than other archaea.

The gene organization of Sulfolobus is significantly associated with the three origins of replication. The surrounding regions are dense with genes of high importance for the organisms such as highly transcribed genes, genes with known function in fundamental cellular processes and conserved archaeal genes. The overall gene density is elevated and transposons are underrepresented.

The archaeal virus SIRV2 displays a lytic life style where the host cell at the final stage of infection is disrupted for release of new virus particles. The remarkable pyramid-like structure VAP (virus associated pyramids), that is formed independently of the virus particle, is used for cell lysis.

The research presented in this thesis describes unique features of the archaeal cell and influences our understanding of the entire tree of life.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2012. , 72 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 888
Keyword [en]
Archaea, Cdv, Cell cycle, Cell division, Cell lysis, Crenarchaea, ESCRT-III, Flow cytometry, Microarray, Microscopy, Nitrosopumilus, SIRV2, Sulfolobus, Thaumarchaea, Transcription, VAP, Virus
National Category
Microbiology Cell Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
URN: urn:nbn:se:uu:diva-162886ISBN: 978-91-554-8244-2 (print)OAI: oai:DiVA.org:uu-162886DiVA: diva2:464718
Public defence
2012-02-03, C4:301, Biomedicinskt Centrum, Husargatan 3; BMC, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2012-01-10 Created: 2011-12-05 Last updated: 2012-01-16
List of papers
1. A unique cell division machinery in the Archaea
Open this publication in new window or tab >>A unique cell division machinery in the Archaea
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2008 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 105, no 48, 18942-18946 p.Article in journal (Refereed) Published
Abstract [en]

In contrast to the cell division machineries of bacteria, euryarchaea, and eukaryotes, no division components have been identified in the second main archaeal phylum, Crenarchaeota. Here, we demonstrate that a three-gene operon, cdv, in the crenarchaeon Sulfolobus acidocaldarius, forms part of a unique cell division machinery. The operon is induced at the onset of genome segregation and division, and the Cdv proteins then polymerize between segregating nucleoids and persist throughout cell division, forming a successively smaller structure during constriction. The cdv operon is dramatically down-regulated after UV irradiation, indicating division inhibition in response to DNA damage, reminiscent of eukaryotic checkpoint systems. The cdv genes exhibit a complementary phylogenetic range relative to FtsZ-based archaeal division systems such that, in most archaeal lineages, either one or the other system is present. Two of the Cdv proteins, CdvB and CdvC, display homology to components of the eukaryotic ESCRT-III sorting complex involved in budding of luminal vesicles and HIV-1 virion release, suggesting mechanistic similarities and a common evolutionary origin.

Keyword
cdv, Crenarchaeota, cytokinesis, ftsZ, Sulfolobus
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-106988 (URN)10.1073/pnas.0809467105 (DOI)000261489100060 ()
Available from: 2009-07-15 Created: 2009-07-15 Last updated: 2012-01-11Bibliographically approved
2. A unique virus release mechanism in the Archaea
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2009 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 106, no 27, 11306-11311 p.Article in journal (Refereed) Published
Abstract [en]

Little is known about the infection cycles of viruses infecting cells from Archaea, the third domain of life. Here, we demonstrate that the virions of the archaeal Sulfolobus islandicus rod-shaped virus 2 (SIRV2) are released from the host cell through a mechanism, involving the formation of specific cellular structures. Large pyramidal virus-induced protrusions transect the cell envelope at several positions, rupturing the S-layer; they eventually open out, thus creating large apertures through which virions escape the cell. We also demonstrate that massive degradation of the host chromosomes occurs because of virus infection, and that virion assembly occurs in the cytoplasm. Furthermore, intracellular viral DNA is visualized by flow cytometry. The results show that SIRV2 is a lytic virus, and that the host cell dies as a consequence of elaborated mechanisms orchestrated by the virus. The generation of specific cellular structures for a distinct step of virus life cycle is known in eukaryal virus-host systems but is unprecedented in cells from other domains.

Keyword
lysis, virus factory, hyperthermophile, infection cycle
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-128369 (URN)10.1073/pnas.0901238106 (DOI)000267796100079 ()
Available from: 2010-07-22 Created: 2010-07-20 Last updated: 2017-12-12Bibliographically approved
3. Cdv-based cell division and cell cycle organization in the thaumarchaeon Nitrosopumilus maritimus
Open this publication in new window or tab >>Cdv-based cell division and cell cycle organization in the thaumarchaeon Nitrosopumilus maritimus
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2011 (English)In: Molecular Microbiology, ISSN 0950-382X, E-ISSN 1365-2958, Vol. 82, no 3, 555-566 p.Article in journal (Refereed) Published
Abstract [en]

Cell division is mediated by different mechanisms in different evolutionary lineages. While bacteria and euryarchaea utilize an FtsZ-based mechanism, most crenarchaea divide using the Cdv system, related to the eukaryotic ESCRT-III machinery. Intriguingly, thaumarchaeal genomes encode both FtsZ and Cdv protein homologues, raising the question of their division mode. Here, we provide evidence indicating that Cdv is the primary division system in the thaumarchaeon Nitrosopumilus maritimus. We also show that the cell cycle is differently organized as compared to hyperthermophilic crenarchaea, with a longer pre-replication phase and a shorter post-replication stage. In particular, the time required for chromosome replication is remarkably extensive, 15-18 h, indicating a low replication rate. Further, replication did not continue to termination in a significant fraction of N. maritimus cell populations following substrate depletion. Both the low replication speed and the propensity for replication arrest are likely to represent adaptations to extremely oligotrophic environments. The results demonstrate that thaumarchaea, crenarchaea and euryarchaea display differences not only regarding phylogenetic affiliations and gene content, but also in fundamental cellular and physiological characteristics. The findings also have implications for evolutionary issues concerning the last archaeal common ancestor and the relationship between archaea and eukaryotes.

National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-162884 (URN)10.1111/j.1365-2958.2011.07834.x (DOI)000297282200004 ()21923770 (PubMedID)
Available from: 2011-12-05 Created: 2011-12-05 Last updated: 2017-12-08Bibliographically approved
4. Replication-biased genome organisation in the crenarchaeon Sulfolobus
Open this publication in new window or tab >>Replication-biased genome organisation in the crenarchaeon Sulfolobus
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2010 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 11, 454- p.Article in journal (Refereed) Published
Abstract [en]

Background: Species of the crenarchaeon Sulfolobus harbour three replication origins in their single circular chromosome that are synchronously initiated during replication. Results: We demonstrate that global gene expression in two Sulfolobus species is highly biased, such that early replicating genome regions are more highly expressed at all three origins. The bias by far exceeds what would be anticipated by gene dosage effects alone. In addition, early replicating regions are denser in archaeal core genes (enriched in essential functions), display lower intergenic distances, and are devoid of mobile genetic elements. Conclusion: The strong replication-biased structuring of the Sulfolobus chromosome implies that the multiple replication origins serve purposes other than simply shortening the time required for replication. The higher-level chromosomal organisation could be of importance for minimizing the impact of DNA damage, and may also be linked to transcriptional regulation.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-134173 (URN)10.1186/1471-2164-11-454 (DOI)000282787800003 ()
Available from: 2010-11-22 Created: 2010-11-22 Last updated: 2017-12-12Bibliographically approved

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