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Cdv-based cell division and cell cycle organization in the thaumarchaeon Nitrosopumilus maritimus
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
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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.

Place, publisher, year, edition, pages
2011. Vol. 82, no 3, 555-566 p.
National Category
URN: urn:nbn:se:uu:diva-162884DOI: 10.1111/j.1365-2958.2011.07834.xISI: 000297282200004PubMedID: 21923770OAI: oai:DiVA.org:uu-162884DiVA: diva2:461883
Available from: 2011-12-05 Created: 2011-12-05 Last updated: 2012-01-11Bibliographically approved
In thesis
1. Unique Solutions to Universal Problems: Studies of the Archaeal Cell
Open this publication in new window or tab >>Unique Solutions to Universal Problems: Studies of the Archaeal Cell
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.
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 888
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
urn:nbn:se:uu:diva-162886 (URN)978-91-554-8244-2 (ISBN)
Public defence
2012-02-03, C4:301, Biomedicinskt Centrum, Husargatan 3; BMC, Uppsala, 13:15 (English)
Available from: 2012-01-10 Created: 2011-12-05 Last updated: 2012-01-16

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