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Group I Introns and Homing Endonucleases in T-even-like Bacteriophages
Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Homing endonucleases are rare-cutting enzymes that cleave DNA at a site near their own location, preferentially in alleles lacking the homing endonuclease gene (HEG). By cleaving HEG-less alleles the homing endonuclease can mediate the transfer of its own gene to the cleaved site via a process called homing, involving double strand break repair. Via homing, HEGs are efficiently transferred into new genomes when horizontal exchange of DNA occurs between organisms.

Group I introns are intervening sequences that can catalyse their own excision from the unprocessed transcript without the need of any proteins. They are widespread, occurring both in eukaryotes and prokaryotes and in their viruses. Many group I introns encode a HEG within them that confers mobility also to the intron and mediates the combined transfer of the intron/HEG to intronless alleles via homing.

Bacteriophage T4 contains three such group I introns and at least 12 freestanding HEGs in its genome. The majority of phages besides T4 do not contain any introns, and freestanding HEGs are also scarcely represented among other phages.

In the first paper we looked into why group I introns are so rare in phages related to T4 in spite of the fact that they can spread between phages via homing. We have identified the first phage besides T4 that contains all three T-even introns and also shown that homing of at least one of the introns has occurred recently between some of the phages in Nature. We also show that intron homing can be highly efficient between related phages if two phages infect the same bacterium but that there also exists counteracting mechanisms that can restrict the spread of introns between phages.

In the second paper we have looked at how the presence of introns can affect gene expression in the phage. We find that the efficiency of splicing can be affected by variation of translation of the upstream exon for all three introns in T4. Furthermore, we find that splicing is also compromised upon infection of stationary-phase bacteria. This is the first time that the efficiency of self-splicing of group I introns has been coupled to environmental conditions and the potential effect of this on phage viability is discussed.

In the third paper we have characterised two novel freestanding homing endonucleases that in some T-even-like phages replace two of the putative HEGs in T4. We also present a new theory on why it is a selective advantage for freestanding, phage homing endonucleases to cleave both HEG-containing and HEG-less genomes.

Place, publisher, year, edition, pages
Stockholm: Institutionen för molekylärbiologi och funktionsgenomik , 2004. , 73 p.
Keyword [en]
Bacteriophage, Self-splicing introns, Homing endonucleases
National Category
Biochemistry and Molecular Biology
Identifiers
URN: urn:nbn:se:su:diva-211ISBN: 91-7265-925-4 (print)OAI: oai:DiVA.org:su-211DiVA: diva2:191002
Public defence
2004-09-17, sal G, Arrheniuslaboratorierna, Svante Arrhenius väg 14-18, Stockholm, 12:00
Opponent
Supervisors
Available from: 2004-08-26 Created: 2004-08-26Bibliographically approved
List of papers
1. Distribution, Sequence Homology, and Homing of Group I Introns among T-even-like Bacteriophages: Evidence for recent transfer of old introns
Open this publication in new window or tab >>Distribution, Sequence Homology, and Homing of Group I Introns among T-even-like Bacteriophages: Evidence for recent transfer of old introns
2004 (English)In: Journal of Biological Chemistry, ISSN 0021-9258, Vol. 279, no 21, 22218-22227 p.Article in journal (Refereed) Published
Abstract [en]

Self-splicing group I introns are being found in an increasing number of bacteriophages. Most introns contain an open reading frame coding for a homing endo-nuclease that confers mobility to both the intron and the homing endonuclease gene (HEG). The frequent occurrence of intron/HEG has raised questions whether group I introns are spread via horizontal transfer between phage populations. We have determined complete sequences for the known group I introns among T-even-like bacteriophages together with sequences of the intron-containing genes td, nrdB, and nrdD from phages with and without introns. A previously uncharacterized phage isolate, U5, is shown to contain all three introns, the only phage besides T4 found with a “full set” of these introns. Sequence analysis of td and nrdB genes from intron-containing and intronless phages provides evidence that recent horizontal transmission of introns has occurred among the phages. The fact that several of the HEGs have suffered deletions rendering them non-functional implies that the homing endonucleases are of no selective advantage to the phage and are rapidly degenerating and probably dependent upon frequent horizontal transmissions for maintenance within the phage populations. Several of the introns can home to closely related intronless phages during mixed infections. However, the efficiency of homing varies and is dependent on homology in regions flanking the intron insertion site. The occurrence of optional genes flanking the respective intron-containing gene can strongly affect the efficiency of homing. These findings give further insight into the mechanisms of propagation and evolution of group I introns among the T-even-like bacteriophages.

Place, publisher, year, edition, pages
American Society for Biochemistry and Molecular Biology, 2004
National Category
Biological Sciences
Research subject
Molecular Biotechnology
Identifiers
urn:nbn:se:su:diva-23266 (URN)10.1074/jbc.M400929200 (DOI)
Note
Part of urn:nbn:se:su:diva-211Available from: 2004-08-26 Created: 2004-08-26 Last updated: 2010-01-07Bibliographically approved
2. Self-splicing of the Bacteriophage T4 Group I Introns is Affected by the Growth of the Infected Bacterium and Requires Efficient Translation of teh Pre-mRNA In Vivo.
Open this publication in new window or tab >>Self-splicing of the Bacteriophage T4 Group I Introns is Affected by the Growth of the Infected Bacterium and Requires Efficient Translation of teh Pre-mRNA In Vivo.
Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-23267 (URN)
Note
Part of urn:nbn:se:su:diva-211Available from: 2004-08-26 Created: 2004-08-26 Last updated: 2010-01-13Bibliographically approved
3. Two Genes Encoding Novel Homing Endonucleases Replace the Putative Homing Endonuclease Genes mobC and mobE in Several T4-related Phages.
Open this publication in new window or tab >>Two Genes Encoding Novel Homing Endonucleases Replace the Putative Homing Endonuclease Genes mobC and mobE in Several T4-related Phages.
Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-23268 (URN)
Note
Part of urn:nbn:se:su:diva-211Available from: 2004-08-26 Created: 2004-08-26 Last updated: 2010-01-13Bibliographically approved

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